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Deadly Amanita Mushrooms As Food: a Survey of the Feeding Preferences of Mycophagous Diptera from Across North America, with Notes on Evolved Detoxification

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Deadly Amanita Mushrooms As Food: a Survey of the Feeding Preferences of Mycophagous Diptera from Across North America, with Notes on Evolved Detoxification Deadly Amanita Mushrooms as Food: A Survey of the Feeding Preferences of Mycophagous Diptera from Across North America, with Notes on Evolved Detoxification. Britt A. Bunyard (It’s probably worth pointing out to the mushroom identification (based on non-entomologically inclined that all current taxonomy concepts), or made no flying insects are not true flies. All insects, attempt to identify mushrooms to species, by definition, in addition to having a focusing only on dipteran identification. three-segmented body, have two pairs of Some studies have made no attempt to verview: The genus Amanita is well-known for their typically wings—except for Diptera, which have identify to species the flies or mushroom large, showy, and ubiquitous only a single pair of wings; think house hosts (Hosaka and Uno, 2012). mushrooms. Additionally, the genus is flies, fruit flies, and mosquitos.) The ecology and life cycle of O Despite the frequency and diversity mushroom-feeding species has been infamous for being toxic to mammals, and especially humans, that consume of Diptera that inhabit mushrooms, mostly overlooked by previous studies these mushrooms. While most species mycophagous species mostly remain and currently little is known about larval of Amanita probably are not toxic, a poorly known. Although the coevolved stages, feeding preferences, seasonality, handful of species are responsible for 95% associations among mushrooms and their or geographic range for numerous species of the fatal mushroom poisonings in North insect symbionts is fascinating, they have (Bunyard and Foote, 1990a; 1990b; Graves America and they are feared worldwide. caught the attention of few researchers and Graves, 1985; Buxton, 1960). The The mode of action of Amanita toxins over the years. (As mycophiles and larval stages of many of the rarer species in mammalian cells is well-known. mushroom hunters frequently encounter of mycophagous flies have never been Paradoxically, many disparate groups mushroom-eating insects, and may be described (Bunyard, 2003) and most of invertebrate animals consume curious as to the nature of the association reports infer that mycophagous flies are Amanitas, along with other mushrooms, and wonder just what these insects are, I probably generalists and not specific to with impunity. True flies are among the will cite ample references that the reader any species of fungus, as fungal hosts are most successful mycophagous animals; may seek out for additional information.) considered too patchy and/or ephemeral; mycophagy has likely arisen many times No comprehensive studies of mushroom or are scavengers, feeding on all sorts of within the order and is found in several flies have been conducted across North decaying organic material (Krivosheina, families of flies. Recently, tolerance America, however some regional studies 2008; Hackman and Meinander, 1979; to Amanita toxins (primarily α-amanitin) have been published (Bunyard, 2003; Jaenike, 1978a; 1978b) in addition to was elucidated in mycophagous species Bunyard and Foote, 1990a). In Europe, mushrooms. Occasional accounts of of Drosophilidae. It is not known how there have been a few large-scale studies oligophagous and specialist species (and many other groups of Diptera have species involving a large diversity of mushroom even monophagy) are likely artifacts of tolerant to Amanita toxins and if the same host species and fly species (Ševčík, 2006; insufficient sampling (Hanski, 1989). mechanisms are involved as those in the Yakovlev, 1994; Hackman and Meinander, It is likely that very few mycophagous Drosophilidae. This current report on the 1979; Buxton, 1960) as well as reviews Diptera truly are obligate consumers Diptera of Amanitas of North America is of previous work (Krivosheina, 2008). of mushrooms. Many, if not most, are a brief synopsis of a larger manuscript in However, most such ecological studies facultatively mycophagous, and able to preparation for publication later this year. were conducted several decades ago utilize a wide array of fresh or rotting The purpose of this study was to find out (Shorrocks and Wood, 1973; Papp, 1972; plant and fungal material (Hackman and how widespread Amanita mycophagy is Valley et al., 1969; Pielou and Verma, 1968; Meinander, 1979). Some have suggested among species of Diptera and to determine Pielou, 1966; Pielou and Mathewman, that many species found in mushrooms if there are feeding preferences for or 1966; Buxton, 1960) and often gave only are predacious on other dipteran larvae against species considered toxic. anecdotal accounts of adult flies occurring there (Krivosheina, 2008). Undoubtedly, Fungi are found in virtually every on mushrooms (Graves and Graves, 1985; mycophagy within the Diptera has arisen ecological niche on the planet. And Valley et al., 1969; Patterson, 1943), not several times and it has been postulated the sporophores of many groups verifying true mycophagy. Some studies that mycophagy probably arose from of macrofungi (in plain English: have included flies that emerged solely ancestral detritivores within many, or even “mushrooms” of the Basidiomycota from decaying mushrooms (thus, possibly most groups (Bruns, 1984). and Ascomycota) are food sources for only scavenging) (Frouz and Makarova, Previous studies have not focused a bewildering diversity of animals on 2001) and therefore did not establish a on Amanitas the planet, in addition to humans. Most strong ecological association (e.g., food substrate, site of overwintering, etc.) with Previously, fruitbodies from the groups of mushrooms serve as hosts Basidiomycota and Ascomycota were of mycophagous Diptera, the true flies. fungal sporocarps. Many had improper 40 FUNGI Volume 10:4 Winter 2018 Figure 1. Unidentified species of Family Mycetophilidae. 2b. Photo courtesy of F. Rhoades. 2a. 2c. Figure 2. Mycophagous species of Drosophilidae reared from Amanitas; a) Drosophila falleni; b) Mycodrosophila dimidiata; c) Leucophenga varia. Photos courtesy of F. Rhoades. surveyed as hosts for mycophagous noteworthy to see species of Amanita Diptera (Bunyard, 2003; Bunyard and mushrooms listed as hosts for “Despite the claims Foote, 1990a). Adult flies were reared mycophagous flies, as this group is from sporocarps representing most notoriously toxic to humans. Amanita that the Fly Agaric major commonly-occurring groups of muscaria—one of the most common earned its common eastern North America (belonging to 30 mushrooms of North America (indeed, name as a result of families of basidiomycete and 11 families the world)—is known as the “Fly Agaric,” of ascomycete macrofungi). Furthermore, reportedly due to its historic use as a historical use as a fly- all major groups of known mycophagous fly killer around human dwellings (for killer, the consensus Diptera were represented in those a review of history and toxicology, see surveys: Drosophilidae, Anthomyiidae, Michelot and Melendez-Howell, 2003). based on science is Asteiidae, Heleomyzidae, Chloropidae, Despite the claims that the Fly Agaric that this mushroom Phoridae, Mycetophilidae, Sciaridae, earned its common name as a result of is likely the most Tipulidae, Trichoceridae, Cecidomyiidae, historical use as a fly-killer, the consensus and Platypezidae, as well as mushroom based on science is that this mushroom preferred host of scavengers of decaying mushrooms, is likely the most preferred host of mushroom-consuming including Psychodidae, Ceratopogonidae, mushroom-consuming flies in North Lonchaeidae, Stratiomyiidae, America, and globally. flies in North America, Sphaeroceridae, and Sarcophagidae. To date, there is a paucity of data and globally.” During these surveys, and those on insect mycophagy of Amanitas. No conducted by other authors, it is comprehensive study has been undertaken FUNGI Volume 10:4 Winter 2018 41 Table 1. Amanita species and collection sites discussed in this survey. consecutive years. While ID to species can be difficult, gross morphology allows pretty for this group of fungi due to several Amanita are endemic to small regions, easy identification of Amanitas below reasons. Proper identification of Amanitas thus missed in all studies not inclusive for the level of genus. The genus Amanita is can be difficult and the genus includes all North America. The biggest limitation divided into seven Sections, historically hundreds of species in North America; to any comprehensive ecological study of based on morphology, chemistry of the few previous studies including Amanita is in the generally ephemeral and (specifically, class of toxins, reviewed Amanitas, misidentification was common sporadic nature of mushroom fruitings: below), and more recently supported by (e. g., Amanita phalloides, a nonnative fruitbodies are present for a brief period DNA sequence analysis. species, has been listed in the Great of time (usually just a few days) and Lakes region but is known to occur only fruitings are difficult to predict in years of A 30-year survey of mushroom on the West and East Coast, and was unfavorable weather (e.g., too dry/wet or flies in North America only introduced into North America too cold / hot). Fruitings of any one species Fresh mushrooms were collected during the last century). Many species of may not happen in a given year or even from 1987-2017; collection sites ranged 42 FUNGI Volume 10:4 Winter 2018 3a. 3b. Figure 3. Toxic Amanitas; a) Amanita muscaria var. flavivolvata (Section Amanita); b) Amanita muscaria var. guessowii (Section Amanita), photo courtesy J. Hammond; c) Amanita phalloides
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