New Laboulbeniales parasitic on endogean ground beetles
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1 Mycologia, 100(4), 2008, pp DOI: /07-081R # 2008 by The Mycological Society of America, Lawrence, KS New Laboulbeniales parasitic on endogean ground beetles Walter Rossi 1 Dipartimento di Scienze Ambientali, Università dell Aquila, Coppito (L Aquila), Italia Sergi Santamaria Unitat de Botànica, Departament de Biologia Animal, de Biologia Vegetal i d Ecologia, Facultat de Biociències, Universitat Autònoma de Barcelona, Bellaterra (Barcelona), España Abstract: Three new species of Laboulbenia occurring on endogean Carabidae are described. These are L. lucifuga, parasitic on Winklerites spp. from Greece, L. magrinii, parasitic on Typloreicheia spp. from Italy, Reicheia spp. from Italy and Corsica and L. vailatii, parasitic on Coecoparvus spp. from Greece. New characters of L. coiffatii and L. endogea are pointed out, and the genus Scalenomyces is synonymized with Laboulbenia. Key words: Ascomycota, Carabidae, Laboulbenia, Scalenomyces, taxonomy INTRODUCTION Until recently the endogean ground beetles (Coleoptera, Carabidae) were little known and were collected only occasionally and then mostly by chance. In recent years however a few entomologists addressed special interest towards these elusive insects. As a consequence the number of described species increased considerably in a short time. The knowledge of the Laboulbeniales parasitic on endogean Carabidae obviously is tied strictly to knowledge of their beetle hosts, and recent interest in the latter has aided a greater understanding of these peculiar parasitic fungi. Here we describe three new species and clarify the concepts of two other species described previously on scanty material. MATERIALS AND METHODS The hosts bearing the new species were received dry and affixed to pinned labels. The parasitic fungi were carefully removed by means of an entomological pin (No. 3) and mounted in Amann s solution following the techniques described in Benjamin (1971). The holotypes are deposited in the Botanical Museum of Florence (FI); the other slides are temporarily preserved in the collection of the senior Accepted for publication 3 April Corresponding author. vrossi@univaq.it author and will be deposited in FI. Observations and photographs were made with a Leica DMR microscope equipped with DIC optics and a Jenoptik ProgRes 10 Plus digital camera. TAXONOMY Laboulbenia lucifuga W. Rossi & Santam. sp. nov. FIGS. 1 5 Basalis et suprabasalis cellulae receptaculi, distalis pars appendicis et apex perithecii hyalini; ceterus fungus ferrugineus. Basalis cellula longior quam latior, ad summum paulo dilatata. Suprabasalis cellula longitudine basalem adaequans, ad summum multo dilatata. Cellula III parva, circiter tam longa quam lata, a cellula II parvo septo divisa. Cellula IV paulo minor quam III. Cellula V parva et elongata, perithecio adhaerens. Appendix simplex, e 6 superpositis et gradatim longioribus cellulis constans, quarum secunda et interdum tertia fusciores. Antheridia desunt. Cellula VI applanata ac obliqua. Perithecium ovoideum, 3/5 longitudinis solutum, obtuso ac inaequali apice, posteriore labio maiore. Ad huiusmodi specimina semper singula specimina adsunt e 5 superpositis cellulis constantia. Longitudo a pede usque ad apicem perithecii mm; perithecium mm; maxima longitudo appendicis 120 mm. Basal and suprabasal cells of the receptacle, distal portion of the appendage, and apex of the perithecium hyaline or almost so; the rest of the fungus is reddish brown. Basal cell (I) longer than broad, slightly broadened distally, similar in length or slightly longer than suprabasal cell (II), which is strongly broadened distally. Cell III relatively small, about as long or slightly longer than broad, separated from cell II by a short septum. Cell IV slightly smaller than cell III. Cell V small and elongate, leaning against the perithecium (FIG. 4, arrow). Insertion cell not present. Primary appendage unbranched, forming an angle of about 45 degrees with the axis of the thallus, consisting of up to six superposed and progressively longer cells, of which the second and sometimes the third are distinctly darker. Stalk cell of perithecium (VI) flattened and oblique. Perithecium ovoid, its upper three-fifths free, hardly tapered to the blunt, asymmetrical apex, the posterior lip being larger and more prominent. Antheridia not seen; a rudimentary paired thallus (48 51 mm) consisting of five superposed cells is present, but there is no evidence that the distal, darker cell is a phialide (FIG. 2, arrow). Length from foot to tip of perithecium mm; perithecium (with basal cells) mm; longest appendage 120 mm. 636
2 ROSSI AND SANTAMARIA: NEW ENDOGEAN LABOULBENIALES 637 FIGS Laboulbenia lucifuga and L. coiffaitii L. lucifuga (FIGS. 1, 5 WR2478 Holotype, FIGS. 2 4 WR2479). 1, 3. Mature thalli. 2. Detail of rudimentary paired thallus with darker distal cell (arrow). 4. Detail of perithecium and upper receptacle showing cell V (arrow), a diagnostic characteristic. 5. Detail of perithecium and upper receptacle of a young thallus with labeled cells L. coiffaitii [WR2914]. 6. Mature specimen paired with a rudimentary thallus (arrow). 7. Detail of perithecium and upper receptacle showing a small triangular cell on the inner side of the basal cell of the appendage (arrow). Bars 1, 3, mm; 2, 4, 5, mm. Etymology. From Latin lucifugus, shrinking from light. Specimens examined. GREECE: nom. Imathia, Oros Piéria, northern slope, between Elatohori and Rizomata, 1 km from Seloma, alt. 890 m, on pronotum of Winklerites imathiae Giachino et Vailati, 15 Jun 1991, P. Giachino and D. Vailati, WR2478 (HOLOTYPE, FI), WR2479. Nom. Imathia, Oros Vérmio, road Séli-Véria, alt m, on the elytra of W. casalei Giachino et Vailati, 4 Jun 1993, P. Giachino and D. Vailati, WR2480. Seven mature and two young specimens have been examined. Remarks. Laboulbenia lucifuga is allied to L. coiffatii
3 638 MYCOLOGIA Balazuc (FIGS. 6 7), parasitic on other genera of endogean Carabidae, that is Binaghites, Hypotyphlus, Rhegmatobius and Scotodipnus (all in the Anillina). The latter parasite differs from the new one in having a dark insertion cell, a wider cell V and a more inflated perithecium with a more tapered tip (Balazuc 1971); moreover on the inner side of the basal cell of the appendage of L. coiffatii a small triangular cell is always present (FIG. 7, arrow). This small cell, which was overlooked by Balazuc, might represent the remains of the basal cell of the inner appendage. Laboulbenia magrinii W. Rossi & Santam. sp. nov FIGS Fungus parvus et clavatus, gradatim fuscior a hyalina receptaculi basali cellula ad fuscum perithecii apicem. Basalis cellula receptaculi (I) circiter duplo longior quam sua maxima latitudo. Suprabasalis cellula longitudine basalem adaequans sed ea latior, irregulatim pentagona, septo II III multo breviore quam II VI. Cellula III parva, latior quam longior. Cellula IV cellulae III similis, extrorsum producta. Cellula V elongata, septo IV V verticali aut obliquo, cellulam III attingens. Psallium atrum, parvum, superne fimbriatum. Appendix simplex, e pluribus superpositis cellulis constans, quarum duae inferiores hyalinae, ceterae majores ac fusciores. Cellula VI latior quam longior, Perithecium ovatum, 3/4 longitudinis solutum, simo extrinseco apice. Longitudo a pede usque ad apicem perithecii mm; perithecium mm; maxima longitudo appendicis 102 mm; ascosporae mm. Thallus small and clavate; color gradually darkening from basal cell of the receptacle, which is hyaline or almost so, to the dark brown perithecial tip. Basal cell of the receptacle (I) about twice as long as its maximum width, slightly tapering to the foot. Suprabasal cell (II) about as long as the basal but wider, irregularly pentagonal, with the septum separating this cell from cell III much shorter than the one separating the same from cell VI. Cell III small, slightly wider than long. Cell IV about as long as cell III, its outer margin distinctly convex. Cell V elongate, with the septum IV V vertical or oblique but always reaching cell III (FIG. 8). Insertion cell dark brown, rather small, irregularly fringed on the upper side. Primary appendage unbranched, consisting of a series of five superposed cells, the lower two of which are small and hyaline, the others much larger and brownish; in most examined specimens the primary appendage is broken and replaced by a linear series of slender, elongate and almost hyaline cells. Cell VI wider than long. Perithecium ovoid, its upper threequarters free, with a blunt apex strongly turned outward. Antheridia not seen; a rudimentary paired thallus (41 50 mm) consisting of five superposed cells is present, but there is no evidence that the distal, tapered cell is a phialide (FIG. 10, arrow). Length from foot to tip of perithecium mm; perithecium (with basal cells) mm; longest appendage 102 mm; length of ascospores mm. Etymology. Name after the Italian entomologist Paolo Magrini (Florence). Specimens examined. ITALY: Isola di Zannone (Latina), Macchia alta, on the elytra of Typhloreicheia usslaubi (Saulcy), 26 Feb 1966, R. Argano,WR3014. Montorsaio (Grosseto), on the elytra of Typhloreicheia damone (Holdhaus), 25 Mar 1991, P. Magrini, WR2919; idem, 20 Mar 1994, WR2920. Selva del Lamone (Viterbo), on the elytra of T. damone, Apr 1985, G. Castellini, WR3054, WR3055. Sambiase (Catanzaro), on the elytra of Reicheia italica Holdhaus, 12 Aug 1973, R. Pace, WR2943 (HOLOTYPE, FI). FRANCE: Corsica, Rogliano, on the elytra of R. palustris Saulcy, 4 Jun 1992, P. Magrini, WR3019. Twenty mature and two young specimens have been examined. Remarks. Laboulbenia magrinii differs from all the other species of Laboulbenia parasitic on endogean and cavernicolous Carabidae from Europe for the septum between cells IV and V, which is vertical or nearly so. On the contrary it is similar in the general habit with Scalenomyces endogaeus (F. Picard) I.I. Tav. (Laboulbenia endogaea F. Picard), described from Sardinia on Typhloreicheia sardoa (Baudi) (Picard 1917) (FIGS ). The latter parasite has an undivided cell III; that is the derivatives cells IV and V are not present (FIG. 15, arrow), and lacks the insertion cell (see DISCUSSION). From the list of the hosts of Laboulbenia magrinii reported above it is evident that both the records of Scalenomyces endogaeus on Reicheia palustris (Balazuc 1971) and Typhloreicheia usslaubi (Rossi and Cesari 1976) were wrong. Laboulbenia vailatii W. Rossi & Santam. sp. nov. FIGS Basalis et suprabasalis cellulae receptaculi, maxima pars appendicis et apex perithecii hyalini; ceterus fungus ferrugineus; cellulae III, IV, V, VI et basales cellulae perithecii verrucosae. Basalis et suprabasalis cellulae receptaculi elongatae, tenuem stipitem ad summum dilatatum efficientes. Cellula III multo longior quam latior, fere triangula, ad basem attenuata. Cellula IV extrorsum producta, brevior quam cellula III. Cellula V relative magna, rotundata, sursum producta. Appendix simplex, e 7 superpositis cellulis constans, quarum prima applanata, ceterae gradatim longiores, tertia vero fuscior. Antheridia desunt. Cellula VI applanata, obliqua aut horizontalis. Perithecium ovoideum, e quarta parte solutum, apice inaequali et extrorsum verso. Ad huiusmodi specimina semper singula specimina adsunt e 5 superpositis cellulis constantia. Longitudo a pede usque ad apicem perithecii mm; perithecium mm; maxima longitudo appendicis 164 mm; ascosporae circiter 38 mm. Basal and suprabasal cells of the receptacle, most of
4 ROSSI AND SANTAMARIA: NEW ENDOGEAN LABOULBENIALES 639 FIGS Laboulbenia magrinii, L. endogaea and L. vailatii L. magrinii (FIGS. 8, 9 WR2919; FIGS. 10, 11 WR3055]. 9, 11. Mature thalli. 8. Detail of upper receptacle and base of appendage with cells III, IV and V labeled. 10. Detail of rudimentary paired thallus with tapered distal cell (arrow) L. endogaea (FIGS. 12, 14, 15 WR2915; FIG. 13 WR3024]. 12. Detail of an immature thallus showing the trichogyne (arrow). 13, 14. Mature thalli. 15. Detail of upper receptacle and base of appendage, showing an undivided cell III (arrow) L. vailatii (FIGS. 16, 18, 19 WR2433 Holotype; FIG. 17 WR2431). 16. Detail of rudimentary paired thallus with tapered distal cell (arrow). 17. Mature thallus. 18. Detail of perithecium and upper receptacle at near phocus to show the warty surface of cells III, IV, V, VI and basal cells of perithecium. 19. Same as FIG. 18 phocused to show cells III, IV and V, which are labeled. Bars 9, 11, 13, mm; 8, 10, 12, 15, 16, 18, mm. the appendage, and apex of the perithecium hyaline; the rest of the fungus is reddish brown; cells III, IV, V, VI and basal cells of perithecium with a warty surface (FIG. 18). Basal (I) and suprabasal (II) cells of the receptacle elongate, the former slightly curved and slightly longer, the latter considerably broadened distally, the two forming a slender stalk of about the same diameter throughout, above which the distal portion of the receptacle is abruptly distinguished (FIG. 17). Cell III much longer than broad and irregularly triangular in mature specimens, with a narrow base. Cell IV distinctly bulging outward, shorter
5 640 MYCOLOGIA than cell III, from which is divided by a slightly oblique septum (FIG. 19). Cell V large, rounded, somewhat prominent upward, thus carrying the base of the appendage obliquely outward (FIG. 17). Primary appendage unbranched, consisting of up to seven superposed cells, the basal of which is flattened in mature specimens, while the others are progressively longer and the third always tinged with brown. Stalk cell of perithecium (VI) strongly flattened, oblique to horizontal. Perithecium ovoid, free for one-quarter of its length or less on the inner side, with an asymmetrically and not strongly tapered tip turned slightly outward. Antheridia not seen; a rudimentary paired thallus (55 65 mm) consisting of five superposed cells is present, but there is no evidence that the distal, tapered cell is a phialide (FIG. 16). Length from foot to tip of perithecium mm; perithecium (with basal cells) mm; longest appendage164 mm; ascospores about 38 mm. Etymology. Named after the Italian entomologist Dante Vailati (Brescia), who collected and described the host-insects. Specimens examined. GREECE: nom. Arkadia, O. Ménalon, alt m, on the elytra and pronotum of Caecoparvus arcadicus (Müller), 26 May 1998, P. Giachino and D. Vailati, WR2431, WR2432, WR2433 (HOLOTYPE, FI). Nom. Fthiotioda, O. Iti Katavotra, alt m, on the pronotum of C. hercules Giachino et Vailati, 1 Jun 1998, P. Giachino and D. Vailati, WR2430. Nom. Fokida Athanasios Diakos, Ori Vardaussia, alt m, on left elytron of C. berrutii Giachino et Vailati, 15 Jun 2000, P. Giachino and D. Vailati, WR2481. Peloponnesus, Killini Oros, alt m, on prosternum and elytra of C. pavesii Giachino et Vailati, 5 Jun 2005, P. Giachino and D. Vailati, WR3069. Nine mature and four young specimens have been examined. Remarks. Laboulbenia vailatii is quite different from other species of Laboulbenia parasitic on endogean ground beetles for the slender and pale stalk formed by the basal and suprabasal cells of the receptacle, above which the thallus is abruptly enlarged (, 60 mm) and darkened. Another distinguishing feature is the large, flattened and hyaline lower cell of the appendage, which might be homologous to the insertion cell of other species, which is usually much smaller and darker (as in L. coiffatii, L. magrinii, etc.). DISCUSSION The three new species of Laboulbenia parasitic on endogean Carabidae described in the present paper share a few common features: simple outer appendage, lack of inner appendage and antheridia, normally developed thalli paired with rudimentary thalli consisting of a linear series of few cells. These same characters are found in other species of Laboulbenia parasitic on endogean or cavernicolous Carabidae: L. coiffatii, L. vignae W. Rossi (1978), and L. taurica W. Rossi (1982). The large genus Laboulbenia is mostly monoecious, but dioecism has been proved in a few species, which are characterised by fully developed thalli lacking antheridia paired with rudimentary thalli (Benjamin and Shanor 1950, Santamaria 1996). It is therefore likely that the three new species and the others mentioned above are also dioecious. Why dioecism is more favourable than monoecism in the endogean environment is an open question. Another interesting question is the similarity between Laboulbenia magrinii and Scalenomyces endogaeus. As stated before the two are similar in the general habit (FIGS. 11, 13), although the latter fungus lacks the insertion cell as well as cells IV and V. These characters also are found in a few species of Laboulbenia; species lacking a darkened insertion cell are not rare among those parasitizing Gyrinidae, and an undivided cell III is found in species parasitic on Chrysomelidae (Tavares 1985). Scalenomyces was erected as a new genus by Tavares (1985) and separated from Laboulbenia mainly because of the wall cells in the perithecium, which were said to be of the same height at each level in all four rows; the new genus inexplicably was placed in the Stigmatomycetinae, a group distantly related to Laboulbenia. Actually the cells of the outer wall of the perithecium are practically identical in Scalenomyces endogaeus and Laboulbenia magrinii. For these reasons we think that Scalenomyces is synonym of Laboulbenia and therefore L. endogaea maintains its original name. We observed Laboulbenia endogaea on these endogean Scaritinae, all from Sardinia (Italy): Typhloreicheia pellita Leo, Magrini et Fancello, near Burcei (Cagliari), alt m, 29 Mar 1999, P. Leo & L. Fancello, WR2915 & WR2916; T. valeriae Fancello, S. Nicolò Gerrei (Cagliari), 29 Mar 1986, L. Fancello, WR2942; T. eleonorae Leo, Magrini et Fancello, Samugheo (Oristano), 15 Nov 2002, L. Fancello, WR3021 & WR3022; T. jucunda jucunda (Holdhaus), Narcao (Cagliari), 5 Jan 1990, L. Fancello & P. Leo, WR3024; T. jucunda vescicularis Magrini, Leo et Fancello, Esterzili (Nuoro), 25 Jan 1989, P. Leo, WR3025; T. jucunda sclanoi Magrini, Leo et Fancello, Tertenia (Nuoro), 15 Mar 1990, L. Fancello & P. Leo, WR3026; T. consortii Magrini, Figaruja (Sassari), 16 Mar 2002, P. Magrini, WR2023; Dimorphoreicheia relicta Magrini, Mt. Gonare, Orani (Nuoro), 3 Dec 2004, L. Fancello, WR3020. ACKNOWLEDGMENTS We are grateful for the help of entomologists who kindly supplied us with infected insects and entomological
6 ROSSI AND SANTAMARIA: NEW ENDOGEAN LABOULBENIALES 641 information; they are Giorgio Castellini (Grosseto), Pier Mauro Giachino (Turin), Paolo Magrini (Florence), Roberto Pace, (Verona), Dante Vailati (Brescia) and Augusto Vigna Taglianti (Rome). This work was supported partially by the US National Science Foundation PEET program Monographic approaches to the Laboulbeniales subtribe Stigmatomycetinae and the genus Stigmatomyces (Fungi, Ascomycota) (Award DEB ) and by MEC and FEDER funds by means of the project No. CGL C02-02/BOS (Flora Micológica Ibérica VI) to SS. LITERATURE CITED Balazuc J Laboulbéniales inédites, parasites de Carabiques. Nouv Rev Entomol 1: Benjamin RK. Introduction and supplement to Roland Thaxter s contribution towards a monograph of the Laboulbeniaceae. Biblioth Mycol 30: Rossi W Sulle Laboulbeniali (Ascomycetes) parassite dei Trechini di Turchia (Coleoptera, Carabidae). Quad Speleol 3: Two new species of Laboulbenia (Ascomycetes, Laboulbeniales) from Asia. Kew Bull 37:69 71., Cesari Rossi MG Contributo alla conoscenza delle Laboulbeniali (Ascomycetes) parassite di Carabidi italiani (Insecta, Coleoptera). Giorn Bot Ital 110: Santamaria S Laboulbeniales I. Laboulbenia. Fl Mycol Iber 4: Tavares II Laboulbeniales (Fungi, Ascomycetes). Mycol Mem 9:1 627.
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