©Verlag Ferdinand Berger & Söhne Ges.m.b.H., Horn, Austria, download unter www.biologiezentrum.at

Cryptovalsaria gen. nov. and its two new species from eastern Asia and south central North America

Larissa N. Vasilyeva1 & Steven L. Stephenson2

1 Institute of Biology & Soil Science, Far East Branch of the Russian Academy of Sciences, Vladivostok 690022, Russia 2 Department of Biological Sciences, University of Arkansas, Fayetteville, AR 72701, USA

Vasilyeva L. N. & Stephenson S. L. (2007). Cryptovalsia gen. nov. and its two new species from eastern Asia and south central North America. ± Sydowia 59 (1): 154±160. Cryptovalsaria is described as a new genus containing two new species C. americana and C. rossica both restricted to the living bark of alders (Alnus spp.) and displaying a vicarious pattern of distribution, with one species known from eastern Asia and the other from south central North America. Keywords: Ascomycetes, diatrypaceous fungi, , biogeography, vicarious distribution

The first collection of an unknown with the superficial features of a member of the genus Cryptosphaeria and brown, 1- septate ascospores (as is the case in Valsaria) was made from the living bark of Alnus hirsuta (Spach) Turcz. ex Rupr. in eastern Rus- sia (Big Khekhtsir Mountains, Khabarovsk Territory) in 2000. The fungus remained undescribed since its discovery. In 2006 a fungus having a similar appearance was collected from the living bark of Alnus serrulata (Ait.) Willd. in the south central United States (Ouachita Mountains, Arkansas). Examination of the two collections revealed some differences that allow us to consider the two entities as closely related but vicarious species of a new genus. When first observed in the field, the fructification of the fungus occurring on the bark of Alnus hirsuta resembled that of Crypto- sphaeria venusta Lar. N. Vasilyeva that was described from the same reserve (Vasilyeva 1986, Fig. 1), where it was found on Betula spp. Especially similar were the prominent (but even larger) cross-like divided tops of perithecial necks (`ostioles') at the bark surface (cf. also Vasilyeva 1998, Fig. 34). Cryptosphaeria venusta was later col- lected in many localities of the Russian Far East (Primorsky Terri-

* Corresponding author; e-mail: [email protected]

154 ©Verlag Ferdinand Berger & Söhne Ges.m.b.H., Horn, Austria, download unter www.biologiezentrum.at

tory, Amur Region) as well in Japan (near Ashio), where it was first recorded in 1999. The newly discovered fungus had large (36 ± 40 6 16 ± 20 mmon average) and brown, uniseptate ascospores (Fig. 1) instead of the aseptate, allantoid ascospores that are characteristic of Crypto- sphaeria Ces. et De Not. Moreover, its large young asci (240 ± 280 6 25 ± 27 mm) did not possess any evidence of the apical apparatus that is typical for many diatrypaceous fungi and often displays a positive reaction when exposed to iodine. Instead, the asci were very thickly bitunicate and even suggestive of some truly ascolocular fungi. However, they did not display the `fissitunicate' type of dehiscence but rather the `pseudofissitunicate' type also observed in Diatrypella (Ces. et De Not.) Nitschke (cf. Eriksson 1981, Fig. 4, A, D).

Fig. 1. One-septate ascospores of Cryptovalsaria rossica, characteristic of members of the genus (bar = 40 mm).

It should be noted that the `bitunicate' nature of the asci would not preclude the placement of the fungus within the , since long ago Nitschke (1867) described the asci of Diatrypella as having ªmembrana praesertim apicem versus crassiuscula textiº (p. 69) and wrote that ªDie Schlauchmembran ist . . . bei allen Arten der Gattung ziemlich dick und deutlich doppelt contourirt, an der Spitze am dickstenº (p. 71±72). It was also said that in the diatry- paceous fungi ªasci are, in common and inaccurate terms, `bituni-

155 ©Verlag Ferdinand Berger & Söhne Ges.m.b.H., Horn, Austria, download unter www.biologiezentrum.at

cate' rather than `unitunicate' and this fact should be taken as fur- ther evidence for the ordinal separationº (Romero & Minter 1988, p. 467) of members of the Diatrypales. We accept this order (Vasi- lyeva 1998), although it is more commonly placed within the Xylar- iales. The spores of the new, superficially cryptosphaeroid, genus on Alnus spp. are most similar in shape to those found in Valsaria Ces. et De Not., which also has been said to have `bitunicate' asci (Ju et al. 1996). The latter genus differs in stromatal type and is assigned to the tribe Quaternarieae within the family Diatrypaceae (Vasilyeva 1998), whereas the features of the new genus indicate that it is more appropriately placed in the tribe Cryptosphaerieae.

Taxonomy Cryptovalsaria Lar. N. Vassiljeva & S. L. Stephenson, gen. nov.

Stromata cortici innata, maculiformia, peridermio elevata; ostiolis (perithe- ciis collis apicis) ad corticis superficiem separatis, prominentis, nigris, conicis, cruciatim divisibus. Asci paraphysati, cylindracei, octospori. Paraphyses longae, septatae, fasciculi formatae, persistentes. Ascosporae uniseriatae, late ellipsoideae, 1-septatae, constrictae, brunneae. Habitu Cryptosphaeriae similis est, sed ascosporis majoribus, medio septatis differt. Typus: Cryptovalsaria rossica sp. nov.

S t ro m a t a in bark, visible as grayish spots where the host periderm is slightly elevated and covered by separate `ostioles' (api- ces of perithecial necks); `o s t i o l e s' prominent, black, conical, cru- ciformly divided. A s c i paraphysate, cylindrical, octosporous. P a r a p h y s e s long, septate, persistent in fascicles. A s c o s p o r e s uniseriate, ellipsoid, 1-septate, constricted, brown. This genus is superficially similar to Cryptosphaeria but differs in its large, 1-septate ascospores. Type species: Cryptovalsaria rossica sp. nov.

Cryptovalsaria rossica Lar. N. Vassiljeva & S. L. Stephenson, sp. nov. (Fig. 1±2)

Stromata cortici innata, maculiformia, peridermio elevata; ostioli (peritheciis colli apicali) ad corticis superficiem separati, prominenti, nigri, conici, ad 1.5 mm lati et alti, cruciatim divisibus; perithecii 700 ± 800 mm diam. Asci paraphysati, cylindracei, octospori, 240 ± 320 6 25±35 mm. Paraphyses ca. 300 ± 350 mm longae, septatae, fasciculi formatae, persistentes. Ascosporae uniseriatae, late ellipsoideae, medio septatae, constrictae, brunneae, (30) 36 ± 40 (42) 6 16.5 ± 20 (24) mm. Holotypus. ± Ad corticem vivum Alni hirsutae Turcz. ex Rupr., 19 Jun 2000 (VLA).

156 ©Verlag Ferdinand Berger & Söhne Ges.m.b.H., Horn, Austria, download unter www.biologiezentrum.at

S t ro m a t a in bark, visible as grayish spots where the host periderm is slightly elevated and covered by separate `ostioles' (api- ces of perithecial necks); `o s t i o l e s' prominent, black, conical, up to 1.5 mm wide and high, cruciately divided. P e r i t h e c i a 700 ± 800 mm diam. A s c i paraphysate, cylindrical, octosporous, 240 ± 320 6 25 ± 35 mm. Paraphyses about 300 ± 350 mm long, septate, persistent in fascicles. A s c o s p o re s uniseriate, ellipsoid, 1-septate, constricted, brown, (30) 36 ± 40 (42) 6 16.5 ± 20 (24) mm.

E t y m o l o g y. ± refers to the country of origin of the type species.

Holotype. ± RUSSIA, Khabarovsk Territory, Big Khekhtsir Nature Reserve, on living bark of Alnus hirsuta (Spach) Turcz. ex Rupr., Lar. N. Vasilyeva, 19 Jun 2000, Institute of Biology & Soil Science, Far East Branch of the Russian Academy of Sciences, Vladivostok (VLA).

Cryptovalsaria americana Lar. N. Vassiljeva & S. L. Stephenson, sp. nov. (Fig. 3)

Stromata cortici innata, maculiformia, peridermio elevata; ostioli (peritheciis colli apici) ad corticis superficiem separati, prominenti, nigri, conici, ad 0.5±0.7 mm lati et alti, cruciatim divisibus; perithecii 400±500 mm diam. Asci paraphysati, cylindracei, octospori, 200±250 6 24±28 mm. Paraphyses ca. 240±260 mm longae, septatae, fasciculi formatae, persistentes. Ascosporae uniseriatae, late ellipsoideae, medio septatae, constrictae, brunneae, 33±38 (40) 6 13.5±16.5 (18) mm. Holotypus. ± Ad corticem vivum Alni serrulatae (Ait.) Willd., 26 Jun 2006 (VLA).

S t ro m a t a in bark, visible as grayish spots where the host periderm is slightly elevated and covered by separate `ostioles' (api- ces of perithecial necks); `o s t i o l e s' black, conical, up to 0.5±0.7 mm wide and high, cruciately divided. P e r i t h e c i a 400±500 mm. A s c i paraphysate, cylindrical, octosporous, 200±250 6 24±28 mm. P a r a - p h y s e s about 240±260 mm long, septate, persistent in fascicles. A s c o s p o r e s uniseriate, ellipsoid, 1-septate, constricted, light brown, 33±38 (40) 6 13.5±16.5 (18) mm.

E t y m o l o g y: ± refers to American continent, where it was first collected.

Holotype. ± USA, Arkansas, Ouachita Mountains, on living bark of Alnus serrulata (Ait.) Willd., Lar. N. Vasilyeva, 26 Jun 2006 (VLA).

Discussion The sizes of asci and ascospores overlap in the two new species of Cryptovalsaria, although C. americana has smaller ascospores on

157 ©Verlag Ferdinand Berger & Söhne Ges.m.b.H., Horn, Austria, download unter www.biologiezentrum.at

Figs. 2±3. Species of Cryptovalsaria. 2. Cruciately divided tips of the perithecia of C. rossica extending from the bark of Alnus hirsuta. 3. Cruciately divided tips of the perithecia of C. americana extending from the bark of Alnus serrulata. (bar = 1 mm).

average. The difference in their appearance is more distinctive, since the `ostioles' of C. rossica are larger and coarser than is the case for C. americana. The size of the `ostioles' is an important character for delimiting many of the diatrypaceous species that strongly resemble Cryptovalsaria. For example, Rappaz (1987) used the degree of pro- minence of the `ostioles' and their size in his keys to species of Eutypa, Eutypella and Diatrype. The pattern of distribution observed in the two species of Cryp- tovalsaria reminds one of other pairs of very similar ascomycetous fungi with the same type of disjunct biogeographical distribution. For example, Biscogniauxia atropunctata (Schwein. : Fr.) Pouzar (eastern North America) and B. maritima Lar. N. Vassiljeva (Russian Far East, Japan, South Korea) occur both on Quercus spp. but have different areas. Pyrenomyxa morganii M. Stadler, Laessùe & Lar. N. Vassiljeva, described from eastern Russia (Khabarovsk and Pri- morsky Territories), is replaced by P. picea (Ellis) M. Stadler, Laessùe & Lar. N. Vassiljeva in eastern North America (Stadler et al. 2005). The latter species was known to have a distribution centered largely around the region of the Great Lakes (Ontario, Connecticut, Iowa, New York and Ohio), but it has recently been recorded from the Great Smoky Mountains National Park (Tennessee). Two ascomycetous fungi parasitize the fruits of mulberry trees (Morus spp.) either in the southeastern United States or eastern Asia (Japan, South Korea, China and southeastern Russia). These two species, Ciboria carunculoides (Siegler & Jenkins) Whetzel and C. shiraiana (Henn.) Whetzel (Whetzel & Wolf 1945), produce a mum- mification of mulberry fruits, and the external characteristics of their apothecia are strikingly similar. However, the two species differ in ascospore size and some other minor morphological differences and are restricted to different geographical regions. The two species

158 ©Verlag Ferdinand Berger & Söhne Ges.m.b.H., Horn, Austria, download unter www.biologiezentrum.at

of Cryptovalsaria described herein also parasitize host plants of the same genus in two different geographical regions and have similar ascospores but display external differences in their morphology. The biogeographical relationships that exist between the fungi of temperate eastern Asia and eastern and central portions of North America have been studied only in certain groups of Basidiomycota (Wu & Mueller 1997). Similar data on the have yet to be compiled. Although it has been noted that the same species of mac- rofungi can exhibit a disjunct distribution by occurring in both eastern Asia and eastern North America, vicarious patterns dis- played by pairs of closely related species are rarely discussed. In the Ascomycota, the same species may occur in both regions. For example, this is the case for pyrenomycetes such as Graphos- troma platystoma (Schwein.) Piroz. Other pyrenomycetous fungi, on the other hand, seem to display a very curious vicarious distribution pattern with species in closely related genera occurring on the same host plants but distinct geographic regions. For instance, new spe- cies of Diaporthella was recently found to parasitize the stem bases of Corylus spp. in eastern Asia (northeastern China, southeastern Russia), whereas the same ecological niche (bases of dying stems) on Corylus spp. in Europe and North America is taken by Sillia ferru- ginea (Pers. : Fr.) P. Karst., which has strikingly similar stromata.

Acknowledgements We are grateful to Dr. Mac Hardy, Director of the Ouachita Mountains Biological Station, for granting permission to collect on the station property. Thanks are extended to A. W. Rollins for help- ing produce the figures used in this paper.

References

Eriksson E. O. (1981) The families of bitunicate ascomycetes. Opera Botanica 60: 1±220. Ju Y.-M., Rogers J. D., Huhndorf S. M. (1996). Valsaria and notes on Endoxylina, Pseudothyridaria, and Roussoella. Mycotaxon 58: 419±481. Nitschke T. (1867) Pyrenomycetes Germanici. Breslau, Germany. Rappaz F. (1987) Taxonomie et nomenclature des Diatrypacees aÁ asques octospores (1). Mycologia Helvetica 2 : 285±648. Romero A. I., Minter D. W. (1988). Fluorescence microscopy: an aid to the elucida- tion of ascomycete structures. Transactions of the British Mycological Society 90: 457±470. Stadler M., Laessùe T., Vasilyeva L. (2005) The genus Pyrenomyxa and its affinities to other cleistocarpous Hypoxyloideae as inferred from morphological and chemical traits. Mycologia 97: 1129±1139. Vasilyeva L. N. 1986. Two new species of the family Diatrypaceae. Nova Hedwigia 43: 373±376.

159 ©Verlag Ferdinand Berger & Söhne Ges.m.b.H., Horn, Austria, download unter www.biologiezentrum.at

Vasilyeva L. N. 1998. Pyrenomycetes and Loculoascomycetes. In: Lower plants, fungi, and bryophytes of the Russian Far East, Vol. IV (ed. Azbukina Z. M.), Nauka, Saint-Petersburg: 1±419 (in Russian). Whetzel H. H., Wolf F. A. (1945). The cup fungus, Ciboria carunculoides, patho- genic on mulberry fruits. Mycologia 37: 477±491. Wu Q.-X., Mueller G. M. (1997). Biogeographic relationships between the macro- fungi of temperate eastern Asia and eastern North America. Canadian Journal of Botany 75: 2108±2116.

(Manuscript accepted 22 Apr 2007; Corresponding Editor: M. Kirchmair)

160