Journal of Threatened Taxa | www.threatenedtaxa.org | 26
September 2019 | 11(12): 14619–14623
Australasian sequestrate Fungi
20: Russula scarlatina
(Agaricomycetes: Russulales: Russulaceae),
a new species from dry grassy woodlands of southeastern
Australia
Todd F. Elliott 1 & James M. Trappe 2
1 Ecosystem
Management, University of New England, Armidale, New
South Wales 2351, Australia.
2 Department of
Forest Ecosystems and Society, Oregon State University, Corvallis, Oregon
97331-5752, USA.
2 USDA Forest
Service, Pacific Northwest Research Station, Forestry Sciences Laboratory, 3200
Jefferson Way, Corvallis, Oregon 97331, USA.
1 toddfelliott@gmail.com
(corresponding author), 2 trappej@gmail.com
Abstract: Russula scarlatina sp. nov. is a common
sequestrate fungus found in the dry sclerophyll Eucalyptus woodlands of southeastern Australia.
Basidiomata are hypogeous
or sometimes emergent; they are scarlet in youth and become dark sordid red or
brown with advanced age. Historically,
this species would have been placed in the genus Gymnomyces,
but in light of recent revisions in the taxonomy of sequestrate Russulaceae, we place it in the genus Russula. It is morphologically distinct from other
sequestrate species of Russula because of its
scarlet peridium and unusual cystidial turf in
youth. It has been collected only in dry
grassy woodlands and open forest habitats of southeastern
Australia.
Keywords:
Basidiomycota, Eucalyptus, hypogeous fungus,
grassy woodlands, open forests, Russulaceae, southeastern Australia.
doi: https://doi.org/10.11609/jott.4907.11.12.14619-14623
Editor: Anonymity
requested. Date of
publication: 26 September 2019 (online & print)
Manuscript details: #4907 | Received 19 February
2019 | Final received 09 September 2019 | Finally accepted 13 September 2019
Citation: Elliott, T.F. & J.M. Trappe (2019). Australasian sequestrate Fungi 20: Russula
scarlatina (Agaricomycetes: Russulales:
Russulaceae), a new species from dry grassy woodlands
of southeastern Australia. Journal of Threatened Taxa 11(12): 14619–14623. https://doi.org/10.11609/jott.4907.11.12.14619-14623
Copyright: © Elliott & Trappe 2019. Creative Commons Attribution
4.0 International License. JoTT allows unrestricted use, reproduction, and
distribution of this article in any medium by adequate credit to the author(s)
and the source of publication.
Funding: The Mycological Society of America, the North American
Truffling Society, the CSIRO Division of Ecosystem
Services (Canberra), Australian Capital Territory Parks, and the Victoria
Department of Environment, Water, Heritage and Arts all contributed travel
grants that enabled us to explore large areas of eastern Australia in search of
sequestrate fungi. The School of
Environmental and Rural Science at the University of New England provided
facilities and an International Postgraduate Research Scholarship to the first
author.
Competing interests: The authors declare no competing
interests.
Acknowledgements:
We appreciate the support and
encouragement of the Marshall family of Terra Preta
Truffles, Dr. Tim Roberts and the Tom Farrell
Institute of the University of Newcastle, and the Stricklands
of Walnut Creek Preserve. Expert
collectors who helped in the field include Andy Murray of Omeo,
Victoria, Jacqui Stol of CSIRO Canberra, and the
Claridge family (Andrew, Debbie, Georgia, and Ben) of Canberra. We are grateful for editorial insights
provided by Kelsey Myers Elliott. We
would also like to thank the following herbaria for accessioning our holotype,
isotypes, and paratype collections: Australian National Herbarium (CANB), New
South Wales Plant Pathology and Mycology Herbarium (DAR), Oregon State
University (OSC), Royal Botanic Gardens Victoria (MEL).
Non-lactating sequestrate members of the Russulaceae were historically placed in one of six genera
based on various aspects of their morphology (Lebel 1998). Recent genetic analysis supports the recombination
of all of these genera with the common mushroom genus Russula
(Lebel & Tonkin 2007; Lebel 2017; Elliott & Trappe 2018). It has been
suggested that adaptations to abiotic environmental factors and symbiotic
associations with vertebrates and invertebrates have led to evolution of
sequestrate and hypogeous basidiomata
(Thiers 1984; Trappe & Claridge 2005; Vernes
& Dunn 2009; Galante et al. 2011).
Nearly 60 of the approximately 145 described sequestrate Russula species are native to Australia and
New Zealand, and numerous undescribed taxa likely inhabit the region (Lebel
1998; Lebel & Tonkin 2007; Lebel 2017; Elliott & Trappe 2018). Australia also has a high diversity of native
mammals and birds that feed on members of the Russulaceae
(Nuske et al. 2017a,b; Elliott & Vernes 2019). These
associations between vertebrates and the Russulaceae
may have contributed to the evolution of the diverse sequestrate morphologies
that are common in Australia.
During multiple collecting expeditions in the
Australian Capital Territory, New South Wales, and Victoria, we have
encountered Russula scarlatina
sp. nov., a brightly colored,
sequestrate fungus. It typically fruits
with Eucalyptus spp. in dry sclerophyll woodlands, but we once found it
emerging from bare, compacted soil between the base of a tree and the sidewalk
in Mitchell, New South Wales.
Materials and Methods
Basidiomata examined in this study were collected during the cold
months of May through September between 2000 and 2010. We found them by raking away the leaf litter
under Eucalyptus spp. and carefully examining the soil layer below. Occasionally, basidiomata
were partially emergent from the soil or were found in the tailings piles of
animal digs. We collected and photographed
the basidiomata, recorded their fresh macroscopic
characteristics, and then placed slices on a portable dehydrator. Dried material was freehand sectioned for
slide mounts under a binocular compound microscope. Thin sections were mounted and examined in 3%
KOH, H2O, cotton blue, and Melzer’s reagent. Heat was used to remove bubbles and for
clearer viewing. Microscopic features
were measured in 3% KOH mounts.
Collections are curated in the herbaria listed in the Acknowledgements
section.
Taxonomic description
Russula scarlatina sp. nov.
MycoBank Number: MB 829958
(Image 1)
Holotype: Australia, Australian Capital Territory, Mulligans
Flat Nature Reserve, 55H 6106140, 696255, elev. 645m. In pure grove of Eucalypus
blakelyi. Col. Ben Claridge, Georgia Claridge,
Debbie Claridge, Andrew Claridge, & Jim Trappe #33233 (CANB; Isotypes OSC,
MEL).
Etymology: scarlatina (Latin, “scarlet”), referring to the scarlet peridium
covered with a turf of scarlet dermatocystia; a
conspicuous feature distinguishing this species from other sequestrate Russula spp.
Description: Basidiomata hypogeous to partially
emergent or sometimes exposed in animal digs, solitary or in scattered,
gregarious groups. Basidiomata
globose to subglobose, flattened, or irregular,
(5–) –25 (–30) x (5–) –20 (–25) mm, in youth with a suprapellis
turf of scarlet, tapered cystidia that fade when dried and a pellis mixture of pale yellow and scarlet areas that often
separate into patches, with age the colors darkening
to darker dull red and the turf fading and collapsing in patches, at senescence
becoming dark reddish-brown with the suprapellis turf
largely to entirely collapsed (Image 1a).
Stipe absent or rarely present as a less than 2mm long, readily
detaching stub at base of fruiting body, its surface concolorous
with peridiopellis.
Gleba loculate, in
youth, the trama white to ivory or pale yellow, with
age developing to brownish yellow with brown zones and brown tissue around worm
holes, and at senescence brown overall (Image 1a & c); spores in mass in
the locules white, often brownish where glebal tissue has stained brown. Odor in youth mild,
later often faintly pleasant, at senescence somewhat unpleasant.
Peridium 115–180 µm thick, beset with a crowded to
dispersed, scarlet pubescence. Peridiopellis 25–90 µm
thick, scarlet in fresh mounts of young specimens and often with scattered red
granular deposits near the surface, later darkening to brown or reddish-brown
and paler towards gleba, the hyphae compact and
tightly entangled, 4–8 µm broad, the suprapellis a
pubescence of tapered, tangled, cystidia 20–40 µm tall, scarlet when fresh and
sometimes with scattered scarlet deposits at the base but fading slowly after
exposure, in microscope mounts of KOH quickly becoming hyaline (Image 1d). Subpellis averaging
90µm thick with loosely interwoven hyphae 3–8 µm thick. Gleba with a
subhymenium up to 30µm thick, composed of irregularly
shaped, inflated cells up to 11µm broad.
Hymenophoral trama up to 18–31 µm
thick, composed of tightly intertwined hyphae, 3–7 µm broad with occasional
cells in trama inflated up to 18µm. Hymenophoral cystidia 39–42 x 8–11 µm,
scattered, hyaline smooth, cylindrical to narrowly clavate with obtuse apices,
walls less than 1µm thick (Image 1f).
Basidia 41–48 x 9–11 µm, clavate, tapering near the base, smooth, less
than 1µm thick, 2 and 4 spored, sterigmata 4–6 x 1–2
µm. Spores 7–8 x 7–9 µm, globose to subglobose with sterigmal
attachment no more than 1µm long tapering towards the tip, spore wall less than
0.5µm thick, becoming slightly thicker near sterigmal
attachment. Spore ornamentation less
than 1µm tall, weakly amyloid, ranging from irregular granules to a
well-developed reticulum (Image 1e).
Habitat and
Distribution
Primarily restricted to dry sclerophyll woodlands and
open forest habitats from the Warrumbungle Mountains
and New England Tablelands south through the South West Slopes, tablelands, and
Riverina of New South Wales, and through the grassy
woodlands of central and coastal Victoria at elevations of 10–678 m and
fruiting between May and September.
Associated trees are typically various mixtures of Acacia spp.,
Allocasuarina luehmannii,
Callitris endlicheri,
Eucalyptus albens, E. blakeleyi,
E. bridgesiana, E. camaldulensis,
E. goniocalyx, E. leucoxylon,
E. macrorhyncha, E. mannifera,
E. melliodora, E. microcarpa,
E. macrorhyncha, E. polyanthemos,
E. populinea, E. sideroxylon,
and E. tricarpa. We have often encountered this species in
nearly monodominant stands of E. blakeley, E. camaldulensis or E. microcarpa. The types of woodlands where R. scarlatina is commonly encountered vary considerably
from North to South within its range: for example, the intensely studied
box-gum grassy woodlands of the Australian Capital Territory (McIntire et al.
2010) and the Gippsland red gum grassy woodland in the Moormurng
Flora and Fauna Reserve in the coastal sand plains near the Gippsland Lakes of
Victoria (Australian Department of Environment 2010). The resilience and adaptability of R. scarlatina is graphically illustrated by collection
35049 (Mitchell, ACT) which was emergent on bare, compacted soil under an
unidentified planted Eucalyptus sp. at the edge of the sidewalk. All other collections were from more intact
albeit often degraded woodlands or open forests.
Paratypes: Australia, Australian Capital Territory: Goorooyaroo Nature Reserve, 55H 699328 N, 6103996 E, elev.
695 m, Trappe 32837, 9 Sep 2008 (OSC 158775, CANB); Mitchell, Hoskins St. T.
Elliott, Trappe 35049, 2 Sep 2010 (CANB).
NEW SOUTH WALES: Benambra Nature Reserve, from
Holbrook on Mountain Creek Rd. 4.5km from Mullengandra
Rd., J. Trappe 31627.1 & B. Skoro, 1 Aug 2006 OSC
158771, CANB); Burrinjuck Nature Reserve SE of Yass,
P. Thrall, Trappe 31959, 28 Jun 2007 (OSC 158774, CANB) Murray River, Cottadidda State Forest, under Eucalyptus camaldulensis, R. Strömmer
& J. Trappe 25209, 3 Jun 2000 (OSC 158744, CANB). Kosciuszko National Park,
Barry Way 0.5km N of Pinch River crossing, Claridge Site 6, Jacobs Mapsheet Grid 625600 Easting 5927350 Northing, under Acacia
implexa & Eucalyptus albens,
A. Jumpponen, AWC 3305, 14 May 2001 (OSC 158814,
CANB) Parkes Shire, Genaren Farm, Genaren
Hill Sanctuary near N boundary fence, Tullamore map 8432-1 & 4, AMG 579900
E, 6396200 N, under Eucalyptus dealbata, E.
sideroxylon, Acacia doratoxyon,
A. deanii, and Callitris
glaucophylla, J. Trappe 26478, 22 Jun 2001 (OSC
158757, CANB); Riverina, Kilpa
Farm, 17.5km SE of Berrigan, under Eucalyptus microcarpa.
R. Strömmer, J. Trappe 25144, 4 Jun 2000
(OSC 158741); Savernake Station, Horse Paddock, 26.5km N of Mulwala, under Eucalyptus melliodora,
and E. microcarpa, J. Trappe 25197, 4
Jun 2000 (OSC 158743, CANB); Womboyne Farm N
of Barooga, under Acacia sp., J. Trappe
25368, 28 Jun 2000 (OSC 158754, CANB); Wandook
Traveling Stock Route 10km W of Deniliquin, 35027’47”S, 14500’40”E,
elev 90m, J. Trappe
28651, 16 Jul 2003 (OSC 158765, CANB); Warrumbungle
National Park, E of Visitors Center, T. Elliott,
Trappe 35062, 3 Sep 2010 (DAR). Weddin Mountains
National Park, Weddin Gap, AMG 592950 E, 6241050 N,
J. Trappe 26437, 19 Jun 2001 (OSC 158756, DAR). VICTORIA: Chiltern Box-Ironbark
National Park, Donchi Hill Rd, R. Strömmer
& J. Trappe 25219, 6 Jun 2000 (OSC 158745); East Gippsland, Moormurng Flora and Fauna Reserve, Leathams
Dam Rd, T. Elliott, Trappe 35049, 26 Aug 2010 (OSC 158812, MEL); Maldon State
Forest, Red White and Blue Track 1.7km S from Pullens
Rd, AMG 242534 E, 5895655 N, elev 300m, J. Trappe
27595, 9 July 2002 (OSC 158759, MEL), Reef Hills Regional Park, Roes Rd., by
pond, under Eucalyptus albens, J. Trappe 25263,
7 Jun 2000 (OSC 158749, MEL).
Discussion
Russula scarlatina is easy to recognize in the field because of its
vibrant scarlet peridium, totally enclosed loculate gleba, and lack of a stipe; these characters set it apart
from other members of the genus. Some Arcangeliella (sequestrate Lactarius) species appear somewhat similar but are
readily distinguished from R. scarlatina. The most similar of these taxa have bright
orange (not scarlet) peridia and lactate and/or have laticiferous
hyphae, unlike R. scarlatina. Other distinctive characters of R. scarlatina include unusually short spore ornamentations
that are weakly amyloid and a distinctive peridiopellis
turf; furthermore, this species has been found only in dry sclerophyll
woodlands and open forest habitats.
Russula theodoroui (T. Lebel) T. Lebel sometimes has reddish to scarlet
peridia, but it differs from R. scarlatina in
having a short but prominent stipe, a pileopellis
epithelium of inflated cells (but lacking a turf of dermatocystidia),
and larger spores (8–10 x 8–9.5 µm) with much larger and more strongly amyloid
ornamentation. Because of its peridiopellis of inflated cells, R. theodoroui
had earlier been placed in the genus Cystangium
but now is in the genus Russula (Lebel
2017; Elliott & Trappe, 2018). Russula theodoroui has never been collected south of
Queensland, whereas R. scarlatina has not been
collected north of the Warrumbungle Mountains of New
South Wales.
Russula westresii (T. Lebel) T. Lebel is one of the more common and
widespread species in eastern Australia and resembles R. scarlatina
in having a brown staining gleba, spores with
short ornamentation, and sometimes orange to brick red streaks and patches on
an otherwise yellowish-white to pale brownish-yellow peridium (but not the
overall scarlet of R. scarlatina). Russula westresii also lacks a peridiopellis
turf of dermatocystidia, and its spores are larger
(8–10 x 7.5–9 µm) than those of R. scarlatina.
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