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Mots-clés : Un spécimen de Lycoperdacées récolté dans l'Extrême Orient Russe, dans la même zone géographique que le type perdu de Calvatiella lioui C. H. Chow correspond à la description originale, y compris la planche lectotype, et est désigné comme épitype. Ses caractères morphologiques et l'identité de la séquence des ITS confirment la synonyie avec Calvatia utriformis proposée par Kreisel et Calonge. De petites différences morphologiques justifient de conserver le nom au rang , Calvatia et Bovistella justifient le transfert de Lycoperdon utriforme (Calvatia u., Handkea u.) dans le genre Bovistella.



Keywords : A specimen of Lycoperdaceae collected in the Russian Far-East, in the same geographical area as the lost type of Calvatiella lioui C. H. Chow fits the original description, including the lectotype plate, and is designated as epitype. Its morphological characters and the identity of ITS sequences to those of Calvatiautriformis confirms the synonymy of the two names as already proposed by Kreisel and Calonge. Small morphological differences justify retentio, Calvatia and Bovistella justify the transfer of Lycoperdon utriforme (Calvatia u., Handkea u.) to the genus Bovistella.


2The genus Calvatiella was described by C. H. Chow in 1936 (p.91) and included two species, both from China. Those were described as new: Calvatiella sinensis C. H. Chow (p. 92) and C. lioui C. H. Chow (p. 93). According to the author, the genus "... may be defined in short as having the peridium of Calvatia but the capillitium of Bovista and Bovistella " (p. 91). Unfortunately, if the descriptions and illustrations are good, some important features like the presence of a pseudodiaphragm are not mentioned and the type material of both species disappeared during the Second World War, as reported by Kreisel and Calonge (1993). Those authors nonetheless considered the descriptions sufficient enough for placing C. sinensis in synonymy of Bovistella radicata (Dur. et Mont.) Pat. and C. lioui in that of Handkea utriformis (Bull. : Pers.) Kreisel (= Calvatia utriformis (Bull. : Pers.) Jaap). They considered that Calvatiella sinensis is the type of Calvatiella, which thus became a synonym of Bovistella. It is not clear if they intended to lectotypify Calvatiella or were aware of a previous lectotypification, which we have not localized, but if this lectotypification does not exist, their statement "...the type species Calvatiella sinensis Chow..." can be accepted as a lectotypification.

3During the study of specimens received from the herbarium (VLA) of the Institute of Biology and Soil Science, Far East Branch of the Russian Academy of Science one of us (Y. R.) noted a specimen that could have been referred to the genus Bovistella, but did not match any of its accepted species. It was close, however, to Calvatiella lioui through its macroscopic aspect and bovistoid capillitium with slit-like pores and hence, as noted by Kreisel and Calonge to Calvatia utriformis. The original material of Calvatiella lioui having been lost, it was interesting to study this collection from the same part of Eastern Asia in detail.


5Light microscope photography and molecular work have been implemented with the equipment of the Centre for cellular and molecular technology of studying plants and fungi at the Komarov Botanical Institute RAS (St Petersburg). Scanning electron micrographs (SEM) were taken with the Carl Zeiss EVO-40 XPV of the South Science centre RAS. Microscopic measurements were made using the program Scandium 5.0.

6DNA was extracted from the gleba following the manufacturer protocol of AxyPrepTM Multisource Genomic DNA Miniprep Kit (Axygen Biosciences (Calif., USA).

7PCR amplification of the ITS1-5.8S-ITS2 region was performed using the fungal specific primers ITS1F and ITS4B (Gardes and Bruns, 1993). The PCR products were purified with the GeneJet PCR Purification kit of Thermo Scientific.

8Sequencing was performed with the ABI model 3130 Genetic Analyzer of Applied Biosystems and the BigDyeTM Terminator Cycle Sequencing Ready reaction Kit, using the same primers as for amplification.

9Data were processed with Sequencing Analysis 5.3.1 (Applied Biosystems) and treated with MEGA 6 (Tamura et al. 2013).


11Collection's details: Russian Federation, Primorsky krai, near the village of Fadeevka, 44°04'N, 131°24'E, comm. A. E. Kozhevnikov (VLA 20697).

12Macroscopic characters (FIG. 1). Fruitbody turbinate, 11 cm high and 12 cm in diam., with soil agglomerated at the base. The specimen is mature, with the upper part destroyed. Exoperidium light brownish-grey, with thin spines up to 3 mm long, connivent in clusters. Endoperidium olive-brown, cracking and disappearing in the upper part. Gleba powdery, rich brown, separated from the subgleba by a pseudodiaphragm. Subgleba prominent, cellular, brown.

13Microscopic characters. Spores globose to subglobose, brown, almost smooth under the light microscope (FIG. 2) but verruculoseunder the scanning electron microscope (FIG. 4 and 5), uniguttulate, 3.7-4.3 m, usually with hyaline straight or curved pedicels up to 4.5 m. Capillitium (FIG. 2, 4 and 5) up to 13.0 m in diam., subelastic, thin-walled, widened at the places of the bipartite ramifications, septate, light-brown to brown, with slit-like and occasionally roundish pores. Exoperidium with subspherical spherocysts (FIG. 3), moderately thick-walled up to 40 µm in diameter.

14Sequencing of the ITS 1-5.8S-ITS 2 region gives a sequence identical to those of Calvatia utriformis GenBank EU833659 and DQ112607 and thus belongs to a clade that also includes Bovistella radicata as previously reported by Bates, Roberson and Desjardin (2004) and Larsson and Jeppson (2008). It should be noted that the sequence AJ237624 entered in GenBank under the name Bovistella radicata is also identical. We suspect this is a misidentification and that it is also Calvatia utriformis. DQ112608 is probably the sequence of a true Bovistella radicata and differs in four positions from that of Calvatia utriformis (see FIG. 2 in Larsson and Jeppson, 2008). It unfortunately does not cover the whole ITS 1.


16The study of a recent collection from the same geographic area that fits the original description of Calvatiella lioui refines our knowledge of that taxon and confirms the opinion of Kreisel and Calonge (1993) that it is a synonym of Calvatia utriformis. A slight difference in the microscopical characters, that is a less fragile capillitium and spores frequently provided with a small pedicel, justifies, in our opinion, to give a varietal status to the taxon. It should be noted that those characters are those that point toward classical Bovistella rather than Calvatia s. l. It was already noted by Moyersoen and Demoulin (1996, pp.39-40) that what was probably an immature Calvatia utriformis had been described by Reid (1969, p. 342) as a new species of Bovistella, B. alpina. It was then noted that the great fragility of the ripe capillitium of Calvatia utriformis must have led to its bovistoid character being overlooked and thus the fact it might be more related to Bovistella radicata than to other Lycoperdaceae.

17Through the help of Dr Begoña Aguirre-Hudson, we couldobtain from the Kew herbarium K(M) a piece of the type of Bovistella alpina. DNA extraction unfortunately proved unsuccessful. Intensive collections of puff-balls in Corsica, before and after the publication by Moyersoen and Demoulin however does not leave us doubts that the immature collection made by Reid is referable to Calvatia utriformis.

18The loss of Calvatiella lioui's type led Coetzee and Van Wyk (2012, p. 34) to designate plate III of the originalpublication as lectotype. The usefulness of this action is not apparent to us, since the name is based on the single specimen pictured there. Nonetheless the action seems legalistically correct and we must accept it. In the absence of the original specimen it thus seems useful to designate as epitype the collection on which we have based our interpretation.

19Epitypification of Calvatiella lioui C. H. Chow, Bull. Fan Mem. Inst. Biol., Bot. VII (2): 93, 1936. We designate as epitype the following collection: Russian federation, Primorsky krai, near the village of Fadeevka, 44°04'N, 131°24'E, comm. A. E. Kozhevnikov (VLA 20697).

20Registration identifier (Index Fungorum): 554055.

21This study also provided the opportunity to give more attention to the taxonomic position of Calvatia utriformis. In the phylogeny chapter of his thesis devoted to the genus Lycoperdon, one of us (V. D., 1971) considered the genus Calvatia highly heterogeneous, being derived at least three times from Lycoperdon through enlargement to the whole upper peridium of the fragility of the pore area of Lycoperdon (p. 266 and fig. 25). This phylogenetic reconstruction was largely inspired from Hennigian principles, analysing characters as primitive or derived (in 1973, V. D. must have been one of the first mycologist to cite Hennig, 1966). If the ideas of Hennig where found valuable for elaboratingphylogenetic trees, his concept of a classification being a strict transcription of a phylogenetic tree was not accepted. This was the same positionas that elaborated in details by Mayr, one of the greatest biologists of the twentieth century (1981).

22We maintain this philosophy, which most importantly acknowledges the need to have so called paraphyletic taxa, as advocated by the lamented Dick Brummitt and the numerous signatories of the manifesto published in Taxon in 2005 (Nordal and Stedje, 2005). A paraphyletic Lycoperdon (see FIG. 2 in Larsson and Jeppson, 2008, for a general account of the phylogeny suggested by the ribosomal locus) is important to describe the evolution of the Lycoperdaceae and a useful link to all the literature since the end of the nineteenth century which used morphologically well defined genera. This does not mean that when enough evidence is available, clearly polyphyletic genera like Calvatia could not be dismembered. This must however be done carefully and the use of a single character such as the slit-like pores in the capillitium, used to define the genus Handkea Kreisel (1989), leads to a smaller but still artificial genus, as can be ascertained from the morphology and supported by sequencing since Bates, Roberson and Desjardin (2004) and Larsson and Jeppson (2008). With those principles in mind we consider Bovistella radicata and Calvatia utriformis so closely related both from the standpoint of morphology and ribosomal locus sequence that they should belong to the same genus, which would then be Bovistella, a genus distinct enough from Lycoperdon s. str. to be worth recognising. We thus introduce the following new combination.

23New combination: Bovistella utriformis (Bull. : Pers.) Demoulin et Rebriev,

24Basionym: Lycoperdon utriforme Bull., Herbier France 10 (109-120): pl. 450, fig. I, 1790 : Pers., Syn. Meth. Fung.: 143, 1801.

25Registration identifier (Index Fungorum): 554053.

26Since we consider Calvatiella lioui is adequately treated as a variety of the former we also introduce the

27New combination (stat. nov.): Bovistella utriformis (Bull. : Pers.) var. lioui (C. H. Chow) Demoulin et Rebriev

28Basionym: Calvatiella lioui C. H. Chow, Bull. Fan Mem. Inst. Biol., Bot. VII (2): 93, 1936.

29Registration identifier (Index Fungorum): 554054.


31We thank Dr E. M. Bulakh for the opportunity to study specimens from the VLA herbarium and Dr Begoña Aguirre-Hudson (K) for the opportunity to study a part of the type of Bovistella alpina. We wish to express our gratitude to Drs E. F. and V. F. Malysheva for their invaluable help with the molecular study, as well as L. Cornet for information treatment. We also thank Dr K. V. Dvadnenko for his help with SEM.


33BATES, S. T., ROBERSON, R. W. & DESJARDIN, D. E., 2009. - Arizona gasteroid fungi I: Lycoperdaceae (Agaricales, Basidiomycota). Fungal Diversity 37: 153-207.

34CHOW, C. H., 1936. - Notes on the genus Calvatiella. Bull. Fan Mem. Inst. Biol., Bot.VII (2): 91-94.

35COETZEE, J. C. & VAN WYK, A. E., 2012. - Nomenclatural and taxonomic notes on Calvatia (Lycoperdaceae) and associated genera. Mycotaxon121: 29-36.

36DEMOULIN, V., 1971. - Le genre Lycoperdon en Europe et en Amérique du Nord. Thesis, University of Liège (Belgium): 284pp.

37DEMOULIN, V., 1973. - Phytogeography of the Fungal Genus Lycoperdon in Relation to the Opening of the Atlantic. Nature 242 (5393): 123-125.

38HENNIG, W., 1966. - Phylogenetic systematics. Urbana, University of Illinois Press: 263 pp.

39KREISEL, H., 1989. - Studies in the Calvatia complex (Basidiomycetes). Nova Hedwigia48 (3-4): 281-296.

40KREISEL, H. & CALONGE, F. D., 1993. - Calvatiella Chow, a synonym for Bovistella Morgan. Mycotaxon XLVIII: 13-25.

41LARSSON, E. & JEPPSON, M., 2008. - Phylogenetic relationships among species and genera of Lycoperdaceae based on ITS and LSU sequence data from north European taxa. Mycol. Res.112 (1): 4-22.

42MAYR, E., 1981. - Biological Classification: Toward a Synthesis of Opposing Methodologies. Science214 (4520): 510-516.

43MOYERSOEN, B. & DEMOULIN, V., 1996. - Les Gastéromycètes de Corse: taxonomie, écologie, chorologie. Lejeunia152: 128 pp.

44NORDAL, I. & STEDJE, B., 2005. - Paraphyletic taxa should be accepted. Taxon54 (1): 5-8

45REID, D. A., 1969 ("1968").  - Spring Fungi in Corsica. Rev. Mycol.XXXIII (5): 341-368.

46TAMURA, K. et al., 2013. MEGA6: Molecular Evolutionary Genetics Analysis Version 6.0. Mol. Biol. Evol.30 (12): 2725-2729.


48All the figures are from the epitype of Calvatiella lioui (VLA 20697).


49FIG. 1. – General view of the fruitbody.


50FIG.2. – Capillitium and spores as seen in light microscopy.


51FIG. 3. – Spherocysts from the exoperidium as seen in light microscopy.


52FIG. 4  – Capillitium and spores as seen under the SEM.


53FIG. 5  – Capillitium and spores as seen under the SEM.


Pour citer cet article

V. DEMOULIN & Y. REBRIEV, «ON CALVATIELLA, BOVISTELLA, AND THE TAXONOMIC POSITION OF CALVATIA UTRIFORMIS (LYCOPERDON UTRIFORME, HANDKEA UTRIFORMIS)», Lejeunia, Revue de Botanique [En ligne], N° 197 (décembre 2017), URL : http://popups.ulg.ac.be/0457-4184/index.php?id=1260.

A propos de : V. DEMOULIN

Université de Liège, Institut de Botanique, B.22, Chemin de la Vallée 4, 4000 LIEGE, Belgium (V.Demoulin@uliege.be).

A propos de : Y. REBRIEV

Southern Scientific Center, Russian Academy of Sciences, 41 Chehova str., 344006 ROSTOV-on-DON, RUSSIA.