The family Hysteriaceae Chevall. 1826
Hysteriales Lindau 1897
by Eric W. A. Boehm
Hysteriaceae Chevall. 1826, Hysteriales Lindau 1897: Fungi classified in the Hysteriaceae (Chevallier 1826) have been traditionally defined by a specialised ascocarp termed the hysterothecium (Clements 1909). Hysterothecia are dense, persistent carbonaceous structures, distinctly navicular in outline, and bear a pronounced longitudinal slit running the length of the long axis of the fruitbody. They can be immersed to erumpent to entirely superficial, solitary to gregarious, ellipsoid to greatly elongated, sometimes branched or triradiate. In vertical section, hysterothecia are globose to obovoid, typically with a thick three-layered peridium, composed of small pseudoparenchymatous cells, the outer layer heavily encrusted with pigment and often longitudinally striated on the surface, the middle layer lighter in pigmentation and the inner layer distinctly thin-walled, pallid and compressed (Barr 1987). The hamathecium is composed of persistent, narrow cellular pseudoparaphyses, often borne in a gel matrix, with tips darkened or branched at maturity above the asci. Bitunicate asci are borne in a basal layer and at maturity are typically clavate to cylindric, bearing 8 ascospores, overlapping biseriate, ranging from hyaline to dark brown, obovoid, clavate, ellipsoid or fusoid. Ascospores are highly diverse in septation and range from didymospores to phragmospores to dictyospores, at times surrounded by a gel coating, and often show bipolar asymmetry (Barr 1987).
Zogg (1962) accepted the following seven genera within the Hysteriaceae: Farlowiella Sacc., Gloniella Sacc., Gloniopsis De Not., Glonium Muhl., Hysterium Tode, Hysterocarina H. Zogg, and Hysterographium Corda. Both coelomycetous pycnidial states (e.g., Hysteropycnis, Aposphaeria) and dematiaceous hyphomycetous anamorphs (e.g., Acrogenospora, Coniosporium, Septonema, Sirodesmium, Sphaeronaema, and Sporidesmium) have been described (Goh et al. 1998; Lohman 1931, 1933 a & b, 1934). Hysteriaceous fungi are pan-global in distribution, having been reported from Japan (Amano 1983), China (Teng 1933), the Russian Far East (Vasilyeva 1999a, b, 2000), South Africa (Lee & Crous 2003; van der Linde 1992), Argentina (Messuti & Lorenzo 1997, 2003; Lorenzo & Messuti 1998), Costa Rica (Checa et al. 2007), North America (Lohman 1933, 1937) and Europe (Zogg 1962). Although primarily lignicolous or corticolous, recently a saxicolous/terricolous and apparently lichenized species has been described from Tasmania (Kantvilas & Coppins 1997). Early authors provided remarkably accurate figures of hysteriaceous fungi (Bolton 1789). Greville (1825) was the first to provide illustrations of asci and ascospores.
The traditional circumspection of the Hysteriaceae was based on character states related to the hysterothecium and spore morphology (e.g., septation and pigmentation), character states previously considered synapomorphic (Zogg 1962). However, recent molecular data underscore the potential for morphology to be difficult to interpret, and even unhelpful in phylogenetic inference and reconstruction for this group of fungi (Schoch et al. 2006; Boehm et al. 2009a, b; Mugambi & Huhndorf 2009). For the most part, molecular data support the premise of a large number of convergent evolutionary lineages within the family, sharing similar spore morphologies, but that are not closely related. This resulted in a polyphyletic core set of genera for the Hysteriaceae, and presented us with a complicated picture of past speciation events within the family (Boehm et al. 2009a, b). To achieve a natural phylogeny, that is, one based on the concordance of morphological and molecular data, required that we break-up what were once thought to be stable genera. Thus, two species of Hysterium were transferred to Oedohysterium gen. nov. (Od. insidens comb. nov. and Od. sinense comb. nov.), and two species of Gloniopsis to Hysterobrevium gen. nov. (Hb. smilacis comb. nov. and Hb. constrictum comb. nov.). While Hysterographium, with the type Hg. fraxini, was removed from the Hysteriaceae (Boehm et al. 2009a, b), some of its species remained within the family, transferred here to Oedohysterium (Od. pulchrum comb. nov.), Hysterobrevium (Hb. mori comb. nov.) and Gloniopsis (Gp. subrugosa comb. nov.). New species were described (e.g., Gp. arciformis sp. nov. and Gp. kenyensis sp. nov.) which would previously have been classified in Hysterographium, but are now accommodated in Gloniopsis. It is important to stress that molecular data necessitated that both Gloniopsis and Hysterobrevium include hyaline and pigmented dictyospores, and the genus Oedohysterium, both phragmospores and dictyospores. This, then, de-emphasised spore morphology as a synapomorphic character state. Likewise, the genus Glonium sensu Zogg (1962) was divided into Psiloglonium in the Hysteriaceae and Glonium in the Gloniaceae (Boehm et al. 2009a, b), and, more recently, Anteaglonium in the Pleosporales (Mugambi & Huhndorf 2009).
Data have also necessitated that we expand the concept of the Hysteriaceae to include thin-walled mytilinidioid forms previously in the Mytilinidiaceae (e.g., Ostreichnion), as well as patellarioid forms previously in the Patellariaceae (e.g., Rhytidhysteron). The inclusion of Ostreichnion within the Hysteriaceae was also entirely unexpected. Unlike most members of the family, the peridium in Ostreichnion is sclerenchymatoid and thin-walled, defining a fragile mytilinidioid ascoma, and with a hamathecium typified by trabeculate pseudoparaphyses (Barr 1975, 1990a). Including the genus Ostreichnion in the Hysteriaceae implies that, either morphological features within the genus need to be re-evaluated, or that the family Hysteriaceae must also encompass mytilinidioid forms. More difficult to understand perhaps is the inclusion of the genus Rhytidhysteron within the Hysteriaceae. Although included within the Patellariaceae (Kutorga & Hawksworth 1997), phylogenetic data presented here and elsewhere (Boehm et al. 2009a, b), clearly indicate that this genus lies quite distant from other members of the Patellariaceae (see below).
These taxonomic changes were entirely unexpected, as they were not premised on past assumptions of synapomorphy related to spore morphology (Zogg 1962), and necessitated a revision of the family. As such, the family Hysteriaceae bears little resemblance to the original concept (Zogg 1962). In the keys that follow, we have endeavoured to provide a morphological basis for the new phylogenies revealed by molecular data.
Some authors have included a number of additional genera within the Hysteriaceae. For instance, the genera Hysteropatella Rehm, Hysteroglonium Rehm ex Lindau, and Pseudoscypha J. Reid & Piroz. were included in the Hysteriaceae by Eriksson (2006). In addition, the genera Hemigrapha (Müll. Arg.) R. Sant. ex D. Hawksw., Graphyllium Clem., and Encephalographa A. Massal. were included in the family by Kirk et al. (2001). In Boehm et al. (2009a), two species belonging to Hysteropatella, namely Hp. clavispora (Peck) Seaver (CBS 247.34) and Hp. elliptica Fr. (CBS 935.97), did not cluster with any of the hysteriaceous taxa surveyed. Instead, they formed a distant clade within the Pleosporomycetidae, postulated to represent the emergence of the Patellariales. In Boehm et al. (2009b), these two species of Hysteropatellacontinued to be distant from the Hysteriaceae, and clustered with Patellaria atrata (Hedw.) Fr. (CBS 958.97). Therefore, we do not include the genus Hysteropatella within the Hysteriaceae. Reid & Pirozynski (1966) in describing Pseudoscypha abietis J. Reid & Piroz. on the needles of Abies balsamea did not mention the Hysteriaceae, and in fact stated that the fungus cannot be assigned to any presently known order. In their illustrations, no sterile tissue or excipulum is presented, and the bitunicate asci and pseudoparaphyses arise directly from an erumpent orange basal stromatic cushion. As such, we do not include Pseudoscypha as a member of the Hysteriaceae. As for the genus Hemigrapha, Diederich & Wedin (2000) make the argument for the inclusion of the genus in the Microthyriaceae, not the Hysteriaceae. The genus Graphyllium possesses applanate, clathrate ascospores borne in thin-walled membranous hysterothecia, at first subcuticular, later erumpent, often associated with aquatic poaceous hosts. The genus was included in the Hysteriaceae by Shoemaker & Babcock (1992) and Kirk et al. (2001), but was earlier classified in the Phaeosphaeriaceae (Barr 1987). A new species was recently described from Costa Rica (Checa et al. 2007). The unique ascospore and the lack of carbonisation or peridial wall thickness argue against the inclusion in the Hysteriaceae, but molecular data are lacking. The genus Encephalographa was originally placed in the Hysteriaceae by Renobales & Aguirre (1990) who thought it to be lichenicolous. Tretiach & Modenesi (1999) demonstrated it to be lichenised, and maintained its placement within the Hysteriaceae. The latter authors illustrate endolithic, saxicolous, dichotomously branched, laterally anastomosed, lirelliform pseudothecia with a longitudinal sulcus, and clavate bitunicate asci bearing pigmented didymospores, highly reminiscent of the saxicolous forms of Glonium circumserpens (Nyl.) Kantvilas & Coppins, in the Gloniaceae (Boehm et al. 2009a, b). We recently were able to obtain fresh material of Encephalographa elisae A. Massal. from Mauro Tretiach (Dipartimento di Biologia, Università di Trieste, Trieste, Italy), and, although cultures failed, we were able to isolate DNA directly from the ascomata (EB 0347 / BPI 879773). Sequence data presented here indicate that E. elisae does not reside within the Hysteriaceae, nor within the Gloniaceae. Instead, E. elisae lies outside of the Pleosporomycetidae and Dothideomycetidae (Boehm et al. 2009b).
To summarise, we accept the following genera in the Hysteriaceae: Actidiographium, Gloniella, Gloniopsis, Hysterium, Hysterobrevium, Hysterocarina, Oedohysterium, Ostreichnion, Psiloglonium, and Rhytidhysteron. Dichotomous keys are presented here for hysteriaceous fungi, with the caveat that phylogenetically unrelated taxa share the same key. Thus, despite their transference from the Hysteriaceae (Boehm et al. 2009a, b), the genera Hysterographium, Farlowiella, Glonium and Anteaglonium (Mugambi & Huhndorf 2009), are nevertheless included in the key. This is because they typically possess ascomata that have traditionally been referred to as hysterothecia.
Key to the genera and allied genera of the Hysteriaceae
- Ascomata apothecioid, opening widely when hydrated, fully exposing the hymenium, which may be red or black (i.e., patellarioid) → Rhytidhysteron
- Hysterothecia usually remaining closed, or only opening slightly through a longitudinal fissure or sulcus to reveal a lenticular, disk-like hymenium when hydrated and mature → 2
- Ascospores pedicellate amerospores, the upper cell pigmented and much larger than the lower, which remains un- or less-pigmented; anamorph Acrogenospora→ Farlowiella
Note: The genus Farlowiella has been removed from the Hysteriaceae and is currently listed as Pleosporomycetidae gen. incertae sedis (Boehm et al. 2009a, b).
- Ascospores not as above, didymospores, phragmospores or dictyospores, sometimes pigmented → 3
- Didymospores small, the two cells more or less equal in size → 4
- Ascospores not as above, phragmospores, dictyospores, +/- pigmentation, or very large didymospores (O. curtisii) → 7
- Ascospores hyaline → 5
- Ascospores pigmented → Actidiographium
- Didymospores less than 8 μm long → Anteaglonium
Note: The genus Anteaglonium lies within the Pleosporales (Mugambi & Huhndorf 2009), but is keyed out here with Psiloglonium. A separate page is not presented.
- Didymospores longer than 8 μm → 6
- Didymospores hyaline, borne in solitary or gregarious hysterothecia, rarely associated with a subiculum, not laterally anastomosed to form radiating stellate composites → Psiloglonium
Note: One species of Anteaglonium, A. latirostrum, will key out here, but belongs in the Pleosporales (Mugambi & Huhndorf 2009) and is also keyed out in the Psiloglonium key.
- Didymospores hyaline, borne in modified hysterothecia, usually associated with a subiculum, strongly laterally anastomosed along their length to form radiating stellate composites → Glonium
Note: The genus Glonium has been transferred from the Hysteriaceae to the Gloniaceae, currently listed as fam. incertae sedis within the Pleosporomycetidae (Boehm et al. 2009a, b).
- Ascospores transversely septate phragmospores, or if with dictyospores then also with red pigmentation → 8
- Ascospores transversely and longitudinally septate dictyospores, or very large didymospores (O. curtisii) → 10
- Ascospores hyaline phragmospores →Gloniella
- Ascospores pigmented phragmospores or in one case (Od. pulchrum) with pigmented dictyospores and red pigmentation in the hamathecium → 9
- Phragmospores 3-septate or rarely more, but without swollen supra-median cell(s) → Hysterium
- Phragmospores with swollen supra-median cell, usually more than 3-septate, in one case with pigmented dictyospores and red centrum pigmentation (Od. pulchrum) → Oedohysterium
- Dictyospores hyaline, +/- gelatinous sheath, or pigmented, but short, less than 25 μm in length → Hysterobrevium
- Dictyospores hyaline, +/- gelatinous sheath, or pigmented, but longer than 25 μm, or very large didymospores (O. curtisii) →11
- Dictyospores, if hyaline, then longer than 25 μm, or if pigmented, then measuring (22-)25-34(-45) x (6-)8-12(-17) μm, with 7-11 transverse and 1-2 vertical septa, and no red pigment associated with the hamathecium (Gp. subrugosa) → Gloniopsis
- Dictyospores pigmented, of different length, or if similar in length to Gp. subrugosa, then tropical with red pigment associated with the hamathecium, or very large didymospores (O. curtisii) → 12
- Dictyospores pigmented, borne in typical hysterothecia, that are erumpent or sessile on the substrate → Hysterographium
Note: The genus Hysterographium, with the type species Hg. fraxini, has been transferred out of the Hysteriaceae as Pleosporomycetidae gen. incertae sedis (Boehm et al. 2009a, b). Residual species classified as Hysterographium, for which sequence data are lacking, are provisionally retained within the genus. The removal of the genus from the family was predicated solely on molecular data, but was substantiated by two geographically disparate isolates collected and deposited by two reputable workers (see Boehm et al. 2009a, b). Thus, there is sound reason to propose this taxonomic change.
- Hysterothecia borne within the substrate, hardly erumpent, with cristate longitudinal apex instead of a sulcus; neotropical → Hysterocarina
- Ascomata thin-walled, globoid to conchate, mytilinidioid, without sunken longitudinal slit; pigmented dictyospores or very large didymospores → Ostreichnion
Note: The genus Ostreichnion, previously in the Mytilinidiaceae, was transferred to the Hysteriaceae (Boehm et al. 2009a).