The Royal Fly Agaric, Amanita regalis (Fries) Michael
a rare toxic mushroom

by Tjakko Stijve

Introduction

The royal fly agaric is such a rare mushroom that the German Mycological Society nominated it Mushroom of the Year 2000. This distinction implies that Amanita regalis is also in need of protection. Indeed, the species occurs only in the natural area of the spruce-fir. It seems to make particular demands from its mycorrhizal partner Picea abis. In new fir woods the mushroom does not grow. It prefers acid soil in hilly country. Both Dörfelt & Conrad (1980) and Otto et al. (1994) review the occurrence of A. regalis in Germany and in some other European countries. The royal fly agaric probably contains the same toxic principle, i.e. ibotenic acid, as A. muscaria and A. pantherina, but this has never been investigated. For this reason, we undertook a comparative study of the toxins contained in the three Amanitas. The results of this study are presented in this paper.

The royal fly agaric in literature

Literature on this particular mushroom was found to be scarce indeed. In modern field guides (Courtecuisse 1994; Bielli 1998; Gerhardt 2000) it is not or hardly mentioned. Even in a classic manual as that of Ricken (1915), the author mentions it only under A. muscaria (no. 925) as the variety regalis, which grows in beech (?) forests. It is described as often twice as big as the normal species, with a leather brown cap, and a scarcely hollow stipe. Ricken also mentions the variety umbrina having an olive-coloured cap with yellow warts. This mushroom should grow in fir woods, where it is often mistaken for A. pantherina.

In Ricken’s time there was still ample confusion in the genus Amanita, as can be illustrated by Michael’s classic Führer für Pilzfreunde in 3 volumes (1918). One is surprised to find there a “Graubrauner Pantherpilz” (the “grey-brown panther-mushroom”, A. umbrina Pers.) described as an edible species. Obviously, the edible A. spissa was then misidentified as A. pantherina.
Moreover, from his descriptions and illustrations it becomes clear that Michael even had difficulties in distinguishing between A. phalloides and A. citrina! The author, however, pays much attention to the royal fly agaric, which he presents under no 75 as A. regalis Fr. He informs the reader that this Amanita is most dangerous, because many cases of poisoning attributed to this mushroom had had a fatal outcome. In a more popular edition (Volksausgabe) of his book with the same title, but having only descriptions of the principal edible and poisonous mushrooms, Michael (1919) still considers the “Königs-Fliegenpilz” dangerous enough to repeat his warning. To distinguish this toxic species from the edible Blusher (A. rubescens), he mentions that A. regalis is characterised by a smooth ring and yellowish flesh under the cap’s cuticle. In a later edition of this popular booklet (1927) which was, after Michael’s death, edited by Roman Schulz, we do not find the royal fly agaric anymore, but a description of A. muscaria L. subspecies umbrina, which is accompanied by the illustration of A. regalis from the older editions! Schulz calls the mushroom now “Brauner Fliegenpilz” (“brown fly-mushroom”); it is still declared poisonous, but apparently not so dangerous anymore as Michael pretended.
Neuhoff (1922) has been the first author who tried to clear up the confusion about the identity of the royal fly agaric. He pointed out that problems had already started with Elias Fries, because the founding father of modern mycology provided only a description of the mushroom, but no illustration. According to Fries, the royal fly agaric grows in beech forests, whereas Michael indicated that it is to be found in fir woods. Attempts to distinguish between an A. umbrina (growing under beech) and an A. regalis (ditto under fir) have not been pursued. Neuhoff suggests that A. regalis is identical with A. emilii, a reddish brown Amanita, which was described in 1907 by P. Riel and named after the French mycologist Emile Boudier. This was confirmed later by Kühner and Romagnesi (1953). In modern European manuals (Dähnke & Dähnke, 1979; Clémençon et al., 1980; Heim, 1984) A. regalis is hardly mentioned, save as a robust brown red variety of A. muscaria growing under conifers in the north of Europe.

Poisoning by A. regalis

We have not been able to find out how Michael (1918) became convinced that the royal fly agaric is a deadly poisonous mushroom. A search in old and modern mycotoxicological literature proved disappointing, since not a single case of poisoning was attributed to this mushroom in the extensive works of Roch (1913), Sartory & Maire (1921), and Heim (1978). The modern compilation of Bresinsky and Besl (1985) devotes one page and a half to A. regalis, but the description is illustrated with a picture of an ordinary fly agaric! The authors warn, just as Michael did, against confusion with the Blusher (A. rubescens), and cite a paper on three cases of poisoning reported by the University Hospital of Helsinki (Elonen et al., 1979), which are interesting enough to be cited here:

• A young woman ate several fried specimens of A. regalis, which she had misidentified as Macrolepiota procera (!). After two hours she turned giddy and became nauseous, whereupon she was admitted in the hospital, where she soon fell into a hallucinatory state, alternated by periods of unconsciousness, which lasted for more than 12 hours. She remained nauseous for another day, but recovered without lasting damage.
• The second patient was an older man who had consumed two cooked A. regalis. First, he vomited during 4 hours, became then mentally confused and hallucinated, but did not lose consciousness. After about twelve hours he recovered.
• The third victim had only eaten a small portion of the poisonous mushroom, which mainly rendered him nauseous.

In the first-mentioned patients cholinergic symptoms such as salivating and profuse sweating were observed, suggesting that muscarine or muscarine-like compounds contributed to the intoxication.

Further literature search yielded very little. Even German publications from the years following World War I, a time of food shortage, and, consequently, of extensive mushroom hunting, do not mention A. regalis. The mushroom was rare then, as it is now. However, in a popular magazine devoted to wild herbs and mushrooms, Der Pilz-und Kräuterfreund, we found a report of a poisoning case in which the culprit probably was the royal fly agaric (Nürnberg, 1922). It was narrated by one of the victims in a letter to the then President of the Berlin Mycological Society. The report is interesting enough to be translated here in extenso, also because the magazine is nowadays hard to find.

A case of poisoning caused by the royal fly agaric, Amanita regalis

In the evening of the 21st September, a beautiful autumn day, my sister and I went for a walk. It had rained during the morning and after a clear up in the afternoon it was really nice walking in the streets of the Westend quarter, where the houses alternate with patches of woodland, often covered by pine trees. Although it had not been our intention to do any mushroom hunting, the warm rain had brought them out, and we could not resist collecting about 1 kg of a mixture of bay boletes, puffballs, big lepiotas and especially Blushers (Amanita rubescens). Near the Reichkanzlerplatz I found near a bush where the soil was poor and trodden an enormous, partly emerged young specimen of a blusher, still mostly white with big warts. I thought it strange that the flesh of this mushroom was so firm, because this is rarely observed in blushers. However, I attributed this to the dry and arid soil.
Back at home I cleaned the mushrooms immediately, and again I wondered about the said Blusher, but since I could not put a different name to this fungus, I also included it in the dish I was going to prepare.
We cooked the mushrooms with groats and it really tasted very well. A lady friend who just dropped by also ate a sizeable portion. After supper, while my sister prepared coffee, I rose from the table and suddenly experienced a strange feeling: I swayed on my legs, but actually had a sensation of well-being. When I told this my sister and suggested the possibility of an intoxication, she answered: “That is nonsense, such a feeling is not unusual at our age. I also feel it, but it does not mean anything.” No sooner had she said this, than the milk jug dropped from her hands. She said quietly: “Strange, my hands are shaking”
Now I really started to get worried. The befriended lady brought us to the Westender hospital which was at 10 minutes walking distance. When we arrived there, my sister immediately lost consciousness. On our way we had already been supporting her, because she stumbled continuously. I had just time to give our names and addresses to the receptionist before passing out myself. What happened after that I do not know. Later they told us that they had pumped out our stomachs.
Between 5 and 6 o’clock in the morning we slowly regained consciousness. At my bed stood a nurse who repeatedly urged me to be quiet, because there were people in the room who were gravely ill. Later I was told that I had continuously shouted a lot of gibberish. Although my sister and I are no sentimental characters, I had continuously assured her of my undying love and affection. Furthermore, I had been raving about the Good Lord who should bring us peace now (in September 1918 the war was still going on) and who would not fail to guard us. When I woke up gradually, I heard myself shouting. My sister who had passed from unconsciousness to a sound sleep, was also awakened by the noise I was making.
Presently, we fully recovered and were much surprised when the nurse asked us if we wanted a room for ourselves. As a matter of fact, we were feeling fine again and wanted to go home. The doctor, however, would not hear of it and declared that we should stay under observation for at least 5 days. He said that we had been in such a bad shape that we probably owed our lives to our speedy arrival at the hospital. As a therapy they had given us caffeine and camphor, and, during the first few days, we only received soup for food.
During our stay, we were several times examined and interrogated, particularly about the species of mushrooms we had eaten. Clearly, the doctors were at a loss to find one that could be responsible for our symptoms. We did not suffer from headaches or stomach cramps, and did not experience such unpleasantness as vomiting or diarrhoea.
We felt rather snug, just as the aftermath of having drunk a bit too much of champagne.
After having left the hospital, I discussed our adventure with the well-known mycologist Michael who suggested that our meal had probably contained a specimen of the royal fly agaric (Amanita regalis). This rare mushroom, especially in its state of early development, can be easily confused with young A. rubescens and our poisoning symptoms also pointed in the direction of that possibility.
However, it remained strange that the friend who had shared our meal had not been affected at all. Michael explained this by assuming that her portion of the meal had not contained any fragment of the poisonous mushroom.
 
Another interesting case happened during the German campaign against Russia in WW II. During autumn 1942 Wehrmacht soldiers gathered and ate what they presumed to be “Perlpilze” (A. rubescens), which resulted in a state of collective drunkenness. This was ascribed to confusion with A. pantherina, but Lendle (1942), who reported on this, did not exclude that the culprit mushroom had been a brown variety of the fly agaric. The symptoms described by this author rather resemble those noted by Frieda Nürnberg and her sister (1922). Since in both cases the responsible mushroom had not been examined by a specialist, it remains uncertain whether these intoxications may be really ascribed to A. regalis. Nürnberg’s report is most interesting, since two persons became gravely poisoned by the presence of a single specimen in a dish of mixed mushrooms.
In a most recent case (Ahnert, 1999) a family of 5 persons in the German Erzgebirge who were looking for “Blushers”, unknowingly also picked some A. regalis. The resulting poisoning brought mother and daughter in a rather confused state of mind, which caused them to talk incoherently, whereas the father and both his sons remained lucid and approachable. After a stomach wash and two days of palliative treatment, the family returned home.

Toxic compounds in the royal fly agaric

The above-mentioned single specimen of an Amanita which brought the two sisters in the hospital must have been extremely toxic. For comparison, it should be noted that experiments with volunteers (Spoerke & Hall, 1990) showed that psychoactive symptoms were only observed after ingestion of 2 – 4 fly agarics. The lethal dose would be no less than 10 or more carpophores (Lincoff and Mitchell, 1977). Since A. regalis is far more toxic, it is likely that it contains more or different toxic compounds than A. muscaria, but no such information is found in the open literature.
In 1993 the author received from Sweden some dried specimens of the royal fly agaric for analysis of muscarine and ibotenic acid. According to the sender (Fonskov, 1993) the collection submitted had caused a most pleasant trip without disagreeable symptoms. Analyses revealed the presence of mainly ibotenic acid with some muscimol and muscazone. No muscarine could be detected. The sum of the isoxazole derivatives was not less than 0.62 %, which is far more than ever reported for a fly agaric (Stijve, 1995). There remained some doubt, however, because A. pantherina also contains much muscimol (Benedict et al., 1966) and no muscarine (Eugster, 1968). Perhaps the Swedish collection was in reality a panther amanita. The question was settled by analysing several dried specimens not only for the said toxins, but also for two characteristic trace elements. The results of this comparative chemical investigation of the three amanitas are given in Table I.

Table 1: Characteristic Toxins and Trace Elements in Three Poisonous Amanita Species

SPECIES	Muscarine in mg/kg on dry matter	Ibotenic acid and muscimol calculated as muscimol in percentage on dry matter	Vanadium in mg/kg on dry matter	Selenium in mg/kg on dry matter
A. muscaria N= 10 (L.:Fr.) Hooker	50 – 110 (~ 80)	0.10 – 0.22 (0.15)	72 – 120 (98)	1.37 – 17.8 (10.5)
A. regalis N= 6 (Fr.) Michael	< 10*	0.10 – 0.62 (0.27)	43 – 67 (58)	1.50 – 12.5 (8.3)
A. pantherina N= 4 (DC:Fr.) Secr.	< 5*	0.19 – 0.31 (0.24)	0.50 – 4.3 (1.65)	0.22 – 1.15 (0.59)

Average values in brackets
*Analysis done on a pooled sample
 
A. pantherina is clearly distinguished from A. muscaria and A. regalis by her low vanadium- and selenium content. The concentrations for both trace elements in the latter two mushrooms are in the same order of magnitude as those reported by Meisch et al.(1977, 1979). Our data for selenium in the fly agaric confirm those of Watkinson (1964) and Stijve (1977). Unfortunately, the high ibotenic acid/muscimol content initially found in A. regalis was not confirmed when analysing three additional Swedish collections from different sites. The concentrations in the latter were about the same as those found in the fly agaric (Eugster, 1968; Stijve, 1982), and well below those measured in A. pantherina (Benedict et al., 1966; Stijve, 1982)
The low muscarine content of A. muscaria (Eugster, 1956) which plays virtually no role in the poisoning syndrome, was confirmed later by Stijve (1981/82). Just as Eugster (1968) we found no muscarine in A. pantherina. It is worth noting that we could not find any muscarine in a pooled sample of A. regalis. If the compound was present, its concentration must have been lower than the limit of determination of 10 mg/kg on dry matter. Other toxins, such as tryptamine derivatives, e.g. bufotenine, beta-carbolines, were also found to be absent.

Conclusion

The royal fly agaric is chemically very close to A. muscaria. Probably, its ibotenic acid/muscimol content is often higher, which would explain the (scarce) reports about its greater toxicity with often emphasis on psychoactive symptoms. Considering that the said iso-oxazole derivatives are not very stable (Stijve, 1982), the concentrations reported here should be interpreted as minimum values. Analyses were carried out on exsiccatae, and losses may have occurred in the drying process. Furthermore, the time between collecting (and drying) of the mushrooms and their chemical analyses was sometimes longer than 6 months. It would therefore be interesting to repeat the study on fresh material, and to include also collections from Germany (Harz, Erzgebirge).
To exclude confusion with other Amanita spp, it is recommended to screen all collections for the characteristic trace elements vanadium and selenium. When analysing for ibotenic acid and muscimol, attention should also be paid to the possible presence of stizolobic acid and related compounds, which were reported by Chilton & Ott (1976) in American varieties of the fly agaric.

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