Research Article |
Corresponding author: Victor M. Bandala ( victor.bandala@inecol.mx ) Academic editor: María P. Martín
© 2018 Mariana Herrera, Victor M. Bandala, Leticia Montoya.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Herrera M, Bandala VM, Montoya L (2018) Cantharellus violaceovinosus, a new species from tropical Quercus forests in eastern Mexico. MycoKeys 32: 91-109. https://doi.org/10.3897/mycokeys.32.22838
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During explorations of tropical oak forests in central Veracruz (eastern Mexico), the authors discovered a Cantharellus species that produces basidiomes with strikingly violet pileus and a hymenium with yellow, raised gill-like folds. It is harvested locally and valued as a prized edible wild mushroom. Systematic multiyear sampling of basidiomes allowed the recording of the morphological variation exhibited by fresh fruit bodies in different growth stages, which supports the recognition of this Cantharellus species from others in the genus. Two molecular phylogenetic analyses based on a set of sequences of species of all major clades in Cantharellus, one including sequences of the transcription elongation factor 1-alpha (tef-1α) and a combined tef-1α and nLSU region (the large subunit of the ribosome), confirm the isolated position of the new species in a clade close to C. lewisii from USA, in the subgenus Cantharellus. Detailed macroscopic and microscopic descriptions, accompanied by illustrations and a taxonomic discussion are presented.
Cantharellales , ectomycorrhizal fungi, Neotropical fungi, oak forest, wild edible mushrooms
The diversity of species in Cantharellus Adans.: Fr., in combination with their ectomycorrhizal nature (mycobionts of several plant lineages), as well as their highly prized value as edible wild mushrooms, have attracted the attention of specialists from different fields worldwide (
Cantharellus encompasses fungi with long-lived, gymnocarpic, fleshy, variedly coloured, trumpet-shaped basidiomes with nearly smooth, veined, gill-like folded to distinctly lamellate hymenophore, pileipellis poorly differentiated, cystidia lacking, smooth and thin-walled spores, with or without clamps (
The two former features are considered amongst the most taxonomically informative at subgeneric level and the latter used to distinguish species (
Taxonomic research on Cantharellus has increased substantially in the last decade, especially by combining DNA and morphological information to support the definition of early recognised species and others recently discovered (
The earliest description of Cantharellus in Mexico dates from
During the authors’ long term explorations in tropical oak forests in central Veracruz, a Cantharellus species was found with a striking habit, distinctive when compared to the previous records from Mexico. In fact, this fungus is unique because the fresh basidiomes in different growth stages possess a strikingly violet pileus and yellow, raised gill-like folded hymenophore, in combination with ellipsoid basidiopores and terminal elements of pileipellis slightly thick-walled. The macro- and micromorphological features depicted in this fungus, as well as its distinct position in two phylogenetic analyses, one of tef-1α and other of a combined tef-1α+nLSU sequences datasets, allowed its recognition as a new species. This Cantharellus species is locally considered a prized edible mushroom.
Cantharellus basidiomes were collected during June-October, through six consecutive years (2012–2017) including some collections in 2009 and 2011, in tropical oak forests from Zentla (837–850 m a.s.l.) and Alto Lucero (400–500 m a.s.l.) counties in central Veracruz (eastern Mexico). In these oak forests, Quercus oleoides is dominant and even forms pure stands. In the Zentla locality, however, Q. glaucescens and Q. sapotifolia are also present and, at times, also form monodominant small patches. Descriptions of morpho-anatomical features were achieved based on fresh samples and following
DNA was isolated from fresh material using DNAeasy Plant Mini Kit (QIAGEN, Hilden, Germany) following the manufacturer´s recommendations. The transcription elongation factor 1-alpha (tef-1α) was amplified using the primers tef1F and tef1R (
Cantharellus species included in this study: samples, location and accession number for tef-1α and nLSU sequences.
Taxon | Voucher Specimen | Location | GenBank | |
---|---|---|---|---|
tef-1α | nLSU | |||
C. addaiensis | BB 98.033 | Tanzania | JX192992 | KF294667 |
C. afrocibarius | BB 96.236 | Zambia | JX192993 | KF294668 |
C. albidolutescens | BB 08.057 | Madagascar | KF294752 | KF294645 |
C. albidolutescens | BB 08.080 | Madagascar | JX192982 | – |
C. ambohitantelyensis | BB 08.336 | Madagascar | JX192989 | – |
C. amethysteus | BB 07.284 | Slovakia | GQ914953 | KF294639 |
C. amethysteus | BB 07.309 | Slovakia | GQ914954 | KF294642 |
C. appalachiensis | BB 07.123 | USA | GQ914979 | KF294565 |
C. cascadensis | BB 13.251 | USA | KX857044 | – |
C. chicagoensis | JJ/MO-CANT1 | USA | KX857025 | – |
C. cibarius | BB 07.300 | Slovakia | GQ914950 | KF294641 |
C. cibarius | GE 07.025 | France | GQ914949 | – |
C. cinnabarinus | BB 07.053 | USA | GQ914984 | KF294630 |
C. cinnabarinus | BB 07.001 | USA | GQ914985 | KF294624 |
C. congolensis | BB 98.039 | Tanzania | JX193015 | KF294609 |
C. congolensis | BB 98.058 | Tanzania | JX192996 | KF294673 |
C. corallinus | JJ/MO-CANT2 | USA | KX857031 | – |
C. corallinus | JJ/MO-CANT5 | USA | KX857034 | – |
C. deceptivus | JJ/NC-CANT5 | USA | KX857029 | – |
C. decolorans | BB 08.278 | Madagascar | GQ914968 | – |
C. decolorans | BB 08.243 | Madagascar | JX192987 | – |
C. densifolius | BB 98.013 | Tanzania | JX193014 | KF294616 |
C. ferruginascens | BB 07.283 | Slovakia | GQ914952 | KF294638 |
C. fistulosus | DT 43 | Tanzania | JX192997 | KF294674 |
C. flavolateritius | VH 1076 | USA | KX857027 | – |
C. flavolteritius | VH1078 | USA | KX857029 | – |
C. gracilis | BB 98.234 | Tanzania | JX192970 | – |
C. humidicolus | BB 98.036 | Tanzania | JX193005 | KF294666 |
C. ibityensis | BB 08.203 | Madagascar | JX192985 | KF294651 |
C. isabellinus var. parvisporus | BB 98.020 | Tanzania | JX192972 | KF294614 |
C. iuventateviridis | SH13/7/2012 | USA | KX857063 | – |
C. iuventateviridis | SH14/7/2012 | USA | KX857064 | – |
C. lateritius | BB 07.025 | USA | GQ914957 | KF294628 |
C. lateritius | BB 07.058 | USA | GQ914959 | KF294633 |
C. lewisii | BB 02.197 | USA | GQ914961 | KF294623 |
C. lewisii | BB 07.003 | USA | GQ914962 | – |
C. lilacinopruinatus | BB 07.221 | Slovakia | GQ914951 | KF294637 |
C. minor | BB 07.002 | USA | JX192978 | KF294625 |
C. minor | BB 07.057 | USA | JX192979 | KF294632 |
C. pallens | BB 09.441 | Italy | KX857013 | – |
C. pallens | BB 12.082 | Italy | KX857035 | – |
C. paucifurcatus | BB 08.320 | Madagascar | KF294655 | JK192988 |
C. persicinus | MH 15.001 | USA | KX857080 | – |
C. phasmasis | CO57 | USA | JX030417 | – |
C. phasmasis | CO74 | USA | JX030418 | – |
C. platyphyllus | BB 98.012 | Tanzania | GQ914969 | KF294617 |
C. platyphyllus subsp. bojeriensis | BB 08.160 | Madagascar | JX192984 | KF294648 |
C. pseudominimus | JV 00.663 | Portugal | JX192991 | KF294657 |
C. quercophilus | BB 07.097 | USA | JX192981 | KF294644 |
C. sebosus | BB 08.234 | Madagascar | JX192986 | KF294652 |
C. spectaculus | C081 | USA | JX030414 | – |
C. cf subamethysteus | AV 12.003 | Thailand | KX857062 | – |
C. subcyanoxanthus | BB 00.1137 | Madagascar | JX192990 | – |
C. subincarnatus subsp. rubrosalmoneus | BB 06.080 | Madagascar | JX192962 | KF294601 |
C. subincarnatus subsp. rubrosalmoneus | BB 06.096 | Madagascar | JX192963 | KF294602 |
C. symoensii | BB 98.011 | Tanzania | GQ914970 | KF294618 |
C. symoensii | BB 98.113 | Tanzania | JX192974 | KF294619 |
C. tabernensis | BB 07.119 | USA | GQ914976 | KF294634 |
C. tabernensis | BB 07.020 | USA | GQ914971 | – |
C. tanzanicus | BB 98.040 | Tanzania | JX192977 | KF294622 |
C. tenuithrix | BB 14.008 | USA | KX857045 | – |
C. tenuithrix | BB 14.009 | USA | KX857045 | – |
C. tomentosus | BB 98.038 | Tanzania | GQ914965 | KF294610 |
C. vellutinus | VH 1583 | USA | KX857070 | – |
C. vellutinus | WR WV 07.074 | USA | KX857068 | – |
C. versicolor | Tian 160 | China | KM893857 | – |
C. versicolor | Yu 24 | China | KM893856 | – |
C. violaceovinosus* | Bandala 4513 | Mexico | MF616520 | MF616524 |
C. violaceovinosus* | Corona 648 | Mexico | MF616521 | MF616525 |
C. violaceovinosus* | Herrera125 | Mexico | MF616522 | MF616526 |
Craterellus tubaeformis | BB 07.293 | Slovakia | GQ914989 | KF294640 |
Hydnum repandum | BB 07.341 | Slovakia | JX192980 | KF294643 |
Six tef-1α and nLSU sequences obtained in this study, together with 113 sequences of Cantharellus species from all major clades across the genus (after
Sixty fresh collections were obtained of the violet Cantharellus species, including basidiomes in different growth stages, most of them detected between August-October, in both localities explored. Six new tef-1α and nLSU sequences from three collections were generated in this study (Table
MEXICO. Veracruz: Municipality of Zentla, around town of Zentla, 850 m a.s.l., gregarious in soil, under Quercus oleoides Schltdl. & Cham., 5 July 2012, Corona 648 (XAL).
Differing from other Cantharellus species by: uniformly dark violet, violet-grey to violet-wine or violet-reddish pileus; yellow, gill-like folded hymenophore and ellipsoid basidiospores 7–10 (–11) × (4.5–) 5–6.5 (–7) µm. X–m = 7.8–9× 5.1–6.3 µm, Q–= 1.31–1.66, basidia (40–) 45–114 (–125) × (6–) 7–11 (–12) µm, with (1–) 2–5 sterigmata, and terminal elements of the pileipellis 4–6 µm diam, slightly thick-walled.
Referring to the dark violaceous, becoming wine to reddish pileus.
Pileus (15–) 25–113 mm diam, convex to broadly-convex with margin incurved when young, expanding to plane or subplane, often shallowly depressed or finally broadly infundibuliform, surface dry, not hygrophanous, dull, smooth, glabrescent, surface at times breaking in faintly tesselate-rimose-like pattern, then appearing appressed fibrillose with age and not forming scales; surface uniformly dark violet (15D4, 15F2–7, 16D3–4, 16D6, 16F4–5) to pale violet with age (15DE5–7) or violet-grey (16D3–4, 16D6), lilac or greyish-lilac (15A3, 15C3–4, 16C2–3), becoming violet-wine or violet-reddish (14E5–8, 14EF4–5), wine (12D4), fading with age and sun exposure, developing pinkish, lilac and reddish tints, especially towards the margin (13A3–4, 13D3–4, 15A4–5), naked parts showing the yellow context (4A2–3); margin incurved or straight, entire or slightly crenate, undulate or irregular, often incised, rarely lobed, not striated. Hymenophore with well-defined gill-like folds, up to 3 mm deep, decurrent, subdistant, in some specimens almost straight and inclusive thin, in other materials with faintly sinuous or irregular thicker folds, frequently forking at different levels or only towards the pileus margin, with lower irregular anastomosis amongst the folds, in some specimens the anastomosis occur practically in the whole hymenophore, while in others only at some areas, especially at pileus margin, some specimens (specially towards the stipe) with irregular low veins amongst the folds or the folds become as low and sinuous vein-like; butter-yellow or yellow (2.5Y 8/4,10YR 8/6; 4A3–4). Stipe (20–) 25–75 × 5–18 mm, equal and only slightly swollen at base or widening above and tapering gradually downwards, solid, surface glabrous, concolorous with hymenophore, often staining ochraceous or rusty orange colour when handled, occasionally with whitish, small rhizomorphs at base. Context whitish to yellow (4A2–3), at times wax-like, odour mild, agreeable, at time fruity somewhat to apricot; taste mild, agreeable.
Basidiospores 7–10 (–11) × (4.5–) 5– 6.5 (–7) µm, [X–m = 7.8–9 × 5.1–6.3 µm, Q–= 1.31–1.66, (n=13)], ellipsoid, smooth, thin-walled, hyaline, inamyloid, devoid of granular contents or refractive droplets. Basidia (40–) 45–114 (–125) × (6–) 7–11(–12) µm, narrowly clavate to subcylindrical, with (1–) 2–5 sterigmata 8–10 µm long, thin-walled, hyaline; subhymenium composed of cylindrical hyphae 4–5 µm diam. Cystidia absent. Pileipellis a cutis composed of hyphae 4–6 µm diam, intermingled in a compact arrangement, cylindrical, hyaline to yellowish, inamyloid, often some of them with pale brownish contents, these decidedly brown coloured in group; distinctive terminal elements 4–6 µm broad, slightly thick-walled (<1 µm thick), smooth, hyaline, some pale brownish, scattered on the surface. Pileus trama composed of cylindrical to inflated hyphae, 3–12 µm diam, slightly thick-walled (<1 µm thick), hyaline, yellowish in mass, some of the hyphal segments completely filled with darker contents. Hymenophoral trama composed of hyphae 3–5 µm diam, thin-walled, some with weakly refringent contents. Clamp connections present on hyphae in all tissues.
Solitary to gregarious, in soil, at tropical oak forest, under Quercus oleoides, less frequently also under both Q. glaucescens Bonpl. and Q. sapotifolia Liebm. June-October, known in the coastal plain of central Veracruz State, east coast of Mexico.
MEXICO. Veracruz, Zentla Co., Road Puentecilla-La Piña, 837 m a.s.l., 2 Jul 2009, Del Moral 427, Ramos 216; 27 Oct 2009, García 20, García 22; 16 Jun 2011, Bandala 4490; 21 Jul 2012, Herrera 25; 31 Jul 2012, Bandala 4513; 20 Sep 2012, Bandala 4550, Corona 743; 4 Oct 2012, Bandala 4569, 4573; 4 Jul 2013, Gutiérrez 23; 12 Jul 2013, Bandala 4671; 20 Sep 2013, Herrera 67; 15 Sep 2015, Herrera 135. Around town of Zentla, 850 m a.s.l., 5 Jul 2012, Corona 648; 25 Jun 2013, Herrera 60, 61; 15 Sep 2015, Herrera 137, Santillan 16; 1 Oct 2015, Herrera 151; 30 Jun 2016, Herrera 172; 6 Jul 2016, Herrera 184; 12 Jul 2016, Herrera 187; 22 Sep 2016, Herrera 200, 201, 202, 203; 5 Oct 2016, De la Cruz 14,15; 13 Oct 2016, De la Cruz 42; 27 Oct 2016, Herrera 210, 211; 6 Jul 2017, Garay 350; 3 Aug 2017, Garay 364; 31 Aug 17, Garrido 79; 7 Sep 2017, Herrera 214, 215, 216; 15 Sep 17, Montoya 5403; 21 Sep 17, Corona 1420; 5 Oct 17, Mateo 5. Alto Lucero Co., NE Mesa de Venticuatro, 450–500 m a.s.l., 2 Jul 15, Herrera 125, Herrera 126; 17 Sep 2015, Herrera 138; 2 Aug 2016, Herrera 191; 10 Aug 2016, Herrera 192; 20 Sep 2016, Herrera 195, 196, 197, 198; 27 Sep 2016, Herrera 205, 206, 207; 4 Oct 2016, Herrera 208, 209; 22 Aug 17, Herrera 214; 12 Sep 2017, Garay 375; 19 Sep 2017, Garay 392; 2 Oct 17, Mateo 1 (all at XAL).
Distinctive features of this species include the medium to large size basidiomes, with pileus practically homogeneously violet pigmented (only fading with age), smooth, with surface free of scales, at times with disrupted pileus surfaces due to age, hymenophore bearing yellow gill-like folds, ellipsoid, medium-sized basidiospores [7–10 (–11) × (4.5–) 5– 6.5 (–7) µm], medium to large basidia [(40–) 45–114 (–125) × (6–) 7–11(–12) µm] and terminal elements of pileipellis 4–6 µm diam, slightly thick-walled (<1 µm thick). Molecular phylogenetic analyses support that the species is genetically distinct from other Cantharellus taxa, in both analyses, C. violaceovinosus was nested in an isolated and well-supported clade (95–99/1) (Figs
Cantharellus species with basidiomata having violet pileus are rare but occur in various regions worldwide (
Cantharellus lewisii grows in floodplain hardwoods, in Water Oak plots next to a Taxodium swamp, in beech-magnolia-loblolly pine forests and also under beech-white oak-loblolly pine-magnolia forests in the south of USA (
Cantharellus atrolilacinus was described from Costa Rica, growing under Quercus corrugata Hook.) and Q. sp. (
Although Cantharellus amethysteus (Quél.) Sacc. (subg. Cantharellus) from Europe, may appear superficially similar to some forms of C. violaceovinosus, the former however, especially has a pileus surface covered with vinous or lilac, small scales. The authors studied two specimens of C. amethysteus from France (BB 07.284 and BB 07.309 at PC) displaying elongate basidiospores, 9.5–12 (–12.5) × 5–7 µm (X–m = 11–11.2 × 5.9–6.4 µm; Q–= 1.76–1.86), as Eyssartier and Buyck (
Cantharellus goossensiae (Beeli) Heinem., C. cyanoxanthus R. Heim ex Heinem., C. subcyanoxanthus Buyck, Randrianjohany & Eyssart. and C. longisporus Heinem. represent African species with basidiomes displaying violaceous tinges (
Cantarellus violaceovinosus was recorded as a common fleshy mushroom, during the multiyear sampling developed in the tropical Quercus forests studied. It was found in ectomycorrhizal association with native trees of Quercus species. This mushroom was very often recorded in pure stands of Q. oleoides and less frequently in Q. glaucescens and Q. sapotifolia patches. This violet pigmented chanterelle shares the same habit preferences as C. lateritius, also found in the study sites. A similar co-ocurrence has been reported between C. lewisii (the sister relative of C. violaceovinosus) and C. lateritius in the State of Texas in the USA (
We recognise the support given by CONACYT (CB 252431) to study the EcM fungi associated with tropical species of Quercus in Veracruz, Mexico. M. Herrera is grateful for the scholarship grant from CONACYT (261413). Thanks are given to Dr. B. Buyck (PC) for the loan of herbarium specimens. We appreciate the assistance in the field and in the laboratory to Biol. D. Ramos (Instituto de Ecología, A.C.). Biol. J.C. Corona collaborated in some explorations. We acknowledge the support given by CONACYT (225382) to the Laboratorio de Presecuenciación, Red Biodiversidad y Sistemática, INECOL. Dra. Edith Garay and IBT Bertha Pérez assisted us in some molecular procedures.