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Poisonous Fungi and Mycotoxins

excerpts from
Fungi in the Ancient World
published by APS Press

Frank Matthews Dugan
USDA-ARS Western Regional Plant Introduction Station
Washington State University, Pullman, WA

Dugan, F.M. 2008. Poisonous Fungi and Mycotoxins. Online. APSnet Features.
doi: 10.1094/APSnetFeature-2008-0208

Poisonous mushrooms gained notoriety even in antiquity for their part in destroying innocent or not so innocent lives. Especially famous was the reputed poisoning of a Roman emperor. The fungal toxins, and the dishes into which the toxins may have been introduced, have been the subjects of considerable speculation. Some cultures, especially the Greeks and Anglo-Saxons, long retained a suspicion of fungi as foodstuffs. Antidotes against poisoning (mostly emetics composed of pungent substances) were probably effective primarily against early-onset gastrointestinal difficulties. They would have been of little use against the toxic Amanita species, whose symptoms may not appear for several hours after ingestion.

Mycotoxins were a threat in both food and forage. Much has been written in modern times regarding probable connections between mycotoxins and events in medieval, Renaissance, or colonial times, including instances of mass hallucinations, changes in birthrates, charges of witchcraft, etc. The impact of mycotoxins in Europe undoubtedly rose in the Middle Ages, with the spread of cultivation of rye, an excellent host for ergot (Claviceps purpurea). But ancient peoples probably also suffered from ergot as well as from the effects of Fusarium, Penicillium, or Aspergillus mycotoxins and from allergens of common fungi. Dramatic claims have also been advanced to explain several events in antiquity. Some, such as the notion that fungi turned the Etruscans into homosexuals, are best relegated to the realm of unintentional humor, but other claims bear close examination.

The ancients were well aware that foodstuffs, including grains, could become moldy, but they had no notion of microorganisms per se. To appreciate the probable impact of toxigenic microorganisms in the ancient world, it is essential to understand in some detail the norms and limits of ancient storage and transport of grains. What we know of these practices comes partly from historical and archaeological data and partly from modern experimentation that seeks to duplicate ancient storage conditions.

Ancient peoples took deliberate and elaborate measures to exclude moisture and provide adequate ventilation in their granaries because they knew that failure to do so would result in spoilage. Small-scale storage in pits may have sometimes purposely excluded air and succeeded in creating anaerobic conditions for long-term storage, but there are indications that success was mixed. Storage pits in moist climates or seasons were probably common sources of contaminated grain. Modern experiments have shown that toxigenic fungi can be recovered from such pits, and colonization of the grain by such fungi could be extensive. The British in particular have shown an enthusiasm for duplicating the storage methods of their ancestors, sometimes finding so little deterioration that some skepticism seems warranted. Recent findings may dispel modern myths about old crops; for example, the notion that covered wheat (such as spelt, whose hull is retained on the kernel at harvest) is more protected from pathogens than "naked" wheat (such as modern bread wheat, which lacks such a hull on harvested kernels) has been strongly called into question by some modern research.

Documentation: Poisonous Fungi and Mycotoxins

Poisonous fungi. The Greeks and Romans were highly aware that some mushrooms were poisonous (Ainsworth 1986, Buller 1915, Houghton 1885). The Greeks early associated fungi with toxins (e.g., the "evil ferment" postulated by Nicander) and attempted to devise remedies for those who had ingested poisonous mushrooms. Buller relates incidents described in classical Greek literature (Eparchides, Hippocrates) concerning fatal and nonfatal poisonings by fungi. Ainsworth (1993b) credits Euripides with a reference to mycetism (eating a poisonous fungus mistaken for an edible one) killing a woman and her two children. The civilizations of preclassical and classical antiquity were not sufficiently developed scientifically to arrive at consistently useful criteria for distinguishing toxic and edible species.

Remedies were varied, including pungent mustard, bird dung, and vinegar, mixed into various concoctions, several of which were effective emetics (Houghton 1885). Hippocrates and Nicander both provided an assortment of remedies against poisonous fungi, and Celsus, a contemporary of Augustus, recommended boiling fungi with the young twig of a pear tree to free them of toxic properties (Phillips 1982). Dioscorides (first century AD) thought that certain substrata that fungi grew on or near (serpents’ dens, rotten rags, rusty nails, etc.) would make them poisonous and recommended as a cure the usual dose of vinegar and bird dung. Houghton (1885) traced the genesis and transmittal of such ideas throughout ancient commentaries.

Dioscorides and Galen (b. AD 130) had great influence on medical thought up through the Renaissance, including the writings of the herbalists of the sixteenth and seventeenth centuries (Buller 1915). On the whole, Galen took a negative view of fungi in the diet, with the possible exceptions of the meadow mushroom (modern name Agaricus campestris) and Caesar’s mushroom (Amanita caesarea, which is edible but which, because it belongs to a genus with so many toxic species, is best avoided by all but the most expert mycologists). Further excerpts from or summaries of Dioscorides, Celsus, Pliny, and Galen are provided by Phillips (1982), and Buller (1915) briefly references Roman writers of the second and third centuries AD who documented cases of poisoning by fungi.

Let us turn now to the deliberate use of poison in dishes containing edible fungi (boleti), allegedly the means by which Agrippina rid herself of her troublesome husband, the emperor Tiberius Claudius. Because Roman emperors of that era were deified when deceased, Nero, the son of Agrippina and Claudius, later quipped that mushrooms were the food of the gods (Grant 1970). A similar incident at a banquet at which mushrooms (edible suilli) were served ended the life of Annaeus Serenus, the prefect of Nero’s guard. For the death of Claudius, Graves (1958) blamed "juice of the lethal amanita phalloides, added to the amanita caesarea, an edible mushroom of which Claudius was extravagantly fond." However, some writers believe that the feast that killed Claudius was based on poisonous Amanita species. Molitoris (2002) seems to echo this view, and Grimm-Samuel (1991) vigorously defends it. Grant (1975) also seems to subscribe to this notion, adding that "accidental loss of life frequently occurs in Italy due to confusions between the harmless mushroom boletus edulis and the fatal amanita phalloides." But this degree of confusion seems unlikely, given that B. edulis has a hymenium of pores, whereas A. phalloides is a gilled mushroom. It is much more likely that young A. phalloides might be mistaken for immature edible A. caesarea. (The account given by Toussaint-Samat [1992] should be disregarded, as it confuses A. phalloides with A. muscaria and moreover misapplies the common name "Caesar’s mushroom" to A. muscaria.)

Poisonous fungi were actually only a small part of the arsenal of drugs and poisons employed in ancient Rome (Cilliers and Retief 2000). And despite multiple commentaries from ancient and modern sources implicating poison, usually from mushrooms, Marmion and Wiedemann (2002) argue that Claudius was not poisoned at all, but simply suffered "sudden death from cerebrovascular disease."

Mycotoxins. Most approaches to assessing the potential impact of mycotoxins in antiquity are indirect. They involve the appraisal of ancient storage practices, experiments conducted under conditions replicating these practices, experiments with plant taxa known as ancient crops, certain findings pertinent to other microorganisms or ancient insects, and occasional references to possible symptoms of mycotoxicosis in the writings of ancient peoples. Direct mentions of mycotoxins in the writings of ancient peoples are, not surprisingly, very rare, but Galen stated that black wheat (probably smutted or rusted grain) is less harmful than ingestion of darnel (tares), a Lolium species infected with toxin-producing fungus (Aaronson 1989).

The fungi that produce mycotoxins did not originate with storage of grain by humans and probably have an extremely ancient history in seeds stored by rodents or other animals (Hawkins 1999, Smith and Reichman 1984). However, it is likely that conditions of food storage by humans from the Neolithic onward were sometimes conducive to such fungi. This is the stated assumption of Wijbenga and Hutzinger (1984), who note the potential for chronic effects from mycotoxins in early agricultural societies but provide concrete examples of such effects only from medieval or modern periods. (Other writers have speculated freely about such effects in classical and Biblical antiquity, as documented below.) Sprouted grains from ancient stores excavated in Armenia and dated to the third millennium BC showed that wheat was sometimes wet going into storage or that storage conditions became moist (Gandilian 1998).

Indirect evidence that storage fungi might have invaded ancient grain stores comes from detection of tetracycline (a product of Streptomyces and other actinomycetes) in bone tissues recovered from ancient burials. Mills (1992) discusses the plausibility that ingestion of Streptomyces-contaminated grain was responsible for the tetracycline and draws inferences about grain storage conditions in ancient Egypt and Nubia. If conditions were favorable for the growth of actinomycetes, it is plausible that fungi may also have grown in similar circumstances. [Some ongoing research uses similar principles to attempt to distinguish between wild and domesticated animals. Assuming domesticated animals were sometimes fed stored grasses and grains, the presence of tetracycline in excavated bone tissues may indicate domestication, and inversely, the absence of tetracycline could indicate that the animal was not domestic (H. P. Schwarcz).]

The presence of fungi can plausibly be inferred from the presence of certain arthropods as well as from the presence of other microorganisms. That stored cereals and legumes were attacked by insect pests, both those from the field and those more specialized as storage pests, has been documented for Bronze Age Santorini, an island in the Aegean and site of a massive volcanic eruption that preserved by burial many artifacts (Panagiotakopulu and Buckland 1991). Other documentation is available for Egypt and Roman Britain (Buckland 1981). Panagiotakopulu and Buckland (1991) make two points pertinent to the topic of fungi: that many of the insects identified from these ancient stores were likely the result of transport by humans along with seeds, and that extensive insect infestations promoted toxins from microbial infestation. Transport by humans in stored grain is also the most plausible reason for the appearance of certain insect pests in the archaeological record of the Roman period and preceding times, and damage by such insects is correlated with damage from toxic microflora (Buckland 1981). These are not just speculations; according to Christensen (1973), for example, "infestations by weevils and mites are almost inevitably accompanied by storage fungi." Indeed, even Theophrastus (1916b, trans. A. Hort) noted that rot of seeds was correlated with insect activity: "As seeds decay . . . they engender special creatures" and he mentions grubs, worms, etc. And Columella (1941a, trans. H. B. Ash) had much to say about mustiness and weevils in grain. Although insect pests have been documented in grain stores as far back as the Neolithic, these insects may not really have functioned as economic pests until grain was stored and/or transported on a large scale, perhaps by the Middle Bronze Age (Valamoti and Buckland 1995). Caution is essential in reviewing some aspects of the archaeoentomological literature, as some specimens identified as indigenous to a substratum, e.g. Lasioderma serricone in Egyptian tombs, are actually intrusive (Chaddick and Leek 1972, Kislev 1991).

Although most of the references cited here pertain to mycotoxins in grain or animal fodder, mycotoxins (especially ochratoxin A) are also important in wine. As noted in the sections above on fermented beverages, wine was a staple throughout much of the ancient world. Even in modern times, wines (especially red wines) are sometimes contaminated with ochratoxin A, especially when grapes have been grown in hot climates such as the Mediterranean region (Battilani and Pietri 2002). Species of Aspergillus and Penicillium are the fungi primarily responsible. It seems quite likely that similar or higher levels of contamination occurred in ancient times. Although many ancient wines were resinated, retsina wines do not appear to be resistant to production of ochratoxin A (Stefanaki et al. 2003). Moreover, although mycotoxins are most well known from their occurrence in cereal grain, they can also contaminate other stored solid foods. Flint-Hamilton (1999) speculates on the role of mycotoxins in lentil and bitter vetch in classical antiquity, citing some observations of Theophrastus in this regard.

Ancient Historical Events Speculatively Attributed to Mycotoxins

Bellemore et al. (1994) give a detailed and speculative account of one spectacular and, if true, historically significant episode of mycotoxicosis. They analyzed Thucydides’s History of the Peloponnesian War in detail with regard to the timing, symptoms, and circumstances of the great plague of Athens during the Peloponnesian War. They conclude that the plague was not, in fact, a contagion but was plausibly induced by Fusarium-molded wheat, with symptoms of mycotoxicosis closely matching those of alimentary toxic aleukia (ATA). Arguments in favor of the hypothesis include that because Athens was under siege, the primary foodstuff for the upper classes (who were very disproportionately affected) was wheat imported from the Black Sea area. The wheat was described by another historian, Diodorus Siculus (12. 58. 3-5) as bad. That the besiegers did not contract the plague is additional evidence. ATA is known as endemic to grain-producing areas of Russia and Ukraine to the present day. Grain from southern Russia was widely imported throughout the Mediterranean in Hellenistic times and later (Grant 1970, Rostovtzeff 1941). Schoental (1994) also points to the plausibility of mycotoxins with regard to the plague at Athens. Salway and Dell (1955) proposed that ergotism was the cause of the plague. It should be noted, however, that literature speculating on the plague of Athens is abundant, and there are indeed references to the plague acting as a contagion (e.g., Thucydides himself attempted to explain how the plague traveled to Athens, and soldiers at the siege of Potidaea were said to have contracted plague from Hagnon’s expeditionary force). But most sources have noted that it was not highly contagious; e.g., Cruse (2004) describes it as "contained" and "local."

In another highly speculative approach, Schoental (1984) gives some evidence from the Book of Job in favor of an etiology involving mycotoxins in the sufferings of Job. Schoental (1980) had previously argued that Mosaic dietary prohibitions "appear now as if . . . designed for protection from mycotoxins." Schoental (1991) also proposes a role for mycotoxins in the decline of the Etruscans. The hypothesis involves toxic metals as well as toxic fungal metabolites, with an eventual effect on the sexual organs and sexual orientation of the Etruscans, resulting in decline vis-à-vis the increasingly powerful Romans. This latter hypothesis has been discounted by Spivey (1996). Yiannikouris and Jouany (2002) briefly note the above accounts on Athens and the Etruscans in their review of mycotoxins in feeds. Schoental (1987) also considers the impact of mycotoxins on the lifespan of individuals in the Bible, arguing that mycotoxigenic fungi flourished in the moist environments after Noah’s flood. Before this event, individuals such as Adam, Methuselah, and Noah had ample lifespans of greater than 900 years, but after the flood persons went to their graves after a trifling 150 to 400 years or so. Schoental carefully documents the lifespan statistics with verses from Genesis. This particular hypothesis from Schoental is creditable only in the context of Biblical literalism.

Another attempt to explain Biblical events by reference to mycotoxins is that of Marr and Malloy (1996), who postulate that exposure to Stachybotrys atra (a strongly toxigenic fungus) might provide a rational explanation for the tenth plague of Egypt (death of the firstborn) as recounted in Exodus. Essentially, the argument is that the Egyptians responded to the prior disasters by hoarding damp grain, which became contaminated with mycotoxins. The eldest children, receiving preferential treatment in such times, would have received the most food and thus the highest dose of trichothecene mycotoxins. Schoental (1980) also mentions the possible relevance of mycotoxins to the Biblical plagues of Exodus and the Pentateuch.

It is difficult to find direct evidence for impacts of T-toxins (trichothecenes), fumonisins, or ochratoxin on ancient peoples, although the above review makes it plausible that negative effects sometimes occurred. There is, however, some evidence for effects from toxins derived from Claviceps species, especially C. purpurea, cause of ergot. (See also Fungi as "Entheogens.") Brothwell and Brothwell (1969) note that the better-documented ravages of ergotism in the Middle Ages strongly imply analogous negative impacts in antiquity. They mention (without attribution) Babylonian and Assyrian tablets alluding to "noxious grasses" and "noxious pustule in the ear of grain," respectively. The allusion to "noxious pustule" has also found its way into the literature on mycotoxins (Bennett and Klich [2003], citing Hofmann [1972], who also wrote of the "noxious pustule" without attribution). Brothwell and Brothwell also point out probable allusions to ergot in Theophrastus, Hippocrates, Pliny, and Galen, but state that the first clear account of ergot was given by the Perso-Arabic physician Muwaffak (AD 950). Carefoot and Sprott (1967) disagree, writing that ergotism was probably absent from ancient Mediterranean civilizations before invading barbarians (Franks, Vandals) brought rye (and with it, ergot) during their incursions into Roman territory. Matossian’s (1989) masterful study of ergotism does not much explore times prior to the Middle Ages, but she states (without attribution) that in Roman Gaul the ruling classes preferred wheat to rye and that even in that era, people were aware that ingestion of rye could be hazardous. Gangrene of the extremities is among the possible symptoms of ergot poisoning, and "Galen spoke of coloured grain causing something like gangrene" (Aaronson 1989). Verster (1976) argues that miscellaneous descriptions of psychosomatic disturbances in classical mythology and literature are in accord with symptoms of ergotism.

Ergot and ergotism are most closely associated with rye (Matossian 1989), and although rye is attested early in the archaeological record in the ancient Near East and eastern Europe (Zohary and Hopf 2000), its cultivation was not widespread in antiquity, except perhaps in some northerly regions. However, weedy forms were prevalent and admixed with other cereal crops (Zohary and Hopf 2000). Zohary and Hopf also report convincing excavations of rye from Neolithic sites in Poland and Romania and from Bronze Age sites in the Czech Republic and Slovakia. Aaronson (1989) compiled records of Neolithic, Bronze Age, and Iron Age sites from which C. purpurea sclerotia were recovered in excavations in Poland, Scotland, Germany, Sweden, and Denmark. The fungus was found in association with rye, wheat, barley, and wild grasses. Dark and Gent (2001) cite further instances of ergot sclerotia recovered from ancient sites in the Netherlands and elsewhere and note that sclerotia were found in the stomach of one of the "bog bodies" from the Danish Iron Age (citing Helbaek 1958). The recording of ergot sclerotia in the digestive tracts of bog bodies has produced an apparent controversy over whether such persons were drugged before their demise (Fischer 1987).

References are provided in the book "Fungi in the Ancient World," available from APS Press.