Exsudoporus frostii

Exsudoporus frostii (formerly Boletus frostii), commonly known as Frost's bolete or the apple bolete, is a bolete fungus first described scientifically in 1874. A member of the family Boletaceae, the mushrooms produced by the fungus have tubes and pores instead of gills on the underside of their caps. Exsudoporus frostii is distributed in the eastern United States from Maine to Georgia, and in the southwest from Arizona extending south to Mexico and Costa Rica. A mycorrhizal species, its fruit bodies are typically found growing near hardwood trees, especially oak.

Exsudoporus frostii
Scientific classification
Kingdom:
Fungi
Division:
Basidiomycota
Class:
Agaricomycetes
Order:
Boletales
Family:
Boletaceae
Genus:
Exsudoporus
Species:
E. frostii
Binomial name
Exsudoporus frostii
(J.L.Russell) Vizzini, Simonini & Gelardi (2014)
Synonyms[1]
  • Boletus frostii J.L.Russell (1874)
  • Suillellus frostii (J.L.Russell) Murrill (1909)
  • Tubiporus frostii (J.L.Russell) S.Imai (1968)
Exsudoporus frostii
float
Mycological characteristics
pores on hymenium
cap is convex or flat
hymenium is adnate
stipe is bare
spore print is olive-brown
ecology is mycorrhizal
edibility: edible but not recommended

Exsudoporus frostii mushrooms can be recognized by their dark red sticky caps, the red pores, the network-like pattern of the stipe, and the bluing reaction to tissue injury. Another characteristic of young, moist fruit bodies is the amber-colored drops exuded on the pore surface. Although the mushrooms are considered edible, they are generally not recommended for consumption because of the risk of confusion with other poisonous red-pored, blue-bruising boletes. E. frostii may be distinguished from other superficially similar red-capped boletes by differences in distribution, associated tree species, bluing reaction, or morphology.

Taxonomy

The species was named by the Unitarian minister John Lewis Russell of Salem, Massachusetts, based on specimens found in Brattleboro, Vermont. He named the fungus after his friend, fellow amateur American mycologist Charles Christopher Frost, who published a description of the species in his 1874 survey of the boletes of New England.[2][3] When the name of a species is contributed by an individual, but the name is formally published by another, the contributor's name can be cited, separated from the publishing author as apud; for this reason, the name and authority are written Boletus Frostii Russell apud Frost in some older literature.[4] Bernard Ogilvie Dodge made reference to B. frostii in 1950 during an address to the Mycological Society of America, in which he spoke about the role of the amateur in discovering new species: "They would have informed us all about the man Russell, who named a fine new bolete for his friend Frost, and about the man Frost, who named a fine new bolete for his friend Russell. Boletus Frostii and Boletus Russellii are mushrooms with character, even though they were described by amateurs."[5] However, in attempting to establish a lectotype specimen, mycologist Roy Halling examined both Russell's original material and his accompanying notes; he concluded that it was Frost who made the original species determinations, further suggesting that "there is no evidence to show that Russell ever collected B. frostii or wrote a description of it."[6]

William Murrill in 1909 placed the species in the genus Suillellus,[7] while Sanshi Imai transferred it to Tubiporus in 1968.[1] Tubiporus has since been synonymized with Boletus.[8] In 1945, Rolf Singer described a bolete he found in Florida; although he originally described it as a subspecies of B. frostii,[9] he later considered the differences between the taxa significant enough to warrant publishing Boletus floridanus as a unique species.[4] Following recent molecular studies that outlined a new phylogenetic framework for the Boletaceae,[10][11] the bolete was transferred to the newly circumscribed genus Exsudoporus in 2014.[12]

Exsudoporus frostii is commonly known as "Frost's bolete"[13] or the "apple bolete". In Mexico, its vernacular name is panza agria, which translates to "sour belly".[14]

Description

The shape of the cap of the young fruit body ranges from a half sphere to convex, later becoming broadly convex to flat or shallowly depressed, with a diameter of 5–15 cm (2.0–5.9 in).[15] The edge of the cap is curved inward, although as it ages it can uncurl and turn upward. In moist conditions, the cap surface is sticky as a result of its cuticle, which is made of gelatinized hyphae. If the fruit body has dried out after a rain, the cap is especially shiny,[4] sometimes appearing finely areolate (having a pattern of block-like areas similar to cracked, dried mud).[15] Young mushrooms have a whitish bloom on the cap surface.[16]

View of the hymenium

The color is bright red initially, but fades with age. The flesh is up to 2.5 cm (1.0 in) thick, and ranges in color from pallid to pale yellow to lemon yellow.[15] The flesh has a variable staining reaction in response to bruising, so some specimens may turn deep blue almost immediately, while others turn blue weakly and slowly.[4]

The tubes comprising the pore surface (the hymenium) are 9–15 mm deep, yellow to olivaceous yellow (mustard yellow), turning dingy blue when bruised. The pores are small (2 to 3 per mm), circular, and until old age a deep red color that eventually becomes paler. The pore surface is often beaded with yellowish droplets when young (a distinguishing characteristic), and readily stains blue when bruised. The stipe is 4 to 12 cm (1.6 to 4.7 in) long, and 1 to 2.5 cm (0.4 to 1.0 in) thick at its apex. It is roughly equal in thickness throughout its length, though it may taper somewhat toward the top; some specimens may appear ventricose (swollen in the middle).[15] The stipe surface is mostly red, or yellowish near the base; it is reticulate—characterized by ridges arranged in the form of a net-like pattern.[15] Mycelia, visible at the base of the stipe, are yellowish white to light yellow.[4]

Young fruit bodies may secrete an amber liquid.

The spore print of E. frostii is olive brown.[15] The spores are thick walled, smooth, and spindle shaped, with dimensions of 11–15 by 4–5 µm. Longer spores up to 18 µm long may also be present.[15] The cap cuticle, or pileipellis, is made of a tangled layer of gelatinized hyphae that are 3–6 µm wide.[17] The spore-bearing cells, the basidia, are four spored and measure 26–35 by 10.5–11.5 µm. Cystidia are non-fertile cells interspersed among the basidia, and they are prevalent in the hymenial tissue of E. frostii. These hyaline (translucent) cells measure 30–53 long by 7.5–14 µm wide, and range in shape from somewhat like a spindle (tapering at each end, but with one end typically rounded) to subampullaceous—shaped somewhat like a swollen bottle.[4]

Edibility and nutritional composition

In 1910, Murrill wrote of this mushroom's edibility: "Usually viewed with suspicion because of its red hymenium, but its properties are not accurately known."[18] Since then, several authors have advised against consuming the species, due to its resemblance to other toxic red-capped boletes.[13][15][19] In his 100 Edible Mushrooms (2007), Michael Kuo notes that although the mushroom is apparently edible for some, it "affects others negatively".[20] Despite these warnings, Exsudoporus frostii is edible, and David Arora mentions that it is commonly sold in rural markets in Mexico;[14] a 1997 study suggests that it is only consumed in rural areas in Querétaro state.[21] Its taste and odor have been described as "pleasant"[13] or "sweet"[22] and somewhat like citrus,[16] although the cuticle of the cap may taste acidic.[15]

Chemical analysis of fresh fruit bodies collected in Mexico showed them to have the following composition: moisture 94.53%; ash 0.323%; dietary fiber 3.024%; fat 0.368%; and protein 1.581%. The free fatty acid content of dried fruit bodies was 4.5%, slightly more than the common button mushroom (Agaricus bisporus), which had 3.5%. The majority of this total was oleic acid (1.95%), followed by linoleic acid (1.68%) and palmitic acid (1.69%).[21]

Similar species
Poisonous Boletus flammans is similar in appearance.

Other red-capped boletes include the poisonous B. flammans and B. rubroflammeus; the former grows most commonly under conifers, the latter in association with hardwoods in eastern North America and southern Arizona.[14] Often confused with E. frostii are E. permagnificus and B. siculus, but the latter two species are known only from Europe and always grow in association with oaks.[23][24] The fruit bodies of young specimens of B. kermesinus, newly described from Japan in 2011, are similar in appearance to E. frostii. In addition to its distribution, B. kermesinus can be distinguished from E. frostii by having flesh that does not bruise blue and a stipe in which the reticulum is not as deep and coarse.[25] B. pseudofrostii, found in Belize, produces smaller caps that are 1.7 to 2.0 cm (0.7 to 0.8 in) in diameter.[26] Boletus russelli, found in eastern North America, has a red to reddish-brown cap and reticulate stipe, but its pore surface is yellow, and the fruit body does not bruise blue.[20]

Exsudoporus floridanus differs from E. frostii in having a lighter cap color and in the texture of the cap surface: it is tomentose (covered with dense, short, soft, matted hairs) or velutinous (like velvet), compared to the relatively smooth surface of E. frostii. Singer notes that although the physical characteristics between the two taxa may be blurred and are hard to define, the area of origin can reliably distinguish them: E. floridanus is found on shaded lawns and scrubland in open oak stands in non-tropical regions of Florida, typically on grassy or sandy soil, where it fruits between May and October.[4]

Ecology, habitat, and distribution
Immature specimen with cap not fully expanded; bruising is evident on the stipe.

Exsudoporus frostii is a mycorrhizal species,[27] meaning that the fungus forms associations with the roots of various species of trees. These associations are mutualistic, because the fungus absorbs mineral nutrients from the soil and channels these into the plant, while the plant provides the fungus with sugars, a product of photosynthesis. The characteristic feature of the mycorrhiza is the presence of a sheath of fungal tissue that encases the terminal, nutrient-absorbing rootlets of the host plant. The fungus forms an extensive underground network of hyphae that radiate outward from the surface of the root sheath, effectively increasing the surface area for nutrient absorption. The hyphae also invade between the root cortical cells to form a Hartig net.[28] Using pure culture techniques, Exsudoporus frostii has been shown to form mycorrhizae with Virginia pine (Pinus virginiana),[27] while a field study confirms a similar association with the oak Quercus laurina.[29]

The fruit bodies grow solitarily, scattered, or in groups on the ground under hardwood trees; the fungus fruits in summer to early autumn. William Murrill noted its preference for growing in "thin oak woods, where the light is sufficient to enable grass to grow",[7] and Alexander H. Smith mentioned its preference for growing in "thin, sandy soil under scrub oak."[3] In the United States, it is distributed from Maine south to Georgia, extending west to Tennessee and Michigan, and in southern Arizona.[4][16] In Mexico, it is often found under Madrone.[14] It has also been collected in Costa Rica, where it associates with the oak species Quercus copeyensis, Q. costaricensis, Q. rapurahuensis, and Q. seemanii.[30] A 1980 publication tentatively suggested that the fungus was also present in Italy,[31] but the author later determined that the putative E. frostii was actually Boletus siculus.[24]

Fruit bodies can be parasitized by the mold-like fungus Sepedonium ampullosporum.[32] Infection results in necrosis of the mushroom tissue, and a yellow color caused by the formation of large amounts of pigmented aleurioconidia (single-celled conidia produced by extrusion from the conidiophores).[33]

See also

References
  1. "Boletus frostii J.L. Russell". MycoBank. International Mycological Association. Retrieved 2011-06-21.
  2. Frost CC. (1874). "Catalogue of Boleti of New England, with descriptions of new species". Bulletin of the Buffalo Society of Natural Sciences. 2: 100–5.
  3. Weber NS, Smith AH (1980). The Mushroom Hunter's Field Guide. Ann Arbor, Michigan: University of Michigan Press. pp. 104–5. ISBN 0-472-85610-3.
  4. Singer R. (1947). "The Boletoideae of Florida with notes on extralimital species III". American Midland Naturalist. 37 (1): 77–8. doi:10.2307/2421647. JSTOR 2421647.
  5. Dodge BO. (1952). "The fungi come into their own". Mycologia. 44 (3): 273–91. doi:10.1080/00275514.1952.12024197. JSTOR 4547605.
  6. Halling RE. (1983). "Boletes described by Charles C. Frost". Mycologia. 75 (1): 70–92. doi:10.2307/3792925. JSTOR 3792925.
  7. Murrill WA. (1909). "The Boletaceae of North America". Mycologia. 1 (1): 4–18. doi:10.2307/3753167. JSTOR 3753167.
  8. Kirk PM, Cannon PF, Minter DW, Stalpers JA (2008). Dictionary of the Fungi (10th ed.). Wallingford, UK: CAB International. pp. 672, 709. ISBN 978-0-85199-826-8.
  9. Singer R. (1945). "New Boletaceae from Florida (a preliminary communication)". Mycologia. 37 (6): 797–9. doi:10.2307/3755143. JSTOR 3755143.
  10. Nuhn ME, Binder M, Taylor AFS, Halling RE, Hibbett DS (2013). "Phylogenetic overview of the Boletineae". Fungal Biology. 117 (7–8): 479–511. doi:10.1016/j.funbio.2013.04.008. PMID 23931115.
  11. Wu G, Feng B, Xu J, Zhu X-T, Li Y-C, Zeng N-K, Hosen MI, Yang ZL (2014). "Molecular phylogenetic analyses redefine seven major clades and reveal 22 new generic clades in the fungal family Boletaceae". Fungal Diversity. 69 (1): 93–115. doi:10.1007/s13225-014-0283-8. S2CID 15652037.
  12. Vizzini A. (August 22, 2014). "Nomenclatural novelties" (PDF). Index Fungorum (183): 1.
  13. Phillips R. "Boletus frostii". Rogers Plants. Archived from the original on 2012-02-18. Retrieved 2012-03-01.
  14. Arora D. (1986). Mushrooms Demystified: A Comprehensive Guide to the Fleshy Fungi. Berkeley, California: Ten Speed Press. p. 529. ISBN 0-89815-169-4.
  15. Thiers HD, Smith AH (1971). The Boletes of Michigan. Ann Arbor, Michigan: University of Michigan Press. pp. 343–4. ISBN 0-472-85590-5.
  16. Bessette AE, Roody WC, Bessette AR (2000). Boletes of North America. Syracuse, New York: Syracuse University Press. p. 114. ISBN 978-0-8156-0588-1.
  17. Kuo M. (January 2007). "Boletus frostii". MushroomExpert.Com. Retrieved 2012-03-01.
  18. Murrill WA. (1910). "Poisonous mushrooms". Mycologia. 2 (6): 255–64. doi:10.2307/3753292. JSTOR 3753292.
  19. Bessette A, Miller OK Jr, Bessette AR, Miller HR (1995). Mushrooms of North America in Color: A Field Guide Companion to Seldom-Illustrated Fungi. Syracuse, New York: Syracuse University Press. p. 385. ISBN 0-8156-2666-5.
  20. Kuo M. (2007). 100 Edible Mushrooms. Ann Arbor, Michigan: The University of Michigan Press. pp. 121–2. ISBN 978-0-472-03126-9.
  21. León-Guzmán MF, Silva I, López MG (1997). "Proximate chemical composition, free amino acid contents, and free fatty acid contents of some wild edible mushrooms from Querétaro, México". Journal of Agricultural and Food Chemistry. 45 (11): 4329–32. doi:10.1021/jf970640u.
  22. Miller HR, Miller OK (2006). North American Mushrooms: A Field Guide to Edible and Inedible Fungi. Guilford, Connecticut: Falcon Guides. p. 385. ISBN 0-7627-3109-5.
  23. Pöder R. (1981). "Boletus permagnificus spec. nov. – ein auffallender Röhrling der Sektion Luridi Fr. assoziiert mit Eichen" [Boletus permagnificus new species – a striking bolete of the section Luridi associated with oak]. Sydowia (in German). 34: 149–56. ISSN 0082-0598.
  24. Alessio CL. (1981). "Boletus siculus inzenga il gia presunto B. frostii Russell rinvenuto in Italia" [Boletus siculus is the supposed Boletus frostii discovered in Italy]. Micologia Italiana (in Italian). 10 (2): 40–2.
  25. Takahashi H, Taneyama Y, Koyama A (2011). "Boletus kermesinus, a new species of Boletus section Luridi from central Honshu, Japan". Mycoscience. 52 (6): 419–24. doi:10.1007/s10267-011-0119-2. S2CID 83544311.
  26. Ortiz-Santana B, Lodge DJ, Baroni TJ, Both EE (2007). "Boletes from Belize and the Dominican Republic" (PDF). Fungal Diversity. 27 (2): 247–416 (see p. 322).
  27. Vozzo JA, Hackskaylo E (1961). "Mycorrhizal fungi on Pinus virginiana". Mycologia. 53 (5): 538–9. doi:10.2307/3756310. JSTOR 3756310.
  28. Deacon J. (2005). Fungal Biology. Cambridge, Massachusetts: Blackwell Publishers. pp. 262–3. ISBN 1-4051-3066-0.
  29. Morris MH, Pérez-Pérez MA, Smith ME, Bledsoe CS (2009). "Influence of host species on ectomycorrhizal communities associated with two co-occurring oaks (Quercus spp.) in a tropical cloud forest". FEMS Microbiology Ecology. 69 (2): 274–87. doi:10.1111/j.1574-6941.2009.00704.x. PMID 19508503.
  30. Halling RE, Muller GM. "Boletus frostii". Macrofungi of Costa Rica. New York Botanical Garden. Retrieved 2011-09-29.
  31. Alessio CL. (1980). "Boletus Frostii presente in Italia?" [Boletus frostii present in Italy?]. Micologia Italiana (in Italian). 9 (3): 15–20. ISSN 0390-0460.
  32. Sahr T, Ammer H, Besl H, Fischer M (1999). "Infrageneric classification of the boleticolous genus Sepedonium: species delimitation and phylogenetic relationships". Mycologia. 91 (6): 935–43. doi:10.2307/3761625. JSTOR 3761625. Archived from the original on 2015-09-23. Retrieved 2011-06-21.
  33. Neuhof T, Berg A, Besl H, Schweche T, Dieckmann R, von Döhren H (2007). "Peptaibol production by Sepedonium strains parasitizing Boletales". Chemistry & Biodiversity. 4 (6): 1103–15. doi:10.1002/cbdv.200790099. PMID 17589879. S2CID 40865857.

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