MycoKeys 7: 31–44, doi: 10.3897/mycokeys.7.4710
Three new species of foetid Gymnopus in New Zealand
Jerry A. Cooper 1, Pat L. Leonard 2
1 Landcare Research, PO Box 40, Lincoln, 7640, New Zealand
2 Motueka, New Zealand

Corresponding author: Jerry Cooper (cooperj@landcareresearch.co.nz)

Academic editor: S. Redhead

received 18 January 2013 | accepted 24 June 2013 | Published 26 June 2013


(C) 2013 Jerry A. Cooper. This is an open access article distributed under the terms of the Creative Commons Attribution License 3.0 (CC-BY), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.


For reference, use of the paginated PDF or printed version of this article is recommended.

Abstract

We describe three new species, Gymnopus imbricatus, Gymnopus ceraceicola and Gymnopus hakaroa, from New Zealand that are similar to Gymnopus foetidus (= Micromphale foetidum), growing on wood, with an insititious stipe and foetid odour. The position of these species within the /gymnopoid clade is confirmed by ITS sequence analysis.

Key words

Gymnopus, Micromphale, New Zealand

Introduction

The new species we describe are members of the family Omphalotaceae, Matheney et al. (2006) and have the morphological characteristics of Gymnopus section Vestipedes subsection Impudicae (Antonín & Noordeloos 2010) which contains Micromphale foetidum (Sowerby) Singer, the type species of the formerly recognised genus Micromphale (e.g. in the sense of Singer 1986). Fruitbodies of the group often have a foetid odour when crushed, described as like rotting cabbage or garlic. The only existing records of this group in New Zealand were found to be misapplications of names applied to northern hemisphere species.

Moncalvo et al. (2002) investigated nLSU rDNA sequence data for a large number of agarics and recognised a /micromphale clade containing Micromphale foetidum (AF261328). The clade also contained Gymnopus pro parte, Caripia, Setulipes and Micromphale. Their /micromphale clade was nested within a broader /lentinuloid clade including Rhodocollybia, Marasmiellus ramealis (Bull.) Singer, Marasmius scorodonius (Fr.) Fr. and Lentinula. Mata et al. (2004), based on an LSU analysis, also identified a clade containing sequences of Micromphale foetidum and material named as Setulipes androsaceus (L.) Antonín and Gymnopus fusipes (Bull.) Gray, the type species of those respective genera. They adopted a broad concept of Gymnopus incorporating these genera together with Marasmiellus. Wilson and Desjardin (2005) used LSU to examine the group and identified a /gymnopus clade containing Gymnopus fusipes, Micromphale foetidum, Setulipes androsaceus at its core with Micromphale perforans (Hoffm.) Gray lying on its boundary. These results were broadly supported by Mata et al. (2006) in their analysis using ITS1–5.8–ITS2 but they demonstrate clustering of Gymnopus fusipes, Setulipes androsaceus and Micromphale on the periphery of a concentration of Gymnopus-labelled samples. On the basis of these results the currently generally accepted concept of Gymnopus is broad (e.g. Noordeloos 2012), and incorporates a number of previously recognised genera. Hughes et al. (2010) erected the genus Connopus to accommodate the Gymnopus acervatus group within the gymnopoid clade and presented LSU and ITS data indicating its placement close to Rhodocollybia. Their LSU analysis supports a core gymnopoid clade containing Gymnopus fusipes, Setulipes androsaceus, which once again places Micromphale foetidum and Micromphale perforans on a boundary with a sister group containing Rhodocollybia, Marasmiellus juniperinus Murrill and various Gymnopus species. The /gymnopus, cladeas interpreted by Hughes et al., contains significant substructure. A multi-gene analysis including more representatives may indicate the recognition of further segregates at genus-level. In this paper we accept our newly described species within the current broad concept of Gymnopus whilst recognising their close alliance to the historical concept of the genus Micromphale.

For this study we analysed ITS1–5.8–ITS2 data for related New Zealand collections together with representative sequences from Genbank, many from the studies cited above. The structure of our ITS tree is consistent with these previous analyses, and once again identifies a /micromphale clade closely linked to core Gymnopus species. ITS data generated for a number of representative collections of our newly described taxa support species concepts based on morphology.

Materials and methods
Morphological protocols

Spore dimensions are stated as the mean ± 1.5 SD of 20 measurements, thus covering 86% of measurements under an assumed normal distribution model. Fresh or dried material was examined mounted in 10% KOH or Melzer’s reagent. Material was hand-sectioned. Some micrographs were obtained under DIC conditions. Measurements were always taken without DIC optics and an extended objective iris in order to maximise boundary contrast.

Phylogenetic protocols

DNA extraction and sequencing followed the protocols outlined in Cooper and Leonard (2012). We downloaded from Genbank selected sequences used in cited publications, together with close BLAST matches, Table 1. General sequence management was carried out using Geneious (Drummond et al. 2011). Data exchange between applications was facilitated using Alter (Glez-Peña et al. 2010). Sequence alignment was carried out using MAFFT within Geneious (Katoh et al. 2002). A maximum likelihood analysis was executed using RAxML (Stamatakis 2006), with 100 bootstrap runs, launched from Topali 2.5 (Milne et al. 2004). The substitution model of GTR+G was recommended by Topali 2.5. We selected a sequence of Anthracophyllum archeri (Berk.) Pegler as the outgroup.

Table 1.

ITS Sequences used in the analysis. New sequences generated for this analysis are in bold.

Genbank # Collection # Organism PDD Voucher # Country
DQ444308 TENN50049 Anthracophyllum archeri New Zealand
DQ480112 TENN58672 Gymnopus alkalivirens Greenland
DQ480114 TENN55834 Gymnopus alpinus Scotland
AY256691 TENN57012 Gymnopus aquosus Germany
DQ449971 TENN59738 Gymnopus aquosus USA
KC248409 PL6304 Gymnopus ceraceicola PDD 101750 New Zealand
KC248389 PL126406 Gymnopus ceraceicola PDD 101754 New Zealand
KC248400 PL189402 Gymnopus ceraceicola PDD 76358 New Zealand
KC248403 JAC9334 Gymnopus ceraceicola PDD 80771 New Zealand
KC248405 JAC10084 Gymnopus ceraceicola PDD 87181 New Zealand
KC248404 JAC10336 Gymnopus ceraceicola PDD 87424 New Zealand
KC248394 JAC10395 Gymnopus ceraceicola PDD 87483 New Zealand
KC248408 JAC10817 Gymnopus ceraceicola PDD 87661 New Zealand
KC248392 RHP13063 Gymnopus ceraceicola PDD 90101 New Zealand
KC248391 KWH12891 Gymnopus ceraceicola PDD 90119 New Zealand
KC248393 RHP12871 Gymnopus ceraceicola PDD 90132 New Zealand
KC248397 JAC11005 Gymnopus ceraceicola PDD 95459 New Zealand
KC248395 JAC11093 Gymnopus ceraceicola PDD 95544 New Zealand
AY256690 TENN57012 Gymnopus dryophilus USA
DQ449974 TENN58087 Gymnopus dryophilus Costa Rica
AF505778 TENN59141 Gymnopus dysodes Costa Rica
AY256694 TENN59457 Gymnopus earleae USA
DQ449973 TFB10718 Gymnopus exculptus Greenland
AF505780 FB11434 Gymnopus foetidum USA
AY256710 TENN59217 Gymnopus fusipes France
KC248407 JAC9585 Gymnopus hakaroa PDD 81086 New Zealand
KC248410 JAC10225 Gymnopus hakaroa PDD 87315 New Zealand
KC248411 PL25404 Gymnopus imbricatus PDD 101753 New Zealand
KC248406 JAC10089 Gymnopus imbricatus PDD 87186 New Zealand
KC248398 JAC10310 Gymnopus imbricatus PDD 87398 New Zealand
KC248401 JAC10322 Gymnopus imbricatus PDD 87410 New Zealand
KC248399 JAC10815 Gymnopus imbricatus PDD 87659 New Zealand
KC248402 JAC10816 Gymnopus imbricatus PDD 87660 New Zealand
KC248396 JAC10495 Gymnopus imbricatus PDD 87675 New Zealand
KC248390 JAC11038 Gymnopus imbricatus PDD 95489 New Zealand
AF505779 TENN56658 Gymnopus impudicus Costa Rica
DQ449986 Duke RV94154 Gymnopus iocephalus USA
AY256693 TENN59532 Gymnopus junquilleus USA
DQ449960 TENN50620 Gymnopus ocior Switzerland
DQ449972 TENN56321 Gymnopus subsulphureus USA
AY263453 AWW115 Gymnopus vitellinipes Java/Bali
AY256708 TENN59540 Marasmiellus juniperinus USA
GU234007 JB14 Marasmius androsaceus Sweden
DQ444312 TENN50482 Marasmius androsaceus UK
DQ444311 TENN50704 Marasmius androsaceus USA
DQ449990 TENN59293 Micromphale brassicolens Austria
Results

Our analysis places the New Zealand taxa in a monophyletic clade close to Gymnopus foetidum and Gymnopus brassicolens historically recognised in the genus Micromphale (Fig. 1). The combination of sequence data and morphological analysis of many collections indicate two major groups which we equate with the newly described species Gymnopus imbricatus and Gymnopus ceraceicola. In addition we recognise a further species, Gymnopus hakaroa, which is poorly distinguished from Gymnopus imbricatus on the basis of ITS sequences but which is morphologically consistently different. Minor sequence variation in the Gymnopus ceraceicola group does not correlate with morphology and we choose to recognise these specimens as a single species. More information and images of collections may be found on the Landcare Research website (Systematics Collections Data).

Figure 1.

Maximum likelihood cladogram of selected ITS sequences, with bootstrap proportion. Red bar = Gymnopus imbricatus, green bar = Gymnopus hakaroa, blue bar = Gymnopus ceraceicola

Gymnopus ceraceicola J.A.Cooper & P. Leonard, sp. nov.

http://species-id.net/wiki/Gymnopus_ceraceicola

Holotype: PDD 87181. Registration identifier: IF550091

Diagnosis.

Gymnopus ceraceicola is distinguished from related New Zealand species by the combination of pruinose, central stipe and dark pileus.

Macromorphology.

Pileus 5–20 mm, generally broadly convex to applanate, but sometimes campanulate when young, brick to purplish chestnut, minutely felty, radially furrowed and striate towards the margin, margin slightly fimbriate. Lamellae cream, creamy yellow to vinaceous buff, waxy, adnate. Lamellae present, in series of three: intercalated short/long/short. Stipe central, cartilaginous, 10–20 × 1–2 mm, equal, brown vinaceous, sometimes paler towards apex or base, always entirely finely pruinose. Stipe base insititious and always associated with a thin waxy to chalky cream layer of partially gelatinised hyphae covering the substrate. This layer is often extensive, with a distinct margin, and often green with algal cells. Fruitbodies with garlic/rotten cabbage smell, especially when crushed.

Micromorphology.

Pileipellis a partially gelatinised radially arranged clamped cutis of smooth hyphae to 5 µm diameter, with brown extra-cellular encrustation. Epidermal layer to 140 µm. Subepidermis of thick glassy–walled non-gelatinised smooth hyaline hyphae, weakly dextrinoid. Basidia clavate to 40 × 8 µm. Sterigmata to 7 µm, 4–spored. Basidioles cylindrical, tapering towards apex, 40 × 4 µm. Spores hyaline, lacrymoid, 7.9 ± 1 × 4.5 ± 0.6 µm, Q = 1.8 ± 0.1 including apiculus. Cheilocystidia and pleurocystidia not observed. Stipitipellis a cutis of brown parallel hyphae, to 5 µm wide. Caulocystidia smooth, hyaline, agglutinated into fascicles.

Habitat.

Colonies of a few to hundreds of fruitbodies on bark of fallen, dead branches and twigs, especially Nothofagus.

Distribution.

Broadly distributed and common in both North and South Islands of New Zealand.

Etymology.

Ceraceicola, indicating association with a basal waxy layer, although this feature is common to the three species described here.

Notes.

Sequence data indicate variability in the taxon but the morphological details are constant and we choose to recognise a single species. New Zealand records of Gymnopus (Micromphale) foetidum and Gymnopus (Micromphale) brassicolens are attributable to Gymnopus ceraceicola. Authentic New Zealand material of these two species has not been identified. Gymnopus brassicolens has paler pileus colours, non-gelatinized pileipellis, cheilocystidia and pileipellis elements with lateral projections, and larger basidiospores. Gymnopus foetidus is macroscopically similar but does not possess the agglutinate fascicles of caulocystidia of Gymnopus ceraceicola.

Specimens examined.

New Zealand, North Island: PDD 40852, on dead wood, Anawhata Rd., Waitakare Ranges, Collector P.R. Johnston & G. Samuels, 9 June 1981. PDD 80771, on dead wood of Beilschmiedia tawa, Erua Forest, Taupo, Collector J.A. Cooper (JAC9334), 4 April 2005. PDD 87382, on dead wood of Nothofagus fusca, Mt Holdsworth, Gentle Annie Track, Wairarapa, Collector J.A. Cooper (JAC10294), 11 May 2007. PDD 87483, on wood, Mt Holdsworth, Donnelly Flat Loop Track, Wairarapa, Collector G. Gates & D. Ratkowsky (JAC10395), 7 May 2007. PDD 87424, on dead bark of Nothofagus, Mt Holdsworth, Gentle Annie Track, Wairarapa, Collector J.A. Cooper (JAC10336), 11 May 2007. PDD 95544, on bark of Nothofagus fusca, Rimutaka Forest Park, Wellington, Collector J.A. Cooper (JAC11093), 14 May 2009. PDD 95545, on bark of dead branch of Nothofagus fusca, Rimutaka Forest Park, Wellington, Collector J.A. Cooper (JAC11094), 14 May 2009.

New Zealand, South Island: PDD 76357, on dead twig of Nothofagus, Canaan Road Track, Nelson, Collector P.L. Leonard, 30 April 2002. PDD 96730, on dead wood, Wangapeka, Nelson, collector P.L. Leonard (PL126406), 14 April, 2006. PDD 90101=TENN 061068, on bark, vicinity of Seddonville, Charming Creek Track, Nelson, Collector R.H. Petersen (RHP 13063), 11 May 2006. PDD 76358, on bark on dead branch of Nothofagus menziesii, Lake Daniels Track, Nelson, Collector P.L. Leonard (PL189402), 2 April 2002. PDD 95459, on bark of dead branch of Nothofagus solandri, Kowai Bush, Springfield, Mid Canterbury, Collector J.A. Cooper (JAC11005), 2 May 2009. PDD 95462, on bark of dead branch of Nothofagus solandri, Kowai Bush, Springfield, Mid Canterbury, Collector J.A. Cooper (JAC11008), 2 May 2009. Holotype PDD 87181, on dead branch of Nothofagus fusca, Hinewai Reserve, Akaroa, Mid Canterbury, Collector J.A. Cooper (JAC10084), 3 June 2006. PDD 87661, on dead twigs of Leptospermum scoparium, Government Track, Waipori Falls Road, Dunedin, Collector K. Soop (JAC10817), 12 May 2008. PDD 96636, on dead wood of Nothofagus solandri, Lake Hauroko, Fiordland, Collector P. White (JAC12522). 7 May 2012. PDD 90119=TENN061007, on twigs, Vicinity of Te Anau, Kepler Track from Rainbow Reach, Fiordland, Collector K.W. Hughes (KWH12891), 30 April 2006. PDD 90132=TENN060986, vicinity Manapouri, Borland Lodge, Nature Track, Fiordland, Collector R.H. Petersen (RHP12871), 29 April 2006.

Figure 2.

Gymnopus ceraceicola Holotype, PDD 87181. Fruitbodies.

Figure 3.

Gymnopus ceraceicola Holotype, PDD 87181. A Spores (KOH) B Agglutinated fascicles of caulocystidia on stipe (KOH).

Gymnopus imbricatus J.A.Cooper & P. Leonard, sp. nov.

http://species-id.net/wiki/Gymnopus_imbricatus

Holotype: PDD 95489. Registration identifier: IF550092

Diagnosis.

Gymnopus imbricatus is distinguished from related New Zealand species by the smooth stipe, larger basidiospores, and imbricate habit.

Macromorphology.

Pileus 3–20 mm in diameter convex, cream to fawn, minutely felty, radially furrowed and striate towards the margin, margin fimbriate. Lamellae cream to creamy yellow, adnate. Lamellae present, in series of two: short/long. Stipe mostly eccentric, cartilaginous, to 3 × 0.5 mm, equal, umber to black, sometimes paler towards base, always entirely smooth. Stipe base insititious and usually associated with a thin waxy to chalky cream layer of partially gelatinised hyphae covering the substrate, usually green with algal cells. Fruitbodies with garlic/rotten cabbage smell, especially when crushed.

Micromorphology.

Pileipellis a partially gelatinised irregular clamped cutis of hyphae 4 µm diameter, without intra or extracellular pigmentation, terminal layer with gelatinised coralloid elements, to 2 µm wide, and occasional small finger-like trichodermal elements to 20 µm. Epidermal layer to 25 µm. Subepidermis of thick glassy-walled non-gelatinised smooth hyaline hyphae, weakly dextrinoid. Basidia clavate to 50 × 10 µm. Sterigmata to 5 µm, 4–spored. Basidioles to 50 × 6 µm cylindrical and tapered towards apex. Spores hyaline, lacrymoid 9.8 ± 1.2 × 5.1 ± 0.4 µm, Q = 1.9 ± 0.3 including apiculus. Cheilocystidia and pleurocystidia not observed. Stipitipellis a cutis of parallel brown hyphae, to 6 µm wide. Caulocystidia absent.

Habitat.

Forming imbricate colonies of dozens to hundreds of fruitbodies on bark and decorticate wood of dead branches and twigs, especially Kunzea and Leptospermum but occurs with other trees. Also occurs at the stem base of live trees.

Distribution.

Broadly distributed and common in both North and South Islands of New Zealand.

Etymology.

Imbricatus, pertaining to the often tiered and overlapping eccentrically stemmed caps.

Specimens examined.

New Zealand, North Island: PDD 80766, on bark of Beilschmedia tawa, Erua Forest, Taupo, collector J.A. Cooper (JAC9329), 4 April, 2005. PDD 87398, bark on dead branch of Nothofagus, Waiohine Gorge, Wairarapa, Collector J.A. Cooper (JAC10310), 10 May 2007. PDD 87410, dead stems of Ripogonum scandens, Waiohine Gorge, Wairarapa, Collector J.A. Cooper (JAC10322), 10 May 2007.

New Zealand, South Island: PDD 101753, dead branches of Nothofagus menziesii, Riwaka Resurgence, Nelson, Collector P.L. Leonard (PL25404), 10 April, 2006. PDD 96141, dead twigs of Kunzea ericoides, Mt Fyffe Track, Kaikoura, collector J.A. Cooper (JAC11734), 26 Feb. 2011. PDD 80154, dead log of Nothofagus menziesii, Lewis Pass, Buller, collector J.A. Cooper (JAC8287), 24 November, 2001. PDD 80157, on dead de-corticate log, Lyell Walkway, Nelson, collector J.A. Cooper (JAC80157), 25 November, 2001. PDD 87675, living stem of Fuchsia excorticata, Saddle Hill, Mid Canterbury, Collector J.A. Cooper (JAC10495), 22 May 2005. Holotype PDD 95489 (Figs 4 and 5), base of live trees of Kunzea ericoides, Kennedy’s Bush, Mid Canterbury, Collector J.A. Cooper (JAC11038), 24 May 2009. PDD 79799, bark of dead tree, Kennedy’s Bush, Mid Canterbury, Collector J.A. Cooper (JAC8921), 20 March 2004. PDD 87186, on bark of living tree of Kunzea ericoides, Hinewai Reserve, Akaroa, Mid Canterbury, Collector J.A. Cooper (JAC10089), 3 June 2006. PDD 87660, fallen log, Racemans Track, Silverstream Valley, Dunedin, Collector S. Dodd (JAC10816), 13 May 2008. PDD 87659, on dead twigs of Kunzea ericoides, Evansdale Glen, Dunedin, Collector P.R. Johnston (JAC10815), 12 May 2008.

Figure 4.

Gymnopus imbricatus. A Holotype PDD 95489. Fruitbodies, scale 1 cm B PDD 87186. Scale 1 mm.

Figure 5.

Gymnopus imbricatus Holotype PDD 95489. Spores (in KOH).

Gymnopus hakaroa J.A.Cooper & P. Leonard, sp. nov.

http://species-id.net/wiki/Gymnopus_hakaroa

Holotype: PDD 87315. Registration identifier: IF550093

Diagnosis.

Gymnopus hakaroa is distinguished from Gymnopus ceraceicola by smaller stature and a pruinose stipe lacking fascicles of agglutinate caulocystidia. It is distinguished from Gymnopus imbricatus by non-imbricate growth, a consistently central stipe, and smaller basidiospores.

Macromorphology.

Pileus 3–10 mm diam. convex, rusty tawny to umber, minutely felty, weakly radially furrowed and striate towards the margin. Lamella cream to yellow, waxy. Lamellae present, in series of three: intercalated short/long/short. Stipe central, cartilaginous, to 5 × 0.6 mm, equal, umber to black, paler towards base, smooth to minutely pruinose. Stipe base insititious and always associated with an obvious waxy to chalky cream layer of partially gelatinised hyphae covering the substrate, usually green with algal cells. Fruitbodies with garlic/rotten cabbage smell, especially when crushed.

Micromorphology.

Pileipellis a partially gelatinised radially arranged clamped cutis of smooth hyphae to 3 µm in diameter, with brown extra-cellular encrustation. Epidermal layer to 80 µm. Subepidermis of thick glassy-walled non-gelatinised smooth hyaline hyphae, to 3 µm in diameter, weakly dextrinoid. Basidia clavate to 40 × 8 µm. Sterigmata to 7 µm, 2–4-spored. Basidioles cylindrical and tapered towards apex 40 × 6 µm. Spores hyaline, lacrymoid 8.3 ± 1 × 4.8 ± 0.3 µm, including apiculus, Q = 1.7 ± 0.2. Cheilocystidia and pleurocystidia not observed. Stipitipellis a cutis of hyaline to pale brown hyphae, to 5 µm wide. Stipe without caulocystidia.

Habitat.

Forming imbricate colonies of dozens to hundreds of fruitbodies on decorticate dead wood.

Distribution.

Currently Gymnopus hakaroa is only known from a single location on the Canterbury Port Hills in the South Island of New Zealand.

Etymology.

Hakaroa, a Maori name for the Bank’s Peninsula region of New Zealand.

Notes.

Sequence data (Fig. 1) indicates a close phylogenetic relationship to Gymnopus imbricatus but there are consistent and substantial morphological differences.

Specimens examined.

New Zealand, South Island: Holotype PDD 87315 (Figs 6 and 7) on dead log, Kennedys Bush Reserve, Port Hills, Mid Canterbury, Collector J.A. Cooper (JAC10225), 11 Feb. 2007. PDD 81086 (Fig. 8), on dead wood of Kunzea ericoides, Kennedys Bush Reserve, Port Hills, Mid Canterbury, Collector J.A. Cooper (JAC9585), 23 July, 2007. PDD 96390, on dead decorticate log of Melicytus ramiflorus, Kennedys Bush Reserve, Port Hills, Mid Canterbury, Collector J.A. Cooper (JAC11301), 17 April, 2010.

Figure 6.

Gymnopus hakaroa A PDD 81086. Fruitbodies B scale= 2 mm

Figure 7.

Gymnopus hakaroa Holotype PDD 87315. Fruitbodies, showing waxy substratum.

Figure 8.

Gymnopus hakaroa Holotype PDD 87315. Spores (KOH).

Figure 9.

Gymnopus hakaroa PDD 96390. Stipe base (arrow) with surrounding algal mat. Inset, primordial arising from algal mat.

Figure 10.

Gymnopus hakaroa PDD 96390. Pockets of algal cells embedded in hyphal tissue of stem base (cotton blue stain).

Dicussion

Gymnopus imbricatus, as its name suggests forms dense populations of small imbricate fruitbodies. It is most commonly associated with tea-tree (Kunzea ericoides and Leptospermum scoparium) and often found on the bark at the base of living trees. Gymnopus hakaroa is larger, with a dark minutely pruinose cap and again forms dense populations on the bark of dead logs. These two species have smooth stems. Gymnopus ceraceicola is distinguished by larger fruitbodies, a pruinose stipe, and is more commonly associated with southern-beech forests on dead fallen logs. The species of Gymnopus described here belong in the /micromphale clade of Moncalvo et al. (2002) and share the diagnostic feature of this clade of a foetid odour likely due to the presence of mercaptan-like compounds. In New Zealand this feature is shared with Mycetinis curraniae (G. Stev.) J.A. Cooper & P. Leonard, a marasmioid fungus distinguished by its ornamented hymeniderm pileipellis. Another very distinctive character common to all three Gymnopus species, and visible in the accompanying photographs (Figs 2 and 6), is the presence of a waxy layer of partially gelatinised hyphae on the substrate from which the fruitbodies emerge. This layer is usually green from the presence of embedded algal cells. Interestingly, some published images of Gymnopus foetidus in the northern hemisphere also show a similar layer, e.g. Antonín and Noordeloos (2010). Detailed examination of our material does show algal cells deeply embedded within the context of the waxy layer and the basal portion of the stipe (Figs 9 and 10), but it would seem unlikely that algal cells are present in sufficient numbers to confer any significant nutritional benefit to the fungus. The morphologically similar Marasmiellus affixus (Berk.) Singer, described from Australia and commonly known as the ‘little stinker’, is also associated with a waxy algae-infected layer. The association of Marasmiellus affixus with alga was noted by Singer (1973) and has been speculated to be a basidio-lichen, although this has not proven (Lepp 2011). A partial, poor quality ITS1 sequence for Marasmiellus affixus obtained during this work (not deposited) suggests it has affinity with Marasmiellus ramealis (Bull.) Singer rather than the taxa treated here.

Acknowledgements

Thanks to Dukchul Park, Landcare Research, for DNA extraction and sequencing, and to Sapphire McMullen-Fisher for material of Marasmiellus affixus. The New Zealand Department of Conservation is thanked for permission to collect specimens from reserves and national parks that they manage. The first author was supported through the Landcare Research Systematics Portfolio, with Core funding support from the Science and Innovation Group of the New Zealand Ministry of Business, Innovation and Employment.

References
Antonín V, Noordeloos ME (2010) A Monograph of Marasmioid and Collybioid fungi in Europe, IHW-Verlag.
Cooper JA, Leonard PL (2012) Boletopsis nothofagi sp. nov. associated with Nothofagus in the Southern Hemisphere. MycoKeys, 3: 13-22. doi: 10.3897/mycokeys.3.2762
Drummond AJ, Ashton B, Buxton S, Cheung M, Cooper A, Duran C, Field M, Heled J, Kearse M, Markowitz S, Moir R, Stones-Havas S, Sturrock S, Thierer T, Wilson A (2011) Geneious v5.4. Available from: http://www.geneious.com/
Glez-Peña D, Gómez-Blanco D, Reboiro-Jato M, Fdez-Riverola F, Posada D (2010) ALTER: program–oriented format conversion of DNA and protein alignments. Nucleic Acids Research 38 (2): 14-18. doi: 10.1093/nar/gkq321
Hughes KW, Mather DA, Petersen RH (2010) A new genus to accommodate Gymnopus acervatus (Agaricales). Mycologia, 102: 1463-1478. doi: 10.3852/09-318
Katoh K, Misawa K, Kuma K, Miyata T (2002) MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Research 30: 3059-3066. doi: 10.1093/nar/gkf436
Lepp H (2011) Is Marasmiellus affixus a Lichen? Fungimap Newsletter 44: 14.
Mata JL, Hughes KW, Petersen RH (2004) Phylogenetic placement of Marasmiellus juniperinus. Mycoscience 45: 214–221. 10.1007/s10267-004-0170-3
Mata JL, Hughes KW, Petersen RH (2006) An investigation of /omphalotaceae (Fungi: Euagarics) with emphasis on the genus Gymnopus. Sydowia 53: 191-289.
Matheny PB, Curtis JC, Hofstetter V, Aime MC, Moncalvo J-M, Ge ZW, Yang ZL, Slot JC, Ammirati JF, Baroni TJ, Bougher NL, Hughes KW, Lodge DJ, Kerrigan RW, Seidl MT, Aanen DK, Dentis M, Danielle G, Desjardin DE, Kropp BR, Norvell LL, Parker A, Vellinga EC, Vilgalys R. Hibbett DS (2006) Major clades of Agaricales: a multi-locus phylogenetic overview. Mycologia, 98: 982-995. doi: 10.3852/mycologia.98.6.982
Milne I, Wright F, Rowe G, Marshal DF, Husmeier D and McGuire G (2004) TOPALi: Software for Automatic Identification of Recombinant Sequences within DNA Multiple Alignments. Bioinformatics 20 (11): 1806-1807. doi: 10.1093/bioinformatics/bth155
Moncalvo JM, Vilgalys R, Redhead SA, Johnson JE, James TY, Aime MC, Hofstetter V, Verduin SJW, Larsson E, Baroni TJ, Thorn RG, Jacobsson S, Clémençon H, Miller OK (2002) One hundred and seventeen clades of euagarics. Molecular Phylogenetics and Evolution 23: 357-400. doi: 10.1016/S1055-7903(02)00027-1
Noordeloos ME (2012) Gymnopus (Pers.) Roussel. In Knudsen H, Vesterholt J (Eds) (2012) Funga Nordica, p. 341–349, Nordsvamp, Copenhagen.
Singer R (1973) A Monograph of the Neotropical Species of Marasmiellus. Beih. Nova Hedw. 44: 1-339.
Singer R (1986) Agaricales in modern taxonomy. 4th Ed., Cramer, Koenigstein.
Stamatakis A (2006) RAxML-VI-HPC: Maximum Likelihood-based Phylogenetic Analyses with Thousands of Taxa and Mixed Models. Bioinformatics 22 (21): 2688-2690. doi: 10.1093/bioinformatics/btl446
Wilson AW, Desjardin DE (2005) Phylogenetic relationships in the gymnopoid and marasmioid fungi (Basidiomycetes, euagarics clade). Mycologia 97: 667-679. doi: 10.3852/mycologia.97.3.667