1. Puccinia deutziae (Dietel) Fraiture & Vanderweyen, comb. nov.

(Figs 1C, E, F; 2A, B; 3 A-C, E, F, K)

Puccinia kusanoi Dietel, in Engler’s Botanische Jahrbücher 27 (4): 568, 576, table 7 figs 14-15 (1899). — Puccinia kusanoi var. azuma Kusano, Bulletin of the College of Agriculture, Tokyo Imperial University 8 (1): 44 (1908). — Dicaeoma kusanoi (Dietel) Syd., Annales mycologici 20 (3/4): 118 (1922).

Anamorphs:

Aecidium deutziae Dietel, Hedwigia 37: 212 (1898) (basionym).

Uredo arundinariae P. Syd., Hedwigia 37 (Beibl. 6): (208) (1898) [non Puccinia arundinariae Schwein. (1822)].

DISTRIBUTION. — Puccinia deutziae, comb. nov. (sub P. kusanoi) is mostly known from Japan (Hiratsuka 1958; Hiratsuka et al. 1992; Ito 1909; Kusano 1908; Morimoto 1973). It has also been mentioned from China (Tai 1979; Zhuang 2001), Taiwan (Hiratsuka & Chen 1991; Hiratsuka et al. 1992; Shen et al. 2016 aecial stage; Shen et al. 2017; Zhuang 2001), Indonesia (Boedijn 1959), India, Russian Federation (far east, Azbukina 1984), Cuba (Arnold 1986), United Kingdom (Reid 1978; Henderson & Bennell 1979; Ing 1983; Henderson 2000, 2004) and Germany (Kruse et al. 2018, sub P. phyllostachydis). Apart from Belgium (our observations) and Germany (Bochum, in Kruse et al. 2018, sub P. phyllostachydis; J. Kruse confirmed us in e-litt. that the specimen has been misidentified), United Kingdom seems to be the only country in Europe in which the species had been observed until now (Termorshuizen & Swertz 2011; Klenke & Scholler 2015). These observations have been made during the period 1967-2000 in four different places in SE England and Cornwall: – Wakehurst Place, Ardingly, East Sussex (TQ33), 17.V.1967 and 26.XI.1967 (Reid 1978);

– St. Catherine’s Point, Fowey, East Cornwall (SX15), 24.IV.1983 (Ing 1983);

– Oxshott Heath, Oxschott, Surrey (TQ16), XI.1994 (Kirk & Spooner, unpubl.);

– Braywick Nature Centre, Berkshire (SU87), 02.IV.2000 (Storey, unpubl.).

The species is new for the Belgian mycoflora and has been observed in two places:

– Brussels (Ixelles), Parc Tenbosch, 13.V.2018, 05.VI.2018 and 22.VI.2018 (our specimens);

– Meise, Domain of Bouchout (BR), outdoor bamboo collection, 20.VI.2018 and 13.VII.2018 (our specimens).

MATERIAL EXAMINED. — Belgium, Brussels (Ixelles), Parc Tenbosch, 13. V.2018. On the underside of the leaves of Sasa ramosa. Specimens A. Fraiture 3738 (BR) and A. Vanderweyen F 1090. – Ibid., 05. VI.2018. On Sasa ramosa. Specimens A. Fraiture 3741 (BR) and A. Vanderweyen F 1092 (KR-M-0006375). – Ibid., 22. VI.2018. On Sasa ramosa. Specimen A. Fraiture 3748 (BR). – Belgium, Meise, Domain of Bouchout (BR), outdoor bamboo collection, 20. VI.2018. On the underside of the leaves of Sasa ramosa. Specimens A. Fraiture 3747 (BR) and A. Vanderweyen F 1097. – Ibid., 13.VII.2018. On Sasa ramosa. Specimen A. Fraiture 3750 (BR). – Ibid., 05.II.2019. On Sasa ramosa. Specimen A. Fraiture 3759 (BR).

DESCRIPTION

Aecia

Not seen (unsuccessfully searched on the Deutzia present in the Parc Tenbosch).

Uredinia

Hypophyllous, erumpent, 0.2-1.0 mm diam., cinnamon, each of them producing on the upper surface of the leaf a small square to rectangular yellowish spot, 0.2-1.0 × 0.2-0.5 mm, extending between two little veins.

Urediniospores

(25-)26-30.1-34(-35) × (20-)22-23.7-26 µm, Q = 1.15-1.26- 1.38, subglobose, obovoid or ellipsoid, with a pedicel up to 67 µm long rarely remaining attached to the spore, with a brownish wall (1.0-)2.0-2.5 µm thick appearing two layered, provided with acute spines 1.0-1.5 µm long and with four approximately equatorial germ-pores.

Paraphyses

Not seen.

Telia

Hypophyllous, erumpent, appearing in winter, dark cinnamon to blackish, not discolouring leaf tissues.

Teliospores

(50-)57-65.8-77(-89) × (14-)15-18.4-20(-22) µm, Q = 2.86- 3.51-5.17, fusoid, 2-celled, with a smooth to very finely punctuated wall which is 1.0-2.5 µm thick in the sides and 5-11.5 µm thick in the conical top of the spore, inserted on an up to 190 µm long pedicel which is (1-)2(-3) µm thick walled and very light brownish. These spores are mixed with a lower proportion of less elongated spores (dimorphism), 37-40.0-44 × 19-23.2-27 µm, Q = 1.37-1.74-2.26, with a broadly rounded apex and a punctuated wall. Very rare mesospores have been found.

Basidiospores

12-14 × 8.5-9.0 µm, ellipsoid to ovoid, with a hyaline, smooth and thin wall.

Host plant

Sasa ramosa (Makino) Makino & Shibata (Sasaella ramosa (Makino) Makino, × Sasinaria ramosa (Makino) Demoly).

Culms not caespitose, about 1.0- 1.5 m high, with cylindrical internodes and single branch-complement on the nodes. Leaf-blades 9-20 × 1.3-3.0 cm, pubescent on the underside and very sparsely on the upper side, with (4-)5-6 pairs of secondary veins, leaf-sheaths glabrous except for the margins.

Hyperparasitic fungi and mycophagous insect

During the study of our specimens we observed the following organisms, parasitizing Puccinia deutziae, comb. nov., or feeding on it. We already observed them (Fraiture & Vanderweyen 2007) on another rust fungus, Frommeëlla mexicana Fraiture & Vanderweyen (2007), and it seems they are frequent on Uredinales.

Sphaerellopsis filum (Biv.) Sutton (Ascomycota, Pleosporales).

Pycnidia of S. filum are frequent in the sores. They produce long whitish threads (cirrhi, Fig. 1E) entirely composed of conidia. Conidia fusiform, 12-18 × (3.5-)4.0(-5.0) µm, hyaline, with 0-1 septum and a thin and smooth wall (Fig. 1G).

Lecanicillium muscarium (Petch) Zare &W. Gams (Ascomycota, Hypocreales).

Whitish mould covering some sori and sometimes extending on the leaf surface. Phialides hyaline, smooth, very narrowly conical, straight, 20-32 × 1.5-2.5 µm, verticillate, 2-5 in whorls or sometimes solitary, inserted on hyaline, smooth, (1.5-)2 µm diam. hyphae. Conidia (2-)3.5-7.5 × 1-2(-2.5) µm, produced in globose heads, hyaline, with a thin and smooth wall, subglobose to ellipsoidal-diamond shaped to subcylindrical, with rounded ends, straight, non-septate, often with three guttules.

Mycodiplosis sp. (Diptera, Cecidomyiidae).

Several larvae feeding on Puccinia uredinia.

DISCUSSION AND NOTES

Nomenclature

For many years, the Code has prohibited the use of names of anamorphs as basionyms for the composition of correct names of pleomorphic species. However, in recent years this requirement has been removed and the current version of the Code (Turland et al. 2018) states that “all legitimate fungal names are treated equally for the purposes of establishing priority, regardless of the life-history stage of the type ” (Art. F.8.1). We followed this rule here, publishing Puccinia deutziae, comb. nov., to replace P. kusanoi as the correct name of the species. It seems obvious, however, that the application of this rule will result in the replacement of many names in current use. In addition, new names created will often seem strange. For example, in the current case, the Puccinia stage (teleomorph) of Puccinia deutziae, comb. nov., never grows on Deutzia. A solution to this problem would be that plant pathologists use Art. F.2.1 and propose a list of names for protection.

Descriptions

Descriptions of Puccinia deutziae, comb. nov. (sub P. kusanoi) are given by Cummins (1971: 269), Henderson & Bennell (1979), Hiratsuka (1958), Hiratsuka et al. (1992), Kusano (1908, also descr. of the var. azuma), Reid (1978) and Sydow & Sydow (1904).

Aecial stage

Asuyama (1936) realized inoculation experiments with the teliospores of P. deutziae, comb. nov., and showed that the aecial form is growing a.o. on Deutzia scabra var. crenata Makino and must be identified with Aecidium deutziae Diet. Recently, Shen et al. (2016) described the same aecial stage, collected on Deutzia pulchra S.Vidal in Taiwan.

Teliospore variability

Ito (1909) mentions the occasional existence of transitional forms with P. longicornis: some teliospores of P. deutziae, comb. nov., have an apex up to 18 µm thick while, on the other hand, some teliospores of P. longicornis have an apex which is only 8 µm thick. Similarly, Reid (1984) observed that, in P. longicornis, teliospores can be “extraordinarily variable” and that “The fact that in some mixed sori all the teliospores lacked a rostrate apex, while in others all the teliospores showed this feature inevitably raises the possibility of the host being infected by both P. longicornis and P. kusanoi or some other rust.” Also, Kusano (1908) describes the variability he observed in the size and shape of teliospores according to the host plant.

Some variability also exists with regard to the ornamentation of the teliospore wall. Most authors (a.o. Sydow & Sydow 1904; Hiratsuka 1958; Reid 1978) describe it as smooth but Cummins (1971) says “minutely punctate-verrucose (especially the robust spores) or smooth”. In our specimens, teliospore wall was smooth to finely punctate-verrucose.

Ito (1909) observed the presence of transitional forms between f. azuma and the typical form of P. kusanoi. He also notes that, with the exception of the shape of the thickened apex, the general form of the spore of f. azuma is closer to that of P. longicornis than to that of the typical form of P. kusanoi.

Basidiospores

It seems it is the first time that the basidiospores of this species are described and illustrated (Dr M. Scholler, in e-litt.).

Presence of paraphyses

All authors consider P. deutziae, comb. nov., as devoid of paraphyses, exceptReid (1978), who describes and illustrates clavate or subcapitate paraphyses with heads up to 12 µm wide, subhyaline with thin but distinct walls and often 1-septate near the base. We observed clusters of cylindrical cells in our material, but we think they are constituted by the pedicels of the urediniospores. We never saw clavate or subcapitate paraphyses.

Host plants

A large number of bamboo species have been reported as hosts of Puccinia deutziae, comb. nov. (sub P. kusanoi) in the world. Farr & Rossman (2018) cite 71 bamboo species belonging to the following genera: Arundinaria, Bambusa, Nipponobambusa, Phyllostachys, Pleioblastus, Pseudosasa, Sasa, Sasaella, Semiarundinaria, Sinobambusa and Yushania, as well as ten Deutzia species (hosts of the aecial stage).

In Europe, the only host cited so far (United Kingdom) was Semiarundinaria fastuosa Makino. All the Belgian collections described above have been made on Sasa ramosa.

Hyperparasitic fungi and mycophagous insect

Sphaerellopsis filum (Biv.) B. Sutton.

Sphaerellopsis filum is the anamorphic state of Eudarluca caricis (Fr.) O.E. Erikss., 1966 (Keener 1951). The teleomorph is rarely observed. Descriptions of the species are given by Keener (1934), Eriksson (1966, 1967), Scheuer (1988), Nag Raj (1993), Yuan et al. (1998), Płachecka (2005) and Trakunyingcharoen et al. (2014). It is hyperparasitic, leaving on many Uredinales (369 species in the list published by Kranz & Brandenburger 1981; none of our three Puccinia species being included in this list), even if it seems that a certain host-specificity does exist (Keener 1934; Nischwitz et al. 2005). The parasite is already mentioned by P. Sydow, in the description of Uredo arundinariae (“Sori saepe a Darluca Filo occupantur”). It has been recently shown that S. filum was a species complex (Liesebach & Zaspel 2004; Nischwitz et al. 2005; Trakunyingcharoen et al. 2014). After the descriptions (mostly conidia dimensions) given by these last authors, our material belongs to S. filum s. str.

Lecanicillium muscarium (Petch) Zare & W. Gams.

A few dozen species of conidial fungi grow on Uredinales (Hawksworth 1981). The genus Lecanicillium has been created to accommodate a majority of the species formerly classified in Verticillium sect. Prostrata (Gams & Zare 2001; Zare & Gams 2001, 2008). It contains almost thirty species mostly growing as parasites on scale insects, mites and fungi, a.o. Uredinales. Within that genus, our material can be placed in the group of L. lecanii (Zimm.) Zare & W.Gams, L. longisporum (Petch) Zare & W.Gams and L. muscarium, because of the ellipsoidal to cylindrical and straight conidia, produced in globose heads on mostly verticillate phialides. Finally, the dimensions of phialides and conidia in our material allow to determine it as L. muscarium. Descriptions of the species are given by Zare & Gams (2001, 2003). Leinhos & Buchenauer (1992) observed a pronounced chitinolytic activity in vitro of several hyperparasitic fungi (incl. Verticillium lecanii) growing on rust fungi. That study helps to understand why many of these fungi are also attacking scale insects.

Mycodiplosis sp.

Many insect species feed on fungi, but those eating Uredinales are just a few. A family of Diptera, Cecidomyiidae, includes many mycophagous species. Within this family, the genus Mycodiplosis contains several species feeding on rust fungi, a.o. on Puccinia species (Coutin 2005; Henk et al. 2011; Nelsen 2013; Nelsen & Aime 2013). One of them, Mycodiplosis pucciniae is present in Europe (Fauna Europaea) but we are not able to confirm that our collections correspond to this species. According to our observations, larvae mainly eat urediniospores.