Bracken adaptation mechanisms and xenobiotic chemistry*

As opposed to animals, plants have to cope with the resources, environmental restrictions, herbivores, and pathogens they find in the particular spot where they are bound to grow. Hence, resource sequestration, predation and competition relationships, and adaptation to various sources of other environmental stresses and their seasonal variation must be flexible enough to ensure survival and successful reproduction. Plants express this fitness by a combination of biological traits and chemical arsenals which operate under the reign of a genome of considerable plasticity. For the great majority of plants it is either the biological characters or the chemical composition that are explored independently to understand their fitness. But only in a few instances is the combination of these two avenues examined jointly. The extensive studies on the ecology, chemistry, and toxicology of bracken (Pteridium aquilinum) make this fern one of the few examples where a reasonable explanation for its extraordinary success is beginning to emerge by the combined perception of these two most important aspects of plant life. It is the purpose of this article to briefly review how the sum of biological and chemical traits cooperates to make of bracken one of the five most pernicious weeds in the world today. BRACKEN ENCROACHMENT Bracken in its 12 different genets is a cosmopolitan heliophile fern growing in all five continents. Only the northern tundras, large deserts, and climatic forests are exempt of its great invasiveness. In the Americas, Chile is the only country where bracken is, curiously enough, not found. Possibly the barrier of the great Andean chain, the northern deserts, and the prevailing easterly winds from the Pacific Ocean block spore dispersal from existing stands in Bolivia and Argentina. The neotropical varieties of bracken, caudatum and arachnoideum, are altitudinally distributed to allow its growth from the sea level to the Andean periglacial zone, over 3200 m above sea level and well beyond the tree level. This is only possible if considerable genetic plasticity, residing in 104 chromosomes in the haploid genet, assists in providing the required adaptation mechanisms. Pteridium grows in dense thickets that frequently exclude other vegetation and cover vast expanses, sometimes with devastating economic consequences. Critical farming conditions due to bracken encroachment have been recognized in several countries including the British Isles, parts of Eastern Europe, New Zealand, Australia, various Asian countries, Central America, northern South America, Brazil, and Argentina. It not only grows ferociously but it is also intensely toxic to many vertebrates counting farm animals. In particular, cattle and sheep herds are deeply affected by the ingestion of this plant. Among the recorded diseases are severe disruption of blood cell counts, bone marrow degradation, and cancer of various internal organs. Animals usually do *Lecture presented at the 22 IUPAC International Symposium on the Chemistry of Natural Products, São Carlos, Brazil, 3–8 September 2000. Other presentations are published in this issue, pp. 549–626. †Corresponding author: E-mail: [email protected] not recover and die [1]. Insects do not fare better since few species exploit the fronds as source of food and protection, and only in South Africa have been arthropods identified as bracken specialists [2]. Yet they do not imperil the survival of the plant. The question arises as to what components of bracken complex natural life are responsible for this great ecological success. Chemistry undoubtedly must play a role, but not alone. BRACKEN SEXUAL AND ASEXUAL DOMINANCE Bracken produces a prodigious number of microscopic spores, albeit variably from year to year, which may amount to 10 g per frond in the arachnoideum variety, or more than a billion particles. The spores are carried long distances by wind or animals that stray into the thickets. Although the germination rate of these spores is low, it is sufficient to colonize effectively new denuded territory [3]. The chemistry of spores remains unknown but toxicological evidence indicates that they contain xenobiotic material [4]. Bracken spores constitute a rare vacant niche, e.g., there are no known exploiters of this proteinrich resource [5]. Being a fern, P. aquilinum is a rhizomatose plant. This robust underground system, comprising up to 79.8% of the live biomass and 5648 ± 390 kg/hectare (arachnoideum) [6], is not only long-lived, lasting perhaps several hundred years, but also provides various advantages over seed-based plants of the early succession. It stores nutrients that become readily available for new frond growth that develop quickly earlier than other seedlings. By piercing the soil deep underground the rhizome finds protection from wildfires. As a consequence, new blades sprout only days into the new succession at a fast pace to cover rapidly the available space. We have estimated the rate of elongation of rhizomes in a tropical habitat at 4.2 m/year, and a maximum blade growth at 56.7 kg/Ha/day on day 28 [7]. From the time croziers first emerge from the bare soil, around 17 days, to space saturation (100% area coverage) it takes less than 90 days. Blade maximum expansion is attained after only 35–45 days through four phenological stages. A fifth stage ensues in which tissues harden by accumulation of lignin and thickening of cell walls of cholenchyma and sclerenchyma. Although fronds usually wither after three to five months of emergence, they remain standing, thus blocking light and forming a dense canopy, while rhizomes live for many decades. Hence, bracken displays advantageous traits both proper of pioneer species and of the old succession. Xenobiotic materials In order to assess the role played by secondary metabolites in plant fitness it is essential to determine quantitatively the contents and variation of these compounds, either as chemical class or individually. For example, there are five phytoecdysteroids in Pteridium with powerful hormonal effects on insect ecdysis. However, these are present in lower quantity than required to cause any molting disruption in attacking arthropods – up to 53 μg/kg fresh weight [8]. Radical changes in bracken’s secondary chemistry occur during growth [9]. We have examined quantitatively the systematics of key xenobiotics— low molecular phenolics, polimeric tannins, prunasin, a cyanogenic glycoside, and illudanes—during frond development in neotropical Pteridium where insect pressure is high and there is no winter growth diapause. We observed that they appear to complement each other, perhaps under metabolic restriction and environmental necessity. Phenolics and tannins Generally considered effective protectants against herbivory, flavonoids and phenolic acids among the low-molecular-weight derivatives and polymeric proanthocyanidins accumulate in bracken fronds as these grow. Values range from 4.98 ± 1.02 mg of salicilic acid equivalents per g of biomass (gb) in stage I to 21.27 ± 4.62 mg in stage IV for simple phenolics and 6.68 ± 3.0 to 32.38 ± 9.20 mg of tannic acid equivalents/gb, respectively. In places of high solar radiation such as the high tropical Andes, proanM. E. ALONSO-AMELOT et al. © 2001 IUPAC, Pure and Applied Chemistry 73, 549–553 550