Trip to Smurf Village: "Amanita muscaria"

Besides being a toxic and psychoactive fungus belonging to the Amanita genus, the presence of Amanita muscaria traverses the realms of science, pop-culture, and even spiritualism. On top of having symbiotic relationships with multiple types of plant species, Amanita muscaria's biochemical properties, its role as a bioindicator for soil contaminants, and its intricate connection with fungal nutrition provide insights into the adaptability and significance of this intriguing organism. The investigation further examines the cultural narratives surrounding A. muscaria, spanning from its spiritual roles in ancient rituals in Central Asia to its contrasting perception in medieval Europe, marked by associations with witchcraft. The mushroom's iconic status in popular culture is depicted in art, literature, and media including the Smurfs and Secret Santa, underscoring its enduring allure and symbolic representation of magic and enchantment.

Figure 1: "Amanita muscaria" (photo from Shutterstock).

Classification and Morphology

Amanita muscaria, commonly referred to as the fly-agaric or fly Amanita is a toxic and psychoactive fungus belonging to the Amanita genus. It belongs to basidiomycetes that form specialized reproductive structures called basidia,  producing large fruiting bodies released during the fruiting season, typically following rainfall. Prevalent in temperate and boreal regions of the Northern Hemisphere, it has been introduced to various countries in the Southern Hemisphere, often forming symbiotic relationships with pine plantations, making it a globally distributed species (Amanita muscaria, n.d.). So, during the introduction of this ectomycorrhizal fungus, it forms associations with native species and is transported with its symbionts such as "Angiospermae trees like Betula, Castanea, Cistus, and Quercus, as well as coniferous trees such as Abies, Picea, and Pinus" (Catalfomo, 1970).  In acidic soil conditions, the mushroom plays a vital role in plant nitrogen uptake through a high-affinity ammonium importer gene and mycorrhizal symbiosis.

At various stages of growth, it appears as clusters of mushrooms with a bright red cap (although it might diminish due to biotic and metabolic reasons) and yellow-white freckles, just like Smurf houses! These freckles are actually the remnants of the result of the rupture of a membrane that encloses the entire young mushroom, the universal veil. The gills and the spore sprint appear white and the spores are referred to as inamyloid (no color change when iodine is applied for classification) (Bains et al., 2021). The gills of the mushroom is not joined to the stem and it has with a bulbous volva.

Figure 2: "A. muscaria" cap development (photo from Galloway Wild Foods).

Fungi developed a mechanism to optimize nutrient utilization from a combination of organic compounds and inorganic substances, employing activation and repression of genetic networks. It is crucial to note that fungi cannot undergo an increase in their dry weight in the absence of organic food materials. The reason behind this limitation lies in their inability to photosynthesize or employ carbon dioxide to synthesize organic food materials, primarily due to the lack of chlorophyll. Consequently, they are categorized as heterotrophic for carbon, meaning that they rely on external sources of organic compounds for sustenance. Such a regulatory system allows fungi to tightly control metabolic pathways, effectively distinguishing between preferred nutrients that demand minimal energy and resources for utilization, and non-preferred nutrients that involve more energy-intensive catabolic processes. This evolutionary adaptation ensures the efficient allocation of resources, allowing fungi to thrive in diverse environmental conditions by strategically responding to the availability and biochemical nature of nutrients in their surroundings.

Fungal nutrition in A. muscaria occurs through absorbotrophy, where the mycelium absorbs nutrients from the surrounding aqueous film. The composition of the mushroom, including amino acids and sugars, is influenced by the topsoil type. So, A. muscaria serves as an effective bioindicator for soil contaminants, accumulating heavy metals like Hg, Cd, K, Rb, and V. The mushroom maintains consistent absorption of stable compounds over time, although certain metals exhibit variations between younger and mature fruiting bodies, indicating discontinuous absorption processes. In the case of radioactive cesium, the concentration of the 137Cs isotope varies with the developmental stages of the mushroom (Catalfomo, 1970).

Biochemical Properties

Psychedelics, also known as serotonergic hallucinogens, are potent psychoactive substances that may induce alterations in perception, mood, and various cognitive processes. Importantly, these substances are generally regarded as physiologically safe, meaning they do not pose significant risks to the body's physical health (Nichols, 2016). Psilocybe is a genus of fungi known for its hallucinogenic properties, and these mushrooms are commonly referred to as "magic mushrooms". When consumed, these compounds interact with serotonin receptors in the brain, leading to alterations in perception, mood, and cognition. A. muscaria differs from Psilocybe regarding the active compounds, physiology, geographical distribution and cultural significance.

Figure 3: Main compounds found in "A. muscaria" (Carboué& Lopez, 2021).

The primary psychoactive compounds found in A. muscaria are ibotenic acid, muscazone, and muscimol. When consumed, the mushroom induces a state similar to alcohol intoxication, known as the "pantherina-muscaria" poisoning syndrome (Meyer & Quenzer, 2005). The concentration of psychoactive substances can be reduced by a common practice, peeling the cuticle before consuming the mushroom. The most recently identified active substances in A. muscaria belong to a category of isoxazole derivatives. These compounds were simultaneously discovered and isolated by Takemoto and Bowden, with their attention drawn to the fly-killing properties exhibited by these compounds—a characteristic historically associated with A. muscaria, also mentioned in the common names of this mushroom (i.e. the fly-agaric). Studies like these underscore the diverse paths researchers can take to uncover and comprehend the properties of naturally occurring substances, even when the initial focus is on different aspects of the organism's behavior or effects on human metabolism (Catalfomo, 1970).

Figure 4: Muscimol in fly agaric (photo from Depositphotos).

Cultural Significance

The utilization of A. muscaria transcended the earthly realm and found its place in the spiritual landscape of ancient India. Within the sacred Hindu text, the Rigveda, a reference exists to a divine substance known as "Soma", portraying it as a multifaceted entity, embodying the divine as a god, the botanical realm as a plant, and a potent intoxicating brew. While the exact identity of Soma remains shrouded in the mists of history, some scholars propose a compelling connection with this species, given its known psychoactive properties. Within Celtic mythology, a fascinating association emerges between the iconic fly-agaric and the revered goddess Brigid, recognized as the goddess of prophecy and healing in Celtic lore, held a significant place in the spiritual beliefs of the ancient Celts, often invoked for protection during times of war and upheaval (Winkelman, 2022).

In central Asia, shamans engaged in unique practices to harness the power of fly-agaric mushrooms in red coats and pants, accented with white fur on collars and cuffs and completed with black boots. Carrying them in a sack, the shaman, upon returning to the village, entered the yurt—a portable tent dwelling—through the smoke hole on the roof. This entrance bears a resemblance to certain familiar tales, including Santa Claus. During the ceremonial rituals, the shaman not only consumed the fly-agaric mushrooms but also shared them with the participants. The smoke hole served as a symbolic gateway or portal into the spiritual realm, where those partaking in the ritual experienced profound visions (Ramírez-Terrazo et al., 2021). Among the Sami (Laplander) people, the hallucinatory effects of the fly-agaric mushrooms led to sensations of flying in a "spiritual sleigh," often drawn by reindeer or horses—an imagery reminiscent of the iconic portrayal of Santa Claus embarking on a nocturnal journey to deliver gifts.

Figure 5: Alice in Wonderland illustration (photo from BBC).

In children's stories, it often serves as a dwelling for fairies, elves, and even the beloved Smurfs. One intriguing legend suggests that the Fly Amanita played a surprising role in shaping Christmas folklore, as mentioned above, claiming that the iconic red and white colors associated with Santa Claus find their origin in A. muscaria. The narrative goes on to propose several imaginative scenarios: Santa's flying sleigh is a product of hallucinations induced by the mushroom; the reindeer, in this tale, consume these mushrooms; Santa's distinctive attire is linked to those who gather A. muscaria, and even the chimney tradition is explained by individuals supposedly smoking the fly-agaric on rooftops (Collado, 2024). Even the mushroom featured in the popular video game series Super Mario, commonly known as the "Super Mushroom", is indeed fly-agaric itself!

In medieval Europe, the perception of A. muscaria took a stark turn, marked by suspicion and fear due to the psychoactive nature of the mushroom. This led to its association with witchcraft and sorcery. The Church, aligning with prevailing beliefs, depicted the Fly Agaric as an instrument of the devil, framing its consumption as a pact with malevolent forces. Its presence is not only deeply rooted in nature but also ingrained in art, literature, and popular media, making it a symbol of magic and enchantment. In the realm of storytelling, A. muscaria emerges as the archetypal mushroom. Its iconic red cap adorned with white spots has made it a visual shorthand for the magical and mysterious. This portrayal is vividly exemplified in Lewis Carroll's timeless classic, Alice in Wonderland (1865), where Alice encounters a caterpillar perched on a mushroom—an image often illustrated as the distinctive Fly Agaric, adding an extra layer of enchantment to the fantastical world Carroll created.

Figure 6: European folklore (photo from Zoom Out Mycology).

Role in Nature and Medicine

Studies utilizing muscimol and its analogs have provided valuable information about the potential involvement of central GABAergic systems (neurotransmitter systems in the central nervous system (CNS) that involve gamma-aminobutyric acid (GABA), the primary inhibitory neurotransmitter in the brain) in processes such as convulsions, extrapyramidal functions, and other behaviors. An intriguing discovery has been made regarding the neuroprotective effects of a fly-agaric extract enriched with a high concentration of muscimol, which demonstrated a notable ability to safeguard rat brain synaptosomes when exposed to the neurotoxin 6-hydroxydopamine. In comparison to the control group, where the toxin triggered the generation of reactive oxygen species (ROS) and reactive quinones, processes associated with Parkinson's disease, the fly agaric extract significantly preserved synaptosomal viability (Carboué & Lopez, 2021).

Interpreting behavioral outcomes from muscimol studies poses challenges since muscimol undergoes extensive metabolism, and its interactions with membrane sites beyond GABA receptors complicate the interpretation of results. Despite these complexities, the A. muscaria research has shed light on the intricate interplay of GABAergic systems in various physiological and behavioral contexts (DeFeudis, 1980). The extract's effectiveness in mitigating the harmful impact of the neurotoxin suggests a potential role in neuroprotection, particularly in conditions where oxidative stress and neuronal damage play a significant role. Despite the potential benefits of fly-agaric, studies reveal that ingesting high doses might lead to poisoning, highlighting the importance of prompt identification and collaboration with poison control experts for effective clinical intervention. In one case, a 44-year-old previously healthy man was urgently admitted to the emergency department presenting malaise, nausea, and altered consciousness. Shortly after admission, the patient lost consciousness and was unresponsive to both verbal and physical stimuli. The patient's wife revealed that approximately an hour before seeking medical attention, he had ingested about half a kilogram of fly-agaric mushrooms, which he had collected himself (Rampolli et al., 2021).

Conclusion

Amanita muscaria emerges as a captivating subject that transcends its existence as a fungus in the natural world, extending into the realms of mythology, spirituality, and cultural symbolism, painting a vivid tapestry of diverse narratives across different times and regions. From being a revered component in ancient rituals to being feared and demonized in medieval Europe, the fly agaric showcases the intricate interplay between nature and human perception. Its iconic appearance, with a vibrant red cap and white freckles, has etched itself into the collective imagination, making it a cultural icon and a symbol of enchantment. As the layers of A. muscaria's story get unraveled, not only the scientific intricacies of a unique organism are covered, but also the threads that weave it into the rich fabric of human history and imagination.

Bibliographical References

Amanita_muscaria. (n.d.). www.bionity.com. https://www.bionity.com/en/encyclopedia/Amanita_muscaria.html

Bains, A., Chawla, P., Kaur, S., Najda, A., Fogarasi, M., & Fogarasi, S. (2021). Bioactives from Mushroom: Health Attributes and Food Industry Applications. Materials (Basel, Switzerland), 14(24), 7640. https://doi.org/10.3390/ma14247640

Carboué, Q., & Lopez, M. (2021). Amanita muscaria: Ecology, Chemistry, Myths. Encyclopedia, 1(3), 905–914. https://doi.org/10.3390/encyclopedia1030069

Catalfomo P., Eugster C. (1970). Amanita muscaria: Present understanding of its chemistry. Bulletin on Narcotics 22(4): 33–41. https://www.unodc.org/unodc/en/data-and-analysis/bulletin/bulletin_1970-01-01_4_page005.html

Collado, E. (2024). Amanita Muscaria : what is it and what are its effects. Blog de Grow Barato. https://www.growbarato.net/blog/en/amanita-muscaria-what-is-it-and-what-are-its-effects/#Myths_and_legends_about_the_Amanita_Muscaria

DeFeudis, F.V. (1980). Physiological and behavioral studies with muscimol. Neurochem Res 5, 1047–1068 . https://doi.org/10.1007/BF00966163

Michelot D., Melendez-Howell, LM. (2003). "Amanita muscaria": chemistry, biology, toxicology, and ethnomycology. Mycol Res. 107(Pt 2):131-46. doi: 10.1017/s0953756203007305. PMID: 12747324.

National Center for Biotechnology Information. (2024). PubChem Taxonomy Summary for Taxonomy 41956, Amanita muscaria. Retrieved February 1, 2024 from https://pubchem.ncbi.nlm.nih.gov/taxonomy/Amanita-muscaria.

Nichols D. E. (2016). Psychedelics. Pharmacological reviews, 68(2), 264–355. https://doi.org/10.1124/pr.115.011478

Ramírez-Terrazo, A., Adriana Montoya, E., Garibay-Orijel, R., Caballero-Nieto, J., Kong-Luz, A., & Méndez-Espinoza, C. (2021). Breaking the paradigms of residual categories and neglectable importance of non-used resources: the "vital" traditional knowledge of non-edible mushrooms and their substantive cultural significance. Journal of ethnobiology and ethnomedicine, 17(1), 28. https://doi.org/10.1186/s13002-021-00450-3

Rampolli, F. I., Kamler, P., Carnevale Carlino, C., & Bedussi, F. (2021). The Deceptive Mushroom: Accidental Amanita muscaria Poisoning. European journal of case reports in internal medicine, 8(3), 002212. https://doi.org/10.12890/2021_002212

Winkelman, M. J. (2022). Amanita muscaria: Fly Agaric history, mythology and pharmacology. Journal of Psychedelic Studies, 6(1), 1–4. https://doi.org/10.1556/2054.2022.00216

Visual Sources