Research Article |
Corresponding author: Heidi L. Andersen ( heidi.andersen@uib.no ) Academic editor: Imke Schmitt
© 2019 Per M. Jørgensen, Heidi L. Andersen, Arve Elvebakk.
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:
Jørgensen PM, Andersen HL, Elvebakk A (2019) The genus Massalongia (lichenized ascomycetae) in The Southern Hemisphere. MycoKeys 60: 125-140. https://doi.org/10.3897/mycokeys.60.37725
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The species of Massalongia recorded and described from the Southern Hemisphere are revised and it is shown that only one is present; M. patagonica which is widespread, with populations in Australia and New Zealand that differ from the South American populations, but at present best regarded as part of the variation of that species. Records from this hemisphere of all other species placed in the genus are incorrect. The type species, M. carnosa, is restricted to the Northern Hemisphere. Two species, M. antarctica and M. novozelandica cannot be identified precisely due to lack of sufficient type material and with the types as the only collections known of these, but none belongs in Massalongia according to available data. Massalongia griseolobata (from Gough Isl.) is shown here to belong in the Pannariaceae and is part of the parmelielloid clade. M. intricata (from South Georgia) and M. olechiana (from South Shetland) have both recently been correctly transferred to the genus Steinera in the Arctomiaceae.
Peltigerales, Massalongiaceae, phylogeny, taxonomy, South Hemisphere
The genus Massalongia was described by
The situation in the Southern Hemisphere is different, though it took a long time before any species in the genus was recognised.
During fieldwork in Chile in 2015, one of the authors (A.E.) discovered a strange Pannaria-like lichen which, on closer inspection, proved to be a Massalongia with some differences from M. carnosa, as known by us from Norway. However, since this is a variable species, we felt that a more detailed study, including molecular screening, would be useful. This being done and the distinction of this material proven, we found it necessary to check on the surprisingly high number of species of Massalongia described from the Southern Hemisphere. This proved to be time-consuming and complicated, since it was difficult to get hold of suitable material and, when molecularly checked, often not giving clear results and involving quite unrelated lichen families. Fortunately,
Specimens of Massalongia were obtained from various herbaria for phylogenetic analyses, see Tables
List of specimens used for phylogenetic analyses of the broad analysis of the Massalongiaceae and Pannariaceae, with vouchers and accession numbers from GenBank. Bold accession numbers are new in this study.
Species and ID | Voucher | mtSSU | RPB1 |
---|---|---|---|
Austrella arachnoidea | Jørgensen 8200 (BG) | KC608054 | KC608108 |
Collema furfuraceum | Wedin 6187 (BM) | AY340488 | GQ259048 |
Collema nigrescens | Wedin 7046 (UPS) | GQ259020 | GQ259049 |
Collema parvum | Nordin 5500 (UPS) | GQ259021 | GQ259050 |
Degelia duplomarginata | Wedin 8023 (S) | KC608058 | – |
Degelia durietzii | Elvebakk 02-296 (TROM) | KC608059 | – |
Degelia gayana | Wedin 6112 (UPS) | AY652619 | – |
Degeliella rosulata | Galloway 840b (BG) | KC608063 | – |
Degeliella versicolor | Galloway 840a (BG) | KC608064 | – |
Erioderma pedicellatum | mrSSU: MacPitcher s.n. 2007 (BG-L85909), RPB1: MacPitcher s.n. 2007 (BG-L85911) | KC608065 | KC608110 |
Erioderma verruculosum | AFTOL-ID 337 | DQ972990 | DQ973062 |
Fuscoderma applanatum | Tibell 19076 (BG) | KC608112 | KC608066 |
Fuscopannaria pacifica | Tønsberg 29359 (BG) | KC608074 | KC608118 |
Fuscopannaria praetermissa | mrSSU: Tønsberg 36838 (BG) RPB1: Wedin 7671 (UPS) |
KC608075 | GQ259056 |
Joergensenia cephalodina | Passo 269 (BCRU 4895) | EU885330 | – |
Lecidea fuscoatra | Wedin 6860 (UPS) | AY756401 | AY756408 |
Leciophysma furfurascens | Nordin 5695 (UPS) | GQ259028 | GQ259058 |
Leioderma erythrocarpum | Schumm and Frahm s.n. 2009 (BG, dupl of hb. Schumm 15583) | KC608078 | – |
Leioderma pycnophorum | Wedin 8013 (S) | GQ259031 | GQ259059 |
Leptochidium albociliatum | Tønsberg 29087 (BG) | DQ900632 | GQ259060 |
Muggia TSB38886 | JF938191 | – | |
Spribille 20997 (COLO) | JF938193 | – | |
Lobaria pulmonaria | mrSSU: Wedin 6167 (UPS) RPB1: Wedin 5092(UPS) |
AY340503 | GQ259068 |
Lobaria scrobiculata | AFTOL-ID 128 | AY584621 | DQ883736 |
Massalongia carnosa | Tønsberg 44267 (BG) | MN708314 | MN714653 |
Tønsberg 45410 (BG) | MN708315 | MN714654 | |
Johnsen L-86694 (BG) | MN708316 | – | |
Ezhkin 1289 (SAK) | MN708317 | MN714655 | |
Spribille 22021 (COLO) | JF938205 | – | |
Haikonen 20961 (H) | EU558817 | – | |
Hermansson 8916 (UPS) | AY340509 | GQ259071 | |
Spribille 21565 (COLO) | JF938204 | – | |
Massalongia patagonica | Elvebakk 99:775 (TROM) | MN708318 | MN714656 |
Elvebakk 15:033 (SGO) | MN708319 | MN714657 | |
Buck 60287 (NY) | MN708320 | MN714658 | |
Gremmen K-789 (BG) | MN708321 | MN714659 | |
Galloway 5616 (CHR) | MN708322 | MN714660 | |
Galloway s.n. (CHR) | MN708323 | MN714661 | |
Kitaura 4181 (CGMS) | MG243608 | – | |
Kitaura 4188 (CGMS) | MG243607 | – | |
Kitaura 4168 (CGMS) | MG243609 | – | |
Massalongia griseolobata | Gremmen 2006-91 (BG) | MN708324 | – |
Nephroma parile | Wedin 6169 (UPS) | AY340512 | GQ259072 |
Pannaria hookeri | Jørgensen s.n. (BG) | KC608083 | KC608124 |
Pannaria immixta | Elvebakk 02-352b (BG) | KC608084 | KC608125 |
Pannaria rubiginella | Thor 10050 (S) | GQ259037 | GQ259074 |
Parmeliella appalachensis | Lendemer 578 and Smith (BG) | KC608090 | – |
Parmeliella miradorensis | Tønsberg 23053 (BG) | KC608094 | KC608136 |
Parmeliella nigrocincta | Elvebakk 02-356 (BG) | KC608095 | KC608137 |
Parmeliella pannosa | Ståhl s.n. 1999 (BG) | KC608096 | – |
Parmeliella triptophylla | Wedin 7037 (UPS) | AY652623 | GQ259075 |
Pectenia atlantica | Lindblom and Blom L251 (BG) | KC608057 | KC608109 |
Pectenia cyanoloma | Purvis, James and Smith 1995 (BM) | AY340491 | GQ259052 |
Pectenia plumbea | AFTOL-ID 1046 | DQ912300 | DQ912374 |
Placynthium nigrum | Wedin 6778 (UPS) | AY340518 | GQ259079 |
Polychidium muscicola | Obermayer 8547 (UPS) | DQ900634 | GQ959080 |
Spribille 26411 (KLGO) | JF938220 | – | |
Pseudocyphellaria aurata | Purvis, James and Smith 7/5/1995 (BM) | AY340520 | GQ259082 |
Psoroma hypnorum | Ihlen 453 (BG) | KC608100 | KC608142 |
Santessoniella arctophila | Kristinsson s.n. (BG) | KC608104 | KC608145 |
Sticta fuliginosa | Wedin 6078 (BM) | AY340529 | GQ259089 |
Vahliella carnifornica | Tønsberg 26316 and Goward (BG) | HQ268594 | HQ268593 |
Vahliella leucophaea | Wedin 6849 (UPS) | AY652621 | GQ259090 |
List of specimens used for phylogenetic analyses of the species delimitation in Massalongia, M. referring to Massalongia, P. to Polychidium and L. to Leptochidium, with vouchers and accession numbers from GenBank. Bold accession numbers are new in this study.
Species and ID | Voucher | Area | ITS | LSU | mtSSU | RPB1 |
M. carnosa | Tønsberg 44267 (BG) | USA: Alaska | MN708327 | MN708327 | MN708314 | MN714653 |
Tønsberg 45410 (BG) | USA: Alaska | MN708328 | MN708328 | MN708315 | MN714654 | |
Johnsen L-86694 (BG) | Norway | MN708329 | MN708329 | MN708316 | – | |
Ezhkin 1289 (SAK) | East Russia | MN708330 | MN708330 | MN708317 | MN714655 | |
Spribille 22021 (COLO) | USA: Montana | – | – | JF938205 | – | |
Hermansson 8916 (UPS) | Sweden | – | AY340554 | AY340509 | GQ259071 | |
Rui andTimdal 13267 (O) | Norway | MG243601 | – | MG243611 | – | |
Hansen 1138 (COLO, H) | Greenland | MG243599 | MG243615 | MG243610 | – | |
Hansen 1057 (H) | Greenland | MG243603 | MG243616 | MG243612 | – | |
Türk 17280 (H) | Austria | MG243602 | MG243614 | MG243613 | – | |
M. patagonica | Elvebakk 99:775 (TROM) | Chile | MN708331 | MN708331 | MN708318 | MN714656 |
Elvebakk 15:033 (SGO) | Chile | MN708332 | MN708332 | MN708319 | MN714657 | |
Buck 60287 (NY) | Chile | MN708333 | MN708333 | MN708320 | MN714658 | |
Gremmen K-789 (BG) | Australia | – | – | MN708321 | MN714659 | |
Galloway 5616 (CHR) | New Zealand | MN708334 | MN708334 | MN708322 | MN714660 | |
Galloway s.n. (CHR) | New Zealand | MN708335 | MN708335 | MN708323 | MN714661 | |
Kitaura 4181 (CGMS) | Argentina | MG243604 | MG243617 | MG243608 | – | |
Kitaura 4188 (CGMS) | Argentina | MG243606 | MG243619 | MG243607 | – | |
Kitaura 4168 (CGMS) | Argentina | MG243605 | MG243618 | MG243609 | – | |
P. muscicola | Obermayer 8547 (UPS) | Austria | – | DQ900647 | DQ900634 | GQ259080 |
L. albociliatum | Tønsberg 29087 (BG) | USA | – | DQ900644 | DQ900632 | GQ259060 |
Total genomic DNA was extracted using DNeasy Plant Mini Kit (Qiagen). Four DNA markers where amplified; the mitochondrial small subunit rDNA (mtSSU rDNA: primers mrSSU1 and mrSSU3R (
PCR reactions consisted of 1× GeneAmp PCR Buffer II (Applied Biosystems), 2.5 µM MgCl2 (Applied Biosystems), 20 µM dNTPs (Promega), 0.4 µM of each primer, 0.03 U AmpliTaq DNA Polymerase (Applied Biosystems), 2–5.0 µl of genomic DNA extract and distilled water to a total volume of 25 µl. PCR reactions were performed on a C1000 Touch thermal cycler (Bio-Rad Laboratories), with the following temperatures; initial denaturation at 94 °C for 4 min, followed by a 62–56 °C touchdown annealing for the first 6 cycles, ending with 30 cycles at 56 °C for 30 sec, polymerisation at 72 °C for 1 min 45 sec and a final elongation at 72 °C for 10 min.
Direct sequencing of PCR products was run with the PCR primers using a BigDye Terminator Cycle Sequencing kit (Applied Biosystems) on an ABI Prism 3700XL DNA analyser (Applied Biosystems) at the DNA Sequencing Facility (UiB), Norway. Sequences were assembled and edited using Geneious v.11.0.2 (
Newly generated sequences with GenBank accession numbers are listed in Tables
To align the sequences, MAFFT v7.309 (
Two different datasets were analysed; one broad analysis of Massalongiaceae and Pannariaceae to test whether the included species is part of Massalongia (Table
Separate analyses of all genes and concatenated datasets were run as Bayesian MCMC searches using MrBayes v.3.2.1 (
The two resulting concatenated datasets consisted for the broad analysis of Massalongiaceae and Pannariaceae of 63 taxa with 1435 characters, whereas for the species delimitation in Massalongia, of 21 taxa with 2983 characters (details in Table
List of numbers of characters, taxa and constant variables, from the two concatenated datasets.
Dataset | Numbers of characters | Numbers of taxa | Number of constant characters | Number of variable characters |
Broad analysis of the Massalongiaceae and Pannariaceae | 1435 | 63 | 724 | 711 |
Species delimitation in Massalongia | 2983 | 32 | 2745 | 238 |
The resulting phylogenetic consensus tree from the broad analysis of Massalongiaceae and Pannariaceae are given in Fig.
The resulting phylogenetic consensus tree from the species delimitation analysis of Massalongia is given in Fig.
The samples of M. patagonica from New Zealand are grouped in a separate subclade from the rest of the samples from Australia, Chile and Argentina. The phylogenetic tree indicates a high genetic variance within M. patagonica throughout the Southern Hemisphere, but further studies are necessary to evaluate these differences.
The samples from the Northern Hemisphere make a monophyletic clade with little variation between the samples and a sample from Sweden is practically identical to those analysed from Alaska and Greenland.
The only species from the Southern Hemisphere which, according to our data belongs in Massalongia, is M. patagonica, the details of which are as follows:
Massalongia patagonica Kitaura & Lorenz in Liu et al., Sydowia 70: 249–252 (2018) – Holotypus: Argentina, Ushuaia, National Park of Tierra del Fuego, Lapataia Bay, muscicolous on the rock, 54°50'41.42"S, 68°33'52.31"W, 6 m alt., 25 December 2016, leg.M.J.Kitaura, J.Bordin, A.A.Spielmann & D.Peralta 4188 (CGMS).
M. patagonica (Fig.
Thallus foliose, forming rosettes up to 3 cm, mostly muscicolous; lobes 0.5–1.5 mm broad, up to 1 cm long, irregularly and repeatedly divided with isidioid marginal outgrowths, simple to sparingly branched, sometimes developing into branched lobule systems, lobules, 0.1 mm wide. Upper surface brown, glabrous and glossy; upper cortex 20–30 µm thick, paraplectenchymatic, of thick-walled (ca. 1.5–2 µm wide) cells with 7–12 µm large lumina; photobiont layer 40–60 µm thick, often also developed in the subhymenium; cyanobiont Nostoc, cells bluish-green, irregularly subglobose to ellipsoid, 5–9 × 6–11 µm in size, arranged within 20–40 µm large glomeruli without visible chain structures, chain structures visible in some liberated cells; medulla loose, 60–80 µm thick; lower cortex absent, with scattered rhizohyphae.
Apothecia common to scattered, substipitate, laminal, 1–2 mm wide; thalline excipulum lacking, true excipulum weakly prominent; epithecium 5–10 µm thick, of protruding brown and strongly swollen, pyriform paraphyse end cells, 4–6 µm wide, 7–10 µm long, paraphyses undivided to sparingly divided, 2–4 µm thick; hymenium ca. 60 µm thick, IKI + blue; asci clavate 50–70 × 10–15 µm, 8-spored, with distinct internal apical IKI + blue sheath-like structures, sometimes also with weak tube structures; ascospores narrowly ellipsoid, occasionally asymmetric, 1- to 2 (3)-septate, (13) 20–25 (28) × 5–7.5 µm. Hypothecium ca. 60 µm thick, weakly brownish, IKI negative. Conidiomata not seen.
All reactions negative, no lichen substances detected by TLC.
This is a species of wet to dry rock surfaces or boulders, usually growing in between mosses or on plant remains. It has a widely scattered distribution in South America, ranging from the temperate forests of south-central Chile, including the Juan Fernandez Islands and Patagonia, with two widely separated collections from southernmost Chile and Argentinean Tierra del Fuego. In addition, it is known from the Falkland Islands, Antarctica, mountains of SE Australia, where it is rare and from several localities in New Zealand.
Antarctica: South Shetland Islands, King George Isl., Admiralty Bay, creeping slopes above Paradise Cove, 26 Jan 1980, R. Ochyra 1224/80 (BG, H); Urbanek, Crag between Polar Committee Glacier and Ladies Icefall, in Ezcurra Inlet, 20 Feb 1980, R. Ochyra 2319/80 (BG, H).
Argentina: Patagonia: Chubut, Lago Verde, near Futalaufquen, 1 Feb 1950, I. M. Lamb 5877 (over mosses on a rock in open scrub, about 30 m above the lake), 5880 (over mosses on a rock in open forest about 15 metres above the lake) (CANL, UPS).
Australia: New South Wales, near the summit of Mt. Guthrie, Kosciusko National Park, on moss over granite rocks, 9 Feb 1978, J.A. Elix 4360 (CANB); Kosciusko National Park, near Digger’s Creek, 21 Jan 1976, J. A. Elix 1722 (CANB); Île Australia near Kerguelen Isl., on moss cushions, 492823S, 695329E, 45 m alt., 31 Dec 2003, NJM Gremmen, K-789 (BG).
Chile: IX Región de la Araucanía: Reserva Nacional Malalcahuello, W bank of Río Colorado, 500 m W of the Entrance/CONAF building and 200 m S of the junction between the paths Sendero Coloradito and Sendero Sierra de Colorado; 38°25'45"S, 71°32'44"W, 1380 m alt., over Grimmia mosses on a S-facing rock outcrop in a Nothofagus dombeyi-Araucaria araucana forest, probably affected by river water during high flooding events, 9 Jan 2015, A. Elvebakk 15:033 (SGO, BG, UPS, BM, TROM); Archipiélago de Juan Fernandez: Isla Alejandro Selkirk (Mas Afuera), Los Innocentes, 4 Dec 1965, H. Imshaug (MSC); Valdivia, Corral, R. Thaxter (MSC); XII Región de Magallanes y de la Antárctica Chilena, Provincia Magallanes, Morro Chico, 52°03'S, 71°28'W, 200 m alt., on acrocarpous mosses on a NW-facing rocky slope, 28 Nov 1999, A. Elvebakk 99:775 (TROM); Provincia Antártica Chilena, Comuna Cabo de Hornos, Isla Grande de la Tierra del Fuego, Bahía Yendegaia, NNE shore opposite Caleta Ferrari, 54°50'28"S, 68°47'52"W, 13 Jan 2013, W.R. Buck 60287 (NY 01886528).
Falkland Islands: W. Falkland, Chartres, Luxton NNR, 30 Jan 2015, A. Fryday 10999 (MSC).
New Zealand: Canterbury, Cass, between Sugar Loaf and Cass Hill, 761 m alt., 18 Feb 1991, A. J. Fife 9761 (CHR); Banks Peninsula, Mt. Sinclair, summit, 5 Feb 1970, D. J. Galloway (CHR); Mt. Cook National Park, D. J. Galloway (CHR); Otago, Deep Stream, above DCC water intake, 13 Feb 1998, D. J. Galloway 0170 (CHR); Otago, Old Man Range, N of Obelisk, 5 Feb 2009, D. J. Galloway 404009 (CHR); St. Mary’s Range, Anakin’s Skifield, 22 Feb 2006, D. J. Galloway (CHR); Lake Onslow near huts, amongst moss in drainage cracks of schist rock in grassland, 30 Jul 1998, D. J. Galloway 404012 (CHR); Otago, Pomahaka River- Hukarere, rock slabs above river, 13 Apr 1998, D.J. Galloway 404011 (CHR); North Rough Ridge, near “Great Tor”, 12 Apr 1998, D. J. Galloway (CHR).
The other taxa originally described from the Southern Hemisphere as Massalongia species, are listed alphabetically, according to the epithet at the end of the discussion.
The result of the phylogenetic analyses of Massalongia (Fig.
That species is also found as far west as the Juan Fernandez Islands and is also possibly present on the Antarctic Peninsula and the Bouvet Island, but the material examined was sparse, sterile and too old for molecular studies.
Still, M. patagonica is not morphologically easily distinguished from M. carnosa; the two species have different spores, although there is an overlap zone in both length and degree of septation. Both species have a gross morphology showing high variation, probably due to habitat modifications, depending on light exposure, competition, moisture and water availability.
Chilean material of M. patagonica tends to have thicker, narrower and clearly radiating lobes than most material of M. carnosa. However, in cases where habitat information is available, they appear to be dry, but exposed to nutrient supplies by spring flooding (the Río Colorado collection), wind-transported saline lake dust (the Morro Chico collection) or seashore spray (the Tierra del Fuego collection). The New Zealand material, on the other hand, treated as M. carnosa, is cited as widespread and from moist habitats by
This detailed phylogenetic signal within M. patagonica is the result of a long history of evolution and isolation in austral areas, although shorter than the split-up between M. carnosa and M. patagonica. There is a record of M. carnosa from Mt. Kinabalu on Borneo (
The examination of all relevant material from the Southern Hemisphere, shows the following, treated alphabetically according to the epithet:
Massalongia antarctica
Dodge is a species only known from the type specimen from Lambda Island at the tip of the Antarctic Peninsula (Siple 380c-2, FH!). The type specimen is minute and sterile and consists of two different species, none of which belongs in Massalongia. The one fitting best with the description has a crustose, hemi-gelatinous thallus in accordance with species of the Arctomiaceae. There are no apothecia present in the collection and the description of the apothecia, given by
Massalongia griseolobata
Øvstedal is a species only known from the type specimen (from Gough Isl., coll. Gremmen 2006-91, BG!). Even if only incipient apothecia were found, we do not hesitate to place this species in the Pannariaceae, based on morphology and the original description of the asci. They are recorded to have apically blue in tholus in iodine with a weak ring-structure. (Massalongia has sheet-like structures,
Massalongia intricata
Øvstedal was correctly transferred to the genus Steinera by
Massalongia novozelandica
Dodge was recorded by
Massalongia olechiana
Alstrup and Søcht. was correctly transferred to the genus Steinera in the Arctomiaceae by
Massalongia patagonica
Kitaura and Lorenz, the recently described species (Fig.
From these facts, we conclude that there is only one, widespread species of Massalongia in the Southern Hemisphere, M. patagonica, though the populations in Australia and New Zealand differ somewhat molecularly, but more data is necessary to decide their taxonomic status. M. patagonica has a wider distribution than indicated in the original paper, also southwards and westwards. Previous records of several species in the Southern Hemisphere proved incorrect, most of them belonging in other genera.
The type species M. carnosa is restricted to the Northern Hemisphere, where it is widespread and variable, but without distinct molecular groupings requiring taxonomic recognition. There is also a local endemic, M. microphyllizans in California.
We are indebted to the directors and curators of the cited herbaria, to Louise Lindblom, Univ. Bergen for technical assistance and Mari Karlstad, Tromsø University Museum for photographs. Our sincerest thanks to all of you. Corporación Nacional Forestal (CONAF) in Chile kindly granted permission to collect there and the Olaf Grolle Olsen Fund generously gave financial support.