Laboulbenia Mont. & C. P. Robin

Genus Laboulbenia Mont. & C.P.Robin MB#2606 Histoire naturelle des végétaux parasites qui croissent sur l’homme et sur les animaux vivants. J.B.Baillière, Paris: 622 (Robin 1853). – Type species: L. rougetii Mont. & C.P.Robin Thaxteria Giard, Comptes-Rendus Hebdomadaires des Séances et Mémoires de la Société de Biologie et de ses filiales, Paris: 156 (Giard 1892) [MB#5406] Ceraiomyces Thaxt., Proceedings of the American Academy of Arts and Sciences 36: 410 (Thaxter 1901a) [MB#878] Eumisgomyces Speg., Anales del Museo Nacional de Historia Natural de Buenos Aires 23: 176 (Spegazzini 1912) [MB#1927] Laboulbeniella Speg., Anales del Museo Nacional de Historia Natural de Buenos Aires 23: 188 (Spegazzini 1912) [MB#2608] Schizolaboulbenia Middelh., Fungus 27 (1–4): 73 (Middelhoek 1957) [MB#4896] Scalenomyces I.I.Tav., Mycologia Memoirs 9: 313 (Tavares 1985) [MB#25698] Brief description Mostly monoecious. Receptacle typically five-celled. The two-celled pedicel (primary or lower receptacle) consists of superposed cells I and II. Cell II supports on one side the perithecial stalk cell (VI) and the perithecium with associated cells, and on the opposite side the secondary or upper receptacle with appendages. The secondary receptacle is typically three-celled, including cell III underlying ± parallel cells IV and V, separated from each other by a septum joining or not the insertion cell with cell III. The appendages (i.e., the primary appendage) are subtended by a flattened and usually darkened insertion cell. Appendages are typically arranged in two sets: the inner appendage including simple antheridia, and the outer appendage. The solitary perithecium, above the basal cells (m, n, n’ and VII), has an outer wall with 4 unequal cells for each vertical row, with an ostiole surrounded by two ± prominent lips and two preostiolar blackened spots. Remarks Of all the genera included in the Laboulbeniales, this is the richest in number of taxa, with more than 650 species, in addition to countless infraspecific taxa of highly variable value. We have gathered 653 species in our database catalogue. Song et al. (2019) mentioned 633 species where 40 have been described after 2010, Haelewaters et al. (2019b) reported 650 accepted species and many varieties, and according to the same authors, Index Fungorum (2019) includes 897 names of taxa. More than one hundred species are known in Europe (we count 109 species), 47 have been found in Denmark. The most recently described species are L. chionophila, L. halophila (Santamaria et al. 2020a), L. quarantenae (Haelewaters & De Kesel 2020), L. angkorensis, L. fusca, L. polyandra, L. scabra, and L. trilobata (Kong et al. 2020), and L. amblystomi (Haelewaters et al. 2021). Although species of Laboulbenia mostly occurs on ground beetles (Carabidae), some may also be found on other families like Staphylinidae, Gyrinidae, Chrysomelidae, Elateridae, and Corylophidae, even on other orders of Insecta like Diptera, Blattodea, Hemiptera, Hymenoptera, Orthoptera, and unrelated arthropods like mites (Acarina). A subdivision of the genus into subgenera would be desirable, although the difficulty of managing so many taxa, data and intraspecific variability makes it a titanic task. Some attempts were carried out by Spegazzini (1917), who described several unnatural sections, which were not widely followed by subsequent authors. Unfortunately, his contemporary Roland Thaxter passed away before his sixth monograph dealing with this genus could see the light. This fact led to many new species left out but also a probable reorganization of the genus. Many years after, Tavares (1985) distinguished 20 structural groups of species based on morphology but subgenera were not formally described. Some characteristics are key to distinguish and group species: (1) if the septum IV–V is connected with the septum III–IV, as in L. pedicellata, or not as in L. flagellata; (2) if the insertion cell is flattened and dark, clearly distinguished from surrounding cells, as in L. ophoni, or pale, colourless, not distinctly contrasting from the surrounding cells, as in L. fasciculata; (3) whether basal cells of the outer appendage show some septa distinctly darkened and/or constricted, as in L. clivinalis; (4) if the outer appendage is unbranched, as in L. notiophili, or ± ramified, as in L. elaphri; (5) if cell V is totally or partially free from the perithecium, as in L. pseudomasei, or connected along its whole length to the perithecium, as in L. vulgaris. Other important features, such as the cells III, IV and V totally or partially undivided, are not found in the Danish species of Laboulbenia. Key to the Danish species (partially following Majewski 1994 b, and Santamaria 1998) The included key for identification of Danish species in the genus Laboulbenia is broadly based on the mentioned key characteristics. Although it appears to be obvious, it should be noted that some features may be very variable, and because of this we should rely on collections with specimens in good condition and reasonably abundant. Otherwise, if we have to take into account all variations, many of them product of malformations by injury, the key would become useless and unwieldy. 1. Perithecium bearing some kind of apical outgrowths....................................................................... 2 – Perithecium without apical outgrowths............................................................................................ 4 2. Two apical outgrowths on the perithecium; the anterior short, arcuate, the posterior longer, straight but hooked on the top. On Gyrinus Geoffroy, 1762 and allied genera (Col. Gyrinidae).................................................................................................................................................. L. gyrinicola Speg. – Only one solitary outgrowth. On other hosts.................................................................................... 3 3. Outgrowth subapical, horn-like, darkened (may be very short!). Insertion cell not evident, reduced to a groove. Septum IV–V connected with septum III–IV. On the distal part of elytra of Bembidion subgenus Notaphus Dejean, 1821 (Col. Carabidae)............................................... L. cornuta Thaxt. – Outgrowth apical, horn-like, pale. Insertion cell flattened, darkened, and clearly distinguished from surrounding cells. Septum IV–V not connected with septum III–IV. Grows hidden near the pygidium in Dromius (Col. Carabidae).......................................................................... L. hyalopoda De Kesel 4. Insertion cell colourless, not darkened, or not distinctly contrasting with surrounding cells, or absent, sometimes reduced to a groove......................................................................................................... 5 – Insertion cell flattened, darkened, clearly distinguished from surrounding cells........................... 12 5. Receptacle four-celled, because cells III and IV are not separated. On Sphaerius acaroides (Col. Sphaeriusidae)..................................................................................................... L. sphaerii Santam. – Receptacle five-celled as usual. On other hosts............................................................................... 6 6. Cell V divided, proliferating into up to eight cells gradually decreasing in size, each giving rise to secondary appendages. On Chlaenius Bonelli, 1810 and allied genera (Col. Carabidae).... L. fasciculata Peyr. – Cell V not divided............................................................................................................................. 7 7. Septum IV–V not connected with septum III–IV. Cell V shorter than cell IV. Receptacle distinctly constricted between cells II and III/IV. On Bembidion Latreille, 1802 (Col. Carabidae)....................................................................................................... L. murmanica Huldén – Septum IV–V connected with septum III–IV. Cell V as long as cell IV.......................................... 8 8. Primary appendage compact, without distinction between outer and inner appendages. On Cafius Stephens, 1829 and allied genera (Col. Staphylinidae Staphylininae)......................... L. cafii Thaxt. – Primary appendage separated into the two characteristic sets, i.e., the inner and outer appendages, each with respective basal cells (sometimes young thalli need to be studied; overmature or old thalli may have deteriorated appendages where this feature is difficult to see)......................................... 9 9. Perithecium free, measuring more than the half of the total length of the thallus. Primary septum or insertion cell located below the lowermost perithecial outer wall cells (w 1). On legs, typically on tarsi of Bembidion (Col. Carabidae)............................................................................... L. curtipes Thaxt. – Perithecium not free, shorter. Primary septum above w 1 cells....................................................... 10 10. Cell IV longer than cell III. On Bembidion (Col. Carabidae)................................ L. luxurians Peyr. – Cell III longer than cell IV............................................................................................................... 11 11. Perithecial apex rounded, symmetric, with undistinguished lips. Preostiolar spots undefined but replaced with a subapical dark suffusion. On Cillenus lateralis (Col. Carabidae)................................................................................................................................................... L. lichtensteinii F.Picard – Perithecial apex acute, asymmetric, with distinct lips. Preostiolar spots absent. On Bledius (Col. Staphylinidae Oxytelinae)............................................................................... L. parriaudii Balazuc 12. Septum IV–V connected with septum III–IV................................................................................. 13 – Septum IV–V not connected with septum III–IV........................................................................... 22 13. Outer appendage unbranched, exceeding in length the perithecial apex........................................ 14 – Outer appendage branched or, if unusually simple, then short, not exceeding the perithecial apex, or hardly discernible from inner appendage....................................................................................... 15 14. Appendages bent towards perithecium. Dorsal margin of perithecium straight, ventral margin curved. Cell V very narrow. On the prothorax margin of Pterostichus subgenus Argutor Dejean, 1821 (Col. Carabidae)......................................................................................................... L. kajanensis Huldén – Outer appendage straight to flexuous, never bent towards perithecium. Outer and inner margins of perithecium curved. Cell V as broad as cell IV. On Olisthopus Dejean, 1828 (Col. Carabidae)............................................................................................................... L. olisthopi Speg. 15. Appendages with the 2–3 lower cells inflated and separated by thick and dark septa. Cell I showing a blackish lateral swelling above the foot. On Philonthus and allied genera (Col. Staphylinidae Staphylininae)....................................................................................................... L. philonthi Thaxt. – Otherwise........................................................................................................................................ 16 16. Some dorsal septa above the basal cell of outer appendage distinctly blackened and constricted.............................................................................................................................................................. 17 – Not such septa above the basal cell of outer appendage. Thalli very pale, yellowish brown, with the two preostiolar spots of the perithecium merged into a contrasting black ring. On Ophonus Dejean, 1821 and allied genera (Col. Carabidae)................................................................. L. ophoni Thaxt. 17. Insertion cell free, separated from perithecial wall. On Clivina Latreille, 1802 (Col. Carabidae)............................................................................................................. L. clivinalis Thaxt. – Insertion cell or cell V connected along its whole length to the perithecium................................. 18 18. Outer appendage consisting of 2–3 straight, long branches, arising from the suprabasal cell which bears an additional dark reddish-brown branch. On Paederus Fabricius, 1775 and relatives (Col. Staphylinidae Paederinae)...................................................................................... L. cristata Thaxt. – Different.......................................................................................................................................... 19 19. Perithecium showing 1–3 swellings or protuberances on its lower third or broadest part (septa between w 1 and w 2). On Col. Carabidae Tachyina like Tachys Dejean, 1821 and allied genera............................................................................................................................................................ L. egens Speg. – Perithecium without such protuberances........................................................................................ 20 20. Cell II with parallel margins, somewhat constricted towards the upper part. Thallus olive brown, with darker to almost hyaline areas. Outer appendage having the septa between the basal and suprabasal cells and between this and next outer cell thickened, black and constricted. On Bembidion and Dyschirius (Col. Carabidae).............................................................................. L. pedicellata Thaxt. – Cell II with divergent margins, not constricted upwards. Thallus almost uniform yellowish-amber. Outer appendage only with the septum between the basal cell and the posterior branch thickened, black and constricted. On other hosts............................................................................................. 21 21. Outer appendage basal cell bulging outwards, as long or longer than cell IV. Receptacle bent outwards. On Cafius (Col. Staphylinidae Staphylininae)................................ L. littoralis De Kesel & Haelew. – Outer appendage basal cell slightly inflated outwards, shorter than cell IV. Dorsal side of receptacle straight to slightly concave. On Pogonus Dejean, 1821 (Col. Carabidae).................................................................................................................................................. L. slackensis Cépède & F.Picard 22. Outer appendage unbranched (rarely branched from 3 rd cell or above if injured).......................... 23 – Outer appendage branched (usually from basal or suprabasal cells of appendage)....................... 41 23. Dioecious. A seven-celled male thallus is paired to a female thallus, attached by the blackened feet. The terminal cell functions as an antheridium. The three distal septa darkened and constricted. Typically on Acupalpus (Col. Carabidae)................................................................. L. inflata Thaxt. – Monoecious. If some reduced thalli paired to females are present, characteristics are different (see L. lecoareri).................................................................................................................................... 24 24. Cell V totally or partially free from perithecium, or insertion cell separated from perithecial wall........................................................................................................................................................... 25 – Cell V and insertion cell attached to perithecial wall..................................................................... 27 25. Inner appendage absent. On Trechoblemus micros (Col. Carabidae)............................................................................................................................................................... L. lecoareri (Balazuc) Huldén – Inner appendage present................................................................................................................. 26 26. Inner appendage consisting of a small basal cell supporting two unbranched or once ramified branches bearing pairs or clusters of antheridia; sometimes with elongated sterile branches. On Amara Bonelli, 1810 (Col. Carabidae).............................................................................. L. aubryi Balazuc – Inner appendage consisting of a small basal cell supporting two once ramified branches (rarely a 3 rd branch may be present), in total four branches (or six if 3 rd branch is present). Each branch gives rise to a simple three-celled appendage where the terminal cell is an antheridium bearing a long and asymmetric neck. On or near the pygidium of Syntomus (Col. Carabidae)........... L. pygidicola Santam. sp. nov. 27. Inner appendage with long branches supporting lateral paired or solitary brownish antheridia near the base. On Leistus Frölich, 1799 (Col. Carabidae)................... L. leisti J.Siemaszko & Siemaszko – Inner appendage with short branches not exceeding the perithecial apex...................................... 28 28. Thallus small, total length from foot to perithecial apex less than 100 µm. On Corylophus cassidoides (Col. Corylophidae)....................................................................................... L. corylophi Scheloske – Thallus longer, more than 100 µm from foot to perithecial apex (not considering growth forms found on tarsi or antennae of hosts).......................................................................................................... 29 29. Appendages bent towards perithecium. Dorsal margin of perithecium straight, ventral margin curved. Cell V very narrow. On the prothorax margin of Pterostichus subgenus Argutor (Col. Carabidae)......................................................................................................... L. kajanensis Huldén – Otherwise........................................................................................................................................ 30 30. Inner appendage unbranched, consisting of a basal cell, a suprabasal cell and a solitary terminal large antheridium. On Asaphidion Des Gozis, 1886 (Col. Carabidae)........ L. thaxteri Cépède & F.Picard – Inner appendage different, bearing more antheridia....................................................................... 31 31. Stalk cell of the perithecium (cell VI) broader than long, flattened (see also L. stilicicola and L. vulgaris)...................................................................................................................................... 32 – Stalk cell of the perithecium (cell VI) longer than broad, or isodiametric..................................... 34 32. Basal and suprabasal cells of the outer appendage (rarely also the 3 rd cell) elongated, hyaline, narrow, contrasting with darker and broader cells above. Inner appendage consisting of 2(–3) cells bearing 2–3 antheridia. On Acupalpus (Col. Carabidae)............................... L. inexpectata Santam. sp. nov. – Other characteristics....................................................................................................................... 33 33. Perithecium broad (more than 45 µm in width), half free, with the tip pointing towards the ventral margin. On Badister (Col. Carabidae).......................................... L. benjaminii Balazuc ex Santam. – Perithecium narrow (less than 45 µm in width), about ¾ or more free, with straight tip. On Col. Carabidae of the genera Notiophilus Duméril, 1806, Cymindis Latreille, 1806, Demetrias Bonelli, 1810, Dromius, Philorhizus Hope, 1838, Metadromius Bedel, 1907, etc....................................................................................................................................................... L. notiophili Cépède & Picard 34. Outer appendage with the basal cell forming a distinctive blunt outgrowth on its outer side. Cell II and upper part of cell I tuberculate. On Perigona nigriceps (Col. Carabidae).......................................................................................................................................................... L. manubriolata Thaxt. – Otherwise........................................................................................................................................ 35 35. Cell II with delicately undulate and punctate margins. Inner appendage consisting of two short branches above the basal cell, each bearing a solitary lateral antheridium. On Porotachys Netolitzky, 1914 (Col. Carabidae).............................................................................................. L. picardii Maire – With other characters...................................................................................................................... 36 36. Inner appendage embracing the perithecium; consisting of two branches directly arising from the basal cell; each branch with 5–6 superposed cells, each giving rise to unilaterally, simple two or three-celled branches terminated by long and narrow antheridia. Cell VII protruding below the per