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Research Article
Tremella rhizocarpicola sp. nov. and other interesting lichenicolous Tremellales and Filobasidiales in the Nordic countries
expand article infoAna Millanes, Paul Diederich, Martin Westberg§, Tommy Knutsson|, Mats Wedin§
† Universidad Rey Juan Carlos, Mostoles (Madrid), Spain
‡ Musée national d’histoire naturelle, Luxembourg, Luxembourg
§ Swedish Museum of Natural History, Stockholm, Sweden
| Nedre Västerstad 111, Mörbylånga, Sweden
Open Access

Abstract

New data on the diversity and geographical distribution of lichenicolous Tremellales and Filobasidiales in the Nordic countries is presented. One new species, Tremella rhizocarpicola, is formally described. Tremella pertusariae and T. protoparmeliae are reported as new to the Nordic countries, Syzygospora physciacearum is new to Iceland, Tremella rinodinae is new to Sweden, and T. caloplacae is new to Norway. Nine species are reported as new to a number of Swedish provinces, including Biatoropsis usnearum, Syzygospora bachmannii, S. physciacearum, Tremella caloplacae, T. cetrariicola, T. cladoniae, T. coppinsii, T. diploschistina, and T. hypogymniae.

Key words

Basidiomycota, Biatoropsis, new species, new records, Scandinavia, Syzygospora

Introduction

Fungal mycoparasites, including lichen-parasites, are common among the Tremellomycetes (Basidiomycota, Fungi). Lichen-inhabiting species belong to the genera Biatoropsis, Tremella (both Tremellales) and Syzygospora (Filobasidiales). There are currently 50 lichenicolous species described in the group (Diederich 1986, 1996, 2003, Sérusiaux et al. 2003, Diederich 2007, Zamora et al. 2011, Millanes et al. 2012), and an additional five are known but have not yet been formally named (Diederich 1996, 2007). The actual diversity and distribution of lichen-inhabiting species is still largely unknown, as comparatively few mycologists and lichenologists collect lichenicolous fungi. Some tremellalean species are relatively easy to spot in the field as they induce the formation of conspicuous galls on the hosts, whereas others grow only inside the host hymenium producing few or no external symptoms. In these cases, study of host herbarium material is extremely useful for diversity surveys, and also improves our knowledge on the geographical distribution of taxa that are otherwise much overlooked in the field. In the Nordic countries, 15 tremellalean lichenicolous species have been reported so far (Nordin et al. 2014). During fieldwork in Sweden and Norway, and herbarium surveys undertaken in BG, S, and UPS, during 2012–2014, we found material allowing one new species to be formally described and several species to be newly reported to the Nordic countries, Iceland, Norway or Sweden.

Methods

Macromorphological traits were observed using a Zeiss Stemi 2000-C dissecting microscope. Microscopic structures were studied using handmade sections stained with Phloxin (1% in water) after pre-treatment with KOH (5%), following the methods of Diederich (1996), and observed with a Zeiss Axioscope-2 microscope. Macro- and microscopic photographs were taken with a Nikon Coolpix 995 camera fitted to both microscopes. The apiculus is not included in basidiospore measurements. Sizes in parentheses represent minimum and maximum observed values.

Results

Tremella rhizocarpicola Diederich, Millanes & Wedin, sp. nov.

MycoBank No: 809897

Description

Basidiomata inside the hymenium of the host, resulting in blackish swellings of the host apothecia; context hyphae difficult to observe, 2.5–3.5 mm thick, thin walled, with clamp connections; haustorial branches not observed. Hymenium hyaline, containing numerous probasidia, intermixed with the hymenium of the host; probasidial initials clavate, proliferations occurring through the basal clamp; hyphidia and cystidia absent. Basidia, when mature, narrowly ellipsoid to subcylindrical, with one transverse septum (never oblique or longitudinal), slightly constricted at the septum, the lower cell elongate, with an attenuated stalk-like base, (14–)17–44 × 7–12(–13) mm (incl. stalk); epibasidia 3–3.5 mm thick, up to 65 mm long. Basidiospores subglobose, with a large apiculus, 7.5–9.5 × 6–8.5 mm. Anamorph: conidial chains sometimes present in the hymenium. Individual conidia 3–5 × 3–5 mm.

Type

NORWAY, Rogaland, Suldal, on the N side of lake Stranddalsvatnet. On N facing phylitic rock, 59°26.26'N, 6°43.48'E, ca. 1000 m, 18 Aug 1999, P.G. Ihlen 957 (BG: L-68612).

Distribution, ecology and host

The new species is known from one locality in Denmark, two localities in Norway, and nine in Sweden, all growing inside the hymenium of Rhizocarpon lavatum on siliceous rocks, often along shorelines or near water.

Discussion

The species was tentatively described by Diederich (1996: 170) as Tremella sp. 3. The single specimen known at that time was very small, but the discovery of 12 additional collections from Denmark, Sweden and Norway (Fig. 1A) is now enough for a formal description. There is little to add to the description and illustrations given by Diederich (1996), however. The only novelties are the wider range of basidium width and length (Fig. 1G) and the presence, occasionally, of an anamorph consisting of catenulate conidia. A sequence of the ITS barcode region is not provided, since recently collected specimens were too reduced for DNA extraction, and old specimens could not be amplified by PCR. Diederich (1996) indicated that this species was microscopically very similar to Tremella protoparmeliae, but T. rhizocarpicola could be distinguished by the formation of dark brown swellings on the host apothecia and by small differences in the size of the basidia. The additional specimens studied here show that there is an anamorph formed by catenulate conidia in T. rhizocarpicola, and the basidia of this species can be comparatively shorter and wider than those of T. protoparmeliae.

Figure 1.

Photographs of new species or records for the Nordic countries, Norway, and Sweden. Macroscopic habit of Tremella rhizocarpicola on Rhizocarpon lavatum (holotype, BG: L-68612) (A), T. pertusariae on Pertusaria hymenea (S: F-131626) (B), T. protoparmeliae, asymptomatic on Protoparmelia badia (S: F-255342) (C), T. caloplacae on Caloplaca decipiens (S: F-253110) (D), T. caloplacae on Xanthoria parietina (S: F-253109) (E), and T. rinodinae on Rinodina gennarii (S: F-255341) (F). Basidium morphology in Tremella rhizocarpicola (G), T. pertusariae (H), T. protoparmeliae (I), T. caloplacae (S: F-255314) (J), and T. rinodinae (K–L). Scale bars: 1 mm (A–F) and 10 mm (G–L).

Additional specimens examined

(all on Rhizocarpon lavatum): DENMARK. Faroe Islands: Nordoya, Bordö, Klaksvig, N end of Bordö Vig, rivulet Gravarå, 4 Sept 1956, G. Degelius (UPS: L-662460). – NORWAY. Oslo: Ekeberg, 13 May 1886, N.G. Moe (BG: L-58000). Rogaland: Suldal, on the north side of lake Stranddalsvatnet, 59°26.26'N, 6°43.48'E, ca. 1000 m, 18 Aug 1999, P.G. Ihlen 957 (BG: L-68612). – SWEDEN. Bohuslän: Foss, 1851, M.M. Floderus (UPS: L-662426). Bohuslän: Solberga, Rörtången, 10 June 1928, A.H. Magnusson 11329 (UPS: L-662425). Bohuslän: Ödsmål, Korsgården, 1 Aug 1931, A.H. Magnusson 12851b (UPS: L-662448). Bohuslän: Spekeröd, Groland, 28 Aug 1955, A.H. Magnusson 24616b (UPS: L-662457). Halland: Övraby, Sperlingsholm, 3 July 1851, T.M. Fries (UPS: L-132524). Halland: Tölö, Skårby, Valåsberget, 24 May 1925, A.H. Magnusson 9384b (UPS: L-662453). Halland, Karup par., SE of Båstad, on boulder in the river Kägleån, 10 Oct 1970, M. S. Christiansen 6498 (C). Härjedalen: Tännäs, Tännfallet waterfall in Tännån, 11 km NW of Tännäs, 62°29.04'N, 12°29.19'E, 6 July 2012, J. Hermansson 18827 (UPS: L-597926). Småland: Malmbäck, Älgaryd, 1875, P.G.E. Theorin (UPS: L-131500). Uppland: Danmark par., Linnés Hammarby, 2.4-2.5 km SE of Danmark church, the hill NE of the houses, 59°49.02'N, 17°46.59 E, 25 m. 15 Sept 2007, G. Thor 22045 (UPS: L-167626).

New records to the Nordic countries

Tremella pertusariae Diederich

Note

This species was previously recorded in Europe (Belgium, France, Germany, Great Britain, Ireland, Italy, and Spain), where it is very common in the western Pyrenees, and in America (Mexico and U.S.A) (Diederich 1996). Knutsson and Johansson (2011) reported it from Sweden, but with some hesitation since the material could not be identified microscopically. The five additional specimens reported here confirm the presence of the species in the Nordic countries. The fungus forms pale to dark brown or blackish galls, generally on the apothecia of Pertusaria hymenea (Fig. 1B), but also on the thallus of both P. hymenea and P. pertusa, and bears characteristic stalked basidia (Fig. 1H).

Specimens examined

(all on P. hymenea). DENMARK. Jylland: Fredrikkshavn, W of Pikkerbakken, 20 June 1947, A.H. Magnusson 20958b (UPS: F-661189). – SWEDEN. Småland: Femsjö par., Femsjö, 1859, T.M. Fries (UPS: F-661180). Småland: Växjö par., Växjö, Jan 1880, E. Köhler (UPS: L-661177). Skåne: Oppmanna par., Bokenäset, July 1916, E.P. Vrang (S: F-131626). Skåne: Oppmanna par., Bokenäset, 19 July 1943, G. Degelius (UPS: L-661197). Öland: Ås par., Södra Ottenby lund, ”Skogsudden”, on ancient Quercus robur, in oak-dominated deciduous forest. 56°12.98’N 16°24.80’E 16 Feb 1999, T. Knutsson 99-092 (private herb.)

Tremella protoparmeliae Diederich & Coppins

Note

This species was previously only recorded in England (Diederich 1996). The fungus grows intrahymenially on Protoparmelia badia, without producing any external symptoms, which suggests that this species could in reality be common, but much overlooked as it is not visible macroscopically (Figs 1C and 1I).

Specimens examined

(all in the hymenium of Protoparmelia badia). SWEDEN. Torne Lappmark: Jukkasjärvi par., Ábeskosuolo, south-eastern part to the island, facing the shore of the lake, 68°21.88'N, 18°50.17'E, 29 July 2013, A. Millanes 915 & M. Méndez (S: F-255342). Uppland: Djurö par., Runmarö, Small hill at the NW end of the Lake Viträsket, 59°16.44'N, 18°45.91'E, 27 Aug 2011, A. Millanes, S. Klopfstein & M. Westberg (S: F-255343).

New records to Iceland, Norway or Sweden

Syzygospora physciacearum Diederich

Note

New to Iceland and to the Swedish provinces Öland, Södermanland, and Västergötland.

This species is widely distributed, with numerous records in Africa, America, Asia, and Europe (Diederich 1996, van den Boom and Alstrup 1996, van den Boom et al. 1998, Motiejūnaitė 1999, van den Boom and Giralt 1999, Halonen et al. 2000, Kukwa et al. 2002, Himelbrant et al. 2013, Urbanachivene et al. 2013). In the Nordic countries it has been recorded in Finland, Norway, Sweden and Denmark (Diederich 1996, Puolasmaa et al. 2008, Hemberg 2013).

Specimens examined

ICELAND. W of Reyðarfjörður, lake Lagarfljót, SW of Hallormsstaður, Atlavík cove, W of Atlavík camping, siliceous rock outcrops in native Betula forest, on Physcia tenella subsp. marina, 4 Aug 2013, P. Diederich 17521 (private herb.). SWEDEN. Södermanland: Tyresö par., before the entrance of Tyresta National Park, on dead Populus, on Physcia adscendens, 56°10.26'N, 18°14.2'E, 3 m, 5 Apr 2014, A. Millanes 1028, S. Fernández-Brime & M. Westberg (S: F-255317). Västergötland: Österplana par., Mt. Kinnekulle, Österplana hed, E of Nyängarna, 58°33.83 N, 13°24.5'E, 140 m, on Fraxinus, on Physcia tenella, 4 May 2009, M. Wedin 8392 (S: F-255318). Öland: Smedby par., Nedra Västerstad, garden in the N. part of the village., on old Syringa sp., on Physcia tenella, 56°25’27 N, 16°24’47 E, 29 Jan 2011, T. Knutsson 2011-002 (private herb.).

Tremella caloplacae (Zahlbr.) Diederich

Note

New to Norway and to the Swedish province Torne Lappmark.

The species was at first tentatively described as Tremella sp. 1 by Diederich (1996) and eventually formally described by Sérusiaux et al. (2003). It has been reported from Austria, Canada, France, Great Britain, Greece, Greenland, and Spain (Diederich 1996, 2007, Sérusiaux et al. 2003), growing inside the hymenia, or exceptionally on the thallus, of different Caloplaca species, viz. C. arenaria, C. arnoldii, C. aurantia, C. carphinea and C. saxicola (Diederich 1996, Sérusiaux et al. 2003), and on the thallus of Xanthoria sorediata (Diederich 2007). It was recently reported as new to the Nordic countries (Thell et al. 2014) from two Swedish collections, growing on new hosts: Caloplaca decipiens (on the thallus; Fig. 1D) and Xanthoria parietina (inside the hymenium; Fig. 1E). Here it is reported on a new host (Xanthoria elegans), in Sweden. All samples below are on X. elegans, growing inside the hymenium or on the thallus. All specimens bear two-celled basidia (Fig. 1J) and are very similar microscopically. Further investigations are needed, however, to check if all specimens growing on Teloschistaceae belong to a single species.

Specimens examined

(all on Xanthoria elegans): NORWAY. Oppland: Lom municipality, Runningsgrende, Kleive, 61°42.95'N, 8°14.05'E, 720–850 m, 29 June 2013, A. Millanes 808 (S: F-255312). – SWEDEN. Torne Lappmark: Jukkasjärvi par., Paddos, 68°19.16'N, 18°51.93'E, 625 m, 28 Aug 2013, A. Millanes 904 & M. Méndez (S: F-255313). Torne Lappmark: Jukkasjärvi par., Paddos, 68°19.13'N, 18°51.89'E, 596 m, 28 Aug 2013, A. Millanes 908 & M. Méndez (S: F-255314).

Tremella rinodinae Diederich & M. S. Christ.

Note

New to Sweden.

This fungus was previously known only from Denmark (Diederich 1996). It grows in the hymenium of Rinodina gennarii, forming distinct brown swellings on the host apothecia (Fig. 1F). The basidia have one transverse (Fig. 1K), or exceptionally longitudinal (Fig. 1L), septum.

Specimens examined

(all in the hymenium of Rinodina gennarii): SWEDEN. Bohuslän: Skaftö par., Östersida, 3 Aug 1928, G. Degelius (UPS: L-87926). Skåne: Oppmanna par., Arkelstrop, July 1916, E.P. Vrang (S: F-255341).

Records new to some provinces in Sweden

Biatoropsis usnearum Räsänen

Note

New to Bohuslän.

This species has a wide distribution and has been recorded in all Nordic countries except Iceland (i.e., Denmark, Finland, Norway, and Sweden) (Diederich and Christiansen 1994, Nordin et al. 2014).

New specimen examined

SWEDEN. Bohuslän, Kville/Tanum pars., following Torsbo stream, low part of the cliff, mixed forest with Alnus, Betula, Corylus, Picea and Salix, on Usnea sp., 58°47.55'N, 11°8,4'E, 14 Apr 2013, A. Millanes 695 (S: F-255315).

Syzygospora bachmannii Diederich & M.S. Christ.

Note

New to Gotland and Medelpad.

This material had been placed in S long ago, but as the specimens have apparently not been published or otherwise recorded elsewhere, we report them here. The species had been previously recorded in the Nordic countries, particularly in Sweden and Finland (Diederich 1996).

New specimens examined

SWEDEN. Gotland: Sundre par., ca 1 km SE of Sundre church, along small track 500 m S Muskmyr, open limestone pavement (‘alvar’), on the ground, on Cladonia macroceras, 56°55'N, 18°12'E, M. Wedin 6802 (S: F-102481). Gotland: Klinte, on alvar ground, on C. macroceras, 7 May 1937, T.E. Hasselrot (S: F-255268). Medelpad: Selånger par., on rests of rotten plants on the surface of a small stone, next to the ground, in forest, on C. cornuta, 60 m, 25 Nov 1928, E. Eriksson (S: F-161742).

Tremella cetrariicola Diederich & Coppins

Note

New to Dalarna, Norrbotten, and Ångermanland.

In the Nordic countries this species has been recorded in Finland, Norway and Sweden (Diederich 1996, Pippola and Kotiranta 2008).

New specimens examined

(all on Tuckermanopsis chlorophylla). SWEDEN. Dalarna: Mockfjärd par., ca. 1.2 km WNW Bastberget, 60°22.64'N, 14°55.73'E, 220 m, 28 Sept 2010, M. Westberg 10-116 (S: F-255319). Norrbotten: Norrfjärden par., Lustgården Nature Reserve, 65°32.76'N, 21°26.41'E, 25 Aug 2009, M. Wedin 8491 (S: F-255320). Norrbotten: Norrfjärden par., ca. 5.5 km NNW of Sjulsmark, along a forest road to the lake Hällträsket close to the beginning of the road Abborrtjärnvägen, 65°34.19'N, 21°27.35'E, 28 Aug 2009, M. Wedin 8566 (S: F-255333). Ångermanland: Örnsköldsvik, Västanåhöjden, at turnoff towards Västanåbodarna, old Picea-dominated forest, 63°10.42'N, 18°14.33'E, 21 July 2010, M. Wedin 8763 (S: F-255322).

Tremella cladoniae Diederich & M.S. Christ.

Note

New to Öland.

In the Nordic countries this species has been reported from Denmark, Finland, and Sweden (Diederich 1996, Pippola and Kotiranta 2008, Westberg and Thor 2014).

New specimen examined

SWEDEN. Öland: Böda par., Trollskogen, Norra Uddändan, between Hjerteskeppet and Grankullavik, on semi-dead Juniperus, on Cladonia polydactyla and C. coniocraea, 57°21.38'N, 17°6.91'E, 24 Jan 1998, T. Knutsson 98-013 (private herb.).

Tremella coppinsii Diederich & G. Marson

Note

New to Bohuslän, Dalsland, Dalarna and Västergötland.

The species has previously been recorded in the Scandinavian Peninsula, i.e., Norway and Sweden (Holien and Tønsberg 1994, Diederich 1996).

New specimens examined

(all on Platismatia glauca). SWEDEN. Bohuslän: Kville/Tanum pars., following Torsbo stream, low part of a cliff, mixed forest with Alnus, Betula, Corylus, Picea and Salix, on Alnus, 58°47.55'N, 11°8.4'E, 14 Apr 2013, A. Millanes 694 (S: F-255266). Dalarna: Mockfjärd par., ca. 1.2 km WNW Bastberget, 60°22.73'N, 14°55.96'E, 240 m, 28 Sept 2010, M. Westberg 10-114 (S: F-255324). Dalsland: Dals-Ed par., Torstorp, 1.6 km NW Knä sjö, on Sorbus aucuparia at the edge of mixed forest 58°50.55'N, 12°5.9'E, 28 Nov 2013, T. Knutsson (private herb.). Västergötland: Trollhättan par., S of Lake Åkersjö, close to the lock, Picea dominated forest with Quercus, Acer and Corylus, on Picea, 58°28.74'N, 11°36.19'E, 15 Apr 2013, A. Millanes 710 (S: F-255325). Västergötland: Trollhättan par., Brandsbo Nature Reserve, mixed forest with Alnus, Corylus, Quercus, Picea, and Salix, along a stream (very humid area), 58°28.64'N, 11°35.33'E, 11 m, 15 Apr 2013, A. Millanes 725 (S: F-255326).

Tremella diploschistina Millanes, M. Westb., Wedin & Diederich

Note

New to Öland.

In the Nordic countries the species has been so far only reported from Sweden (Millanes et al. 2012).

New specimens examined

(all on Diploschistes muscorum): SWEDEN. Öland: Stenåsa par., Stenåsa alvar, SSW of lake Möckelmossen, 56°40.28'N, 16°23.02'E, 27 Apr 2013, T. Knutsson 2013-018 (S: F-255327). Öland: Resmo par., Gynge alvar, ca. 2,0 km E of Resmo church, 56°32.52'N, 16°28.6'E, 6 May 2014, M. Westberg 14-001 (S: F-255349).

Tremella hypogymniae Diederich & M.S. Christ.

Note

New to Bohuslän, Dalarna, Norrbotten, Pite Lappmark, and Torne Lappmark.

This is a widely distributed species. In the Nordic countries it has been reported from Denmark, Finland, Norway, and Sweden (Diederich 1996, Alstrup et al. 2004, 2008, Pippola and Kotiranta 2008).

New specimens examined

(all on Hypogymnia physodes). SWEDEN. Bohuslän: Tanum par., Lammön, on the way to Lammön, mixed forest with Pinus and Quercus, on dead branch of Quercus, 58°59.63'N, 11°5.39'E, 13 Apr 2013, A. Millanes 664 (S: F-255328). Dalarna: Mockfjärd par., ca. 1.2 km WNW Bastberget, 60°22.72'N, 14°55.94'E, 28 Sept 2010, M. Westberg 10-115 (S: F-255348). Dalarna: Älvdalen par., Gummas Nature Reserve, 61°19.2'N, 13°31.7'E, 29 Sept 2010, M. Wedin 8778 (S: F-255329). Dalarna: Orsa par., Mt. Stora Tunturiberget, 61°22.66'N, 14°49.44'E, 30 Sept 2010, M. Wedin 8796 (S: F-255331). Dalarna: Rättvik par., N of the village Västberg, at the parking lot ca. 50 m S of the E end of Lake Ammtjärnen, on Picea, 60°94'N, 15°08'E, 21 Apr 2012, A. Millanes 610 (S: F-255330). Norrbotten: Norrfjärden par., ca. 5.5 km NNW of Sjulsmark, along a forest road to the lake Hällträsket close to the beginning of the road Abborrtjärnvägen, 65°34.19'N, 21°27.35'E, 28 Aug 2009, M. Wedin 8564 (S: F-255321). Pite Lappmark: Arvidsjaur par., ca. 19 km NE of Moskosel, NE slope of N Granberget, 65°57.76'N, 19°48.83'E, 27 Aug 2009, M. Wedin 8544 (S- F-255332). Torne Lappmark: Jukkasjärvi par., Kungsleden, way to Abiskojaure, after ‘Tältlägret’ on a dead trunk of Betula, 68°19.05'N, 18°44.25'E, 453m. 31 Aug 2013, A. Millanes 946 (S: F-255334).

Acknowledgements

This study is part of the research project “Tremellales in Sweden” funded by the Swedish Taxonomy Initiative (Svenska artprojektet) administered by the Swedish Species Information Center (ArtDatabanken). Mika Bendiksby, Astri Botnen, Reidar Haugan, Einar Timdal and Tor Tønsberg are warmly thanked for organizing and funding fieldwork in Norway. Marcos Méndez and Jan Olsson provided excellent field guiding in Torne Lappmark and Bohuslän, respectively. We are grateful to the staff of BG, S, and UPS for making collections available and arranging loans, and to Laura Williams who very kindly revised the English of this manuscript.

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