PHYTOTOXINS NEW PROBLEMS IN FORESTRY?

PHYTOTOXINS have not received much attention from forest soil scientists or tree physiologists. The subject probably is unfamiliar to many practicing foresters. However, the basic idea that some trees or plants may produce substances which inhibit growth of other vege-tation is not new. People working in agriculture and plant physiology have considered such possibilities for more than a century. In 1832 DeCandolle observed that certain species appeared to inhibit growth of associated species and suggested that toxic substances were involved (12). Shortly thereafter, the toxin theo-ry became less popular and most adverse plant growth interactions were interpreted in terms of nutrient bal-ances (6). Interest in toxic substances was not rekind-led until the early 1900's when organic toxins were isolated from a number of soils by USDA scientists (31, 33, 34). However, sufficient evidence to conclude that phytotoxins can play important roles in develop-ment of vegetation did not accumulate until the 1950's and 1960's.

Today there is little doubt that in certain situations organic substances produced by plants must be consid-ered in managing agricultural and horticultural crops. How common or how important phytotoxic substances may be in timber production is in question, but recent work has suggested that we should not ignore this possibility. This paper reviews some aspects of the phytotoxin theory and cites some specific cases of phytotoxic effects of woody plants.

Nature of Phytotoxins First of all, what are phytotoxins? They are plant-

produced growth substances released to the environ-ment which in small concentrations inhibit germination and growth of higher plants. Phytotoxins found to be ecologically important commonly fall into five chemi-cal classes:

1. Phenolic acids have been isolated from a num-ber of soils and plant tissues. Those believed to be associated with phytotoxic activity include p-hydroxy benzoic, gentisic, benzoic, salicylic, ferulic, and cinna-mic acids.

2. A ldehydes-Salicylaldehyde was one of the tox-ins isolated in the early work at the Bureau of Soils and is one of the most toxic. Other toxic aldehydes are benzaldehyde and vanillin.

3. Coumarins include coumarin, esculetin, and sco-poletin.

4. Glucosides include several of the phytotoxins of proven importance in woody plants. Juglone, the potent inhibitor of walnut, occurs as a glucoside in plant tissues which is readily hydrolyzed, then oxidized

THE AUTHOR is research forester, Southeast Forest Exp. Sta., Forest Serv., U.S. Dep. Agr., Charleston, S. C. Paper presented at Forest Soils Workshop, SAF Annual Meeting, Miami Beach, Fla., October 14, 1969.

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to juglone upon contact with air. Amygdalin and phlorizin, constituents of the bark of peach and apple roots, are glucosides which yield toxic products follow-ing transformation or decomposition by soil microbes. These toxins are involved in problems of replanting fruit orchards.

5. Terpenes-Recent work by Muller and his co-workers (9, 22, 24, 25) has indicated that terpene compounds such as camphor, cineole, and a-pinene may be involved in phytotoxic effects of certain woody plants in the mediterranean climate of southern Cali-fornia.

How Phytotoxins Enter the Environment All plants contain compounds which are capable of

inhibiting growth if present in certain concentrations. However, release to the environment is a prerequisite for phytotoxic activity. Most workers believe that important phytotoxins are metabolic by-products or secondary metabolites and that plants must by some means prevent a build-up of such substances in their tissues (22, 26). The manner and rate at which the plant produces and releases such by-products will determine whether or not they are important ecologi-cally. Phytotoxins are released through ( 1) decom-position of residues, and (2) excretion from various organs of living plants.

Decomposition of residues may release phytotoxins in certain cases (18, 27, 28). Many plants retain metabolic by-products in their tissues by a type of "local excretion" into vacuoles and cell walls (30). Toxic substances may be thereby rendered insoluble or nontoxic, or be incorporated into structural materials as is the case with lignin and flavonoid compounds.

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These substances may be rendered toxic once again and released during microbial decay processes. Pos-sible sources of phytotoxins resulting from microbial breakdown include forest litter, logging slash, and residual stumps and roots.

In other cases, accumulation of metabolic by-products is avoided by external excretion through roots ( 4, 5), leaves (36, 37), and possibly bark. When this occurs to any great extent, chemical interactions be-tween living plants are possible. Mechanisms for re-lease and removal of phytotoxins from living plants include crown leaching by rain or fog drip (9, 36, 37), volatilization from leaves (24), root exudation ( 4, 5), and branch and stem flow.

How Environment Affects Phytotoxins

Although many species produce and release sub-stances with potential growth regulating properties, few seem to have phytotoxic effects on other plants. The substances often do not persist long enough to accumu-late to toxic concentrations. Environment exerts great influence through effects on persistence and accumula-tion of toxins in the soil. In most cases where phytotox-ins have been shown to be associated with decreased germination or growth, soils are characterized by heavy texture, poor aeration, excessive moisture, and often cool temperatures (17, 21, 32, 35). Under well-aerated and well-drained conditions, many phyto-toxins resulting from both plant excretion and residue decomposition are rapidly metabolized by microorga-nisms into nontoxic forms (29). Where oxygen is limit-ing, organisms are lower in number and activity and such toxic substances persist. Soil colloids may be involved also in adsorption and retention of certain toxins (22). However, these are generalizations and certainly do not apply in all cases. Recent and current work by Muller (personal communication) has shown that different classes of phytotoxins persist optimally in different soil types.

Mechanisms of Phytotoxin Action A wide range of injurious plant effects presumably

are due to action of phytotoxins. This includes delay or complete inhibition of seed germination, general reduc-tion in growth, root injury, and wilting. Until recently, little work had been done 'to determine the mecha-nisms through which toxic substances exerted these general effects.

Soil scientists may be interested in the possibility that phytotoxins affect mineral nutrition. Buchholtz ( 7) found that corn grown in association with quack grass suffered from severe nitrogen and potassium deficiency ( even when fertilized). This was due to impaired ability to absorb nutrients when roots are in contact with quack grass infected soil. Reduced respi-ration and interference with ion absorption mecha-nisms, perhaps due to toxic substances, were suggested as possible causes.

Numerous cases are known where phytotoxins pro-duced by a given species act selectively; that is, they affect one species more than another. The phytotoxins of Salvia (14), Ailanthus (20), and Juglans (19) have been demonstrated to affect certain species more

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than others. Although no literature is available on causes for selective action of phytotoxins, such selectiv-ity could be due to differences in uptake, translocation, and chemical alteration of the substance in acceptor species. Such differences in response are known to be associated with the selective action of synthetic herbi-cides (J ).

Reports of Phytotoxic Effects of Woody Plants

Let us now consider some examples of phytotoxic activity in woody plants. Perhaps the best known report is that of juglone produced by black walnut. Roots (8), bark (19), and leaves (3) probably con-tain the substance. Leaching of juglone from leaves by rain is thought to be the main cause of growth inhibi-tion commonly found beneath walnut trees (3).

Concentrated work has also been done on phytotox-ic substances associated with peach (27), guayule (5), Encelia (13, 38), and Artemisia (2, 11). Many other reports are based on field observations followed by little or no greenhouse and laboratory work, or on the inhibitory effects of plant extracts with no follow-up testing in the field. A condensation of such reports is available from the author.

In the last decade, considerable work has been done on a few species which appear to influence vegetation development in forests and rangelands. For example, Jameson (J 6, 17) found that growth of blue grama in Arizona rangelands was reduced in the presence of juniper trees. This inhibitory effect of juniper on her-bage growth was most pronounced on heavy clay soils which were poorly drained and poorly aerated. Labo-ratory assays indicated that substances contained in juniper litter were involved. The active growth-inhibiting substances were found to include polymers and monomers of leucoanthocyanidins or catechins, plus another unidentified compound.

Muller and his students have done intensive work in the chaparral-grassland types of southern California (22, 23, 24). Salvia shrubs form small thickets dis-persed throughout native, uncultivated grassland. Her-baceous vegetation is often absent b~neath the shrubs and within a 6-foot radius of the shrub crowns. Though annuals become established beyond 6 feet, they are usually somewhat stunted; normal grassland development does not occur closer than 20 to 30 feet from these shrubs. Muller has shown that volatile terpenes are produced by Salvia. Inhibition of nearby grassland species presumably is due to these terpenes, especially camphor and cineole.

Vegetation development in Eucalyptus communities near Santa Barbara, Calif. has been studied by del Moral and Muller (9, JO). Volatile terpenes, fog drip from foliage, and litter leachates were involved in the absence of understory vegetation beneath canopies of Eucalyptus globulus. The same holds true for E. camaldulensis, except that fog drip is not a factor. Water soluble phenolic acids were isolated from fog drip and litter leachates. These included chlorogenic, p-coumaric, gentisic, ferulic, gallic, and caffeic acids. Inhibition beneath Eucalyptus was most extreme on heavy clay soils and absent on sands ( del Moral, personal communication).

JOURNAL OF FORESTRY

Such effects are not limited to arid regions of the West. A case of understory inhibition has also been reported in the humid southeast. Three years after a seed-tree cutting, Hook and Stubbs (15) noted that development of reproduction appeared to be retarded under oak seed trees, particularly cherrybark oak. Areas surrounding most seed trees of other species had experienced the tremendous burst of vegetative growth which normally accompanies harvest cuttings in fertile bottoms of coastal South Carolina. Hook and Stubbs suggested that root exudates or crown leachates might be causal factors. Subsequent work by the author which will be published elsewhere indicated that a phytotoxic substance leached from oak crowns was involved. Inhibition beneath cherrybark oak also is most pronounced on soils which are heavy-textured and poorly drained. Where soils are light-textured and sites are well-drained, inhibition is less evident and sometimes absent.

Conclusion Does this mean that foresters should consider phyto-

toxins in the management of forests and forest soils? Work on phytotoxins to date in most timber types is inadequate to answer this question decisively. Howev-er, emphasis on biochemical aspects of physiology and ecology of major species is increasing and it seems likely that other species will be found which release significant amounts of growth substances into the envi-ronment. On certain sites, conditions may be such that these substances may persist and exert effects on other vegetation-possibly stimulatory as well as inhibitory. Effects and possible management uses of subtle factors of this nature should be evaluated if foresters intend to optimize productivity on forest lands.

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