J. Hattori Bot. Lab. No. 76: 21-34 (Oct. 1994) NEW CLASSIFICATION OF ANTHOCEROTAE JIRO HASEGAWA 1 ABSTRACT. The classification of the Anthocerotae is revised based on a cladistic analysis. In the analysis the phylogenetic relationships among ten anthocerote genera or subgenera are based on the available morphological, anatomical and chemical data, using the Hepaticae and the Musci as the outgroup. Six most parsimonious cladograms resulted. The strict consensus tree calculated from these six trees suggests that Notothylas is the sister group to all the remaining taxa, which again form two major branches: one contains five taxa including Anthoceros and Phaeoceros, and another has four taxa including Dendroceros and Megaceros. In the former branch, the clade uniting Anthoceros and Folioceros is strongly supported, but the relationships of Phaeoceros are poorly resolved. In the latter branch, three paraphyletic terminal clades are found. On the basis of the cladistic analysis pre­ sented here, the two family and two subfamily classification of the Anthocerotae is proposed. The taxonomic status of Folioceros, Leiosporoceros, Notoceros, Apoceros and Hattorioceros is discussed, and the genus Notoceros (Schust.) Haseg. stat. nov. and the genus Hattorioceros (Haseg.) Haseg., stat. nov. are also proposed. INTRODUCTION The Anthocerotae are a monophyletic small group with a rather small number of fam­ ilies, genera and species. Although special attention has been paid to the Anthocerotae from a phylogenetic point of view, little has been mentioned about the classification of higher categories of the Anthocerotae until recently when Schuster ( 1987), Hassel de Menendez ( 1988) and Hasegawa ( 1988) almost simultaneously proposed new classifica­ tions of the Anthocerotae (Table l ). As shown in Table I, the classifications of Schuster and Hasegawa are very similar in all essential points. They classified the Anthocerotae into three families or subfamilies (in­ cluding the autonomous family or subfamily, Notothyladaceae or Notothyladoideae), and regarded Folioceros and Leiosporoceros as subgena of Anthoceros (Aspiromitus sensu Schuster) and Phaeoceros (Anthoceros sensu Schuster), respectively. On the contrary, the classification of Hassel de Menendez is quite different from those of Schuster and Hasegawa. In her classification, five families (including the monotypic families, Foliocero­ taceae and Leiosporocerotaceae) were recognized, and Notothylas and Phaeoceros were classified in the same family. Schuster (I 992) reviewed these three classifications, and sug­ gested that the classification of Hassel de Menendez could not reconcile with that of the other two. Thus, at present two basically different classifications of the Anthocerotae exist. To improve this confusion, I attempted to re-evaluate characters on which these classi­ fications were based. Moreover, as the classification of Hassel de Menendez (I 988) was based on a cladistic analysis, I also attemped to examine the reality of these classifications in the light of the cladistic analysis. 1 Laboratory of Applied Botany, Faculty of Agriculture, Kyoto University, Kyoto 606, Japan. 22 J. Hattori Bot. Lab. No. 76 I 9 9 4 Table 1. Classification of the Anthocerotae. Hassel de Menendez ( 1988) Hasegawa (1988) Schuster ( 1992) Ord. Anthocerotales Ord. Anthocerotales Ord. Anthocerotales Fam. Anthocerotaceae Fam. Anthocerotaceae Fam. Anthocerotaceae Gen. Anthoceros Gen. Anthoceros Subfam. Anthocerotoideae Sphaerosporoceros Subgen. Anthoceros Gen. Aspiromitus Fam. Notothyladaceae Folioceros Subgen. Aspiromitus Subfam. Notothyladoideae Gen. Phaeoceros Folioceros Gen. Notothylas Subgen. Phaeoceros Gen. Anthoceros Subfam. Phaeocerotoideae Leiosporoceros Subgen. Anthoceros Gen. Phaeoceros Gen. Megaceros Leiosporoceros Ord. Foliocerotales Subgen.Megaceros Subfam. Dendrocerotoideae Fam. Foliocerotaceae Australoceros Gen. Megaceros Gen. Folioceros Fam. Dendrocerotaceae Subgen.Megaceros Ord. Leiosporocerotales Gen. Dendroceros Notoceros Fam. Leiosporocerotaceae Fam. Notothyladaceae Gen. Dendroceros Gen. Leiosporoceros Gen. Notothylas Subgen. Dendroceros Ord. Dendrocerotales Apoceros Fam. Dendrocerotaceae Subfam. Notothyladoideae Gen. Dendroceros Gen. Notothylas Megaceros A cladistic analysis of the Anthocerotae was, for the first time, given by Mishler and Churchill (1985). Although only five genera of the Anthocerotae were included in their analysis, it suggested some critical points involved in the classification of the Anthocero­ tae; they included problems relating to ( l) their origin and ancestry, (2) the naturalness of the family Anthocerotaceae (sensu lat.), (3) the relationships between Anthoceros and Phaeoceros, and (4) the relationships between Notothylas and the remaining anthocerote genera. Hassel de Menendez (1988) also presented a cladistic analysis of the Anthocerotae, but the cladogram given by her was quite different from that by Mishler and Churchill (1985). One of the most serious problems invloved in a cladistic analysis of the Anthocerotae is that the relationships of the Anthocerotae to other plant groups are so ambiguous that ap­ parent homoplasy occurs everywhere. Mishler and Churchill (1985), in their cladistic ap­ proach to the phylogeny of bryophytes, described the situation as follows; "The relation­ ships of the Anthocerotae are not so straightforward, which is curious since this group has fewer species and is less diverse than the other groups in the analysis. Almost all the appar­ ent homoplasy we detected in the analysis involved the hornworts one way or the other." Thus, it seemed very difficult to designate the outgroup of the Anthocerotae. Recently, Mishler et al. (I 992) and Waters et al. ( 1992), however, showed the mono­ phyletic origin of land plants including the Anthocerotae and the paraphyletic relationships of bryophytes based on their molecular approach to the phylogeny of bryophytes, and gave support to the view of Mishler and Churchill ( 1985), i.e., that the Anthocerotae are the sis- J. HASEGAWA : New classification of Anthocerotae 23 ter group of the lineage including the Musci and the Tracheophyta, and the Hepaticae is the sister group of the remaining land plants including the Anthocerotae. The present study is intended to revise the classification of the Anthocerotae through developing the ideas on which the analysis of Mishler and Churchill (1985, 1984) was based. CLADISTIC ANALYSIS OF THE ANTHOCEROTAE Taxa included in the cladistic analysis In this analysis the following ten genera or subgenera were recognized as operational taxonomic units (OTU); Anthoceros, Apoceros, Dendroceros, Folioceros, Hattorioceros, Leiosporoceros, Megaceros, Notoceros, Notothylas [in Schuster's (1992) nomenclature the genus Aspiromitus was accepted, and consequently Phaeoceros was reduced into a syn­ onym of Anthoceros, but to avoid confusion here I follow the traditional Proskauer (1951) nomenclature]. Hattorioceros was a taxon recently described as a subgenus of Phaeoceros for a species with unusual spore features which had not been known from the Anthocerotae (Hasegawa 1994). In the classification of Hassel de Menendez (1988) another genus Sphaerosporoceros was recognized, but it was not included in this analysis, because as sug­ gested by Schuster (1992) the naturalness of the genus Sphaerosporoceros as defined by Hassel de Menendez was debatable. On the contrary, Notoceros (Australoceros sensu Hasegawa) and Apoceros which were not treated by Hassel de Menendez (I 988), were included in this analysis, as I considered them as well-defined. Methods of the analysis Forty-two characters listed below were analysed using the branch and bound algo­ rithum in PAUP (version 3.1 for the Macintosh; Swofford 1993); no transformation series were hypothesized for the multistate characters and all character states were weighted equally, and the Hepaticae and the Musci were designated as outgroups based on the phy­ logeny for the bryophytes presented by Mishler and Churchill (1985), Mishler et al. ( 1992) and Waters et al. (1992). The distribution of characaters among ten taxa and the outgroup is given in Table 2. Characters included in this analysis I. Archegonium stalked (with free archegonial wall) (O); embedded in thallus (without free archegonial wall) (1). 2. Antheridium originated exogenously (O); endogenously ( l ). 3. First division of zygote transverse (O); vertical ( l ). 4. Slime papillae or slime hairs present on gametophyte (O); absent. (1). 5. Stoma-like clefts absent on gametophyte (O); present (1). 6. Asymetric spermatozoid (O); bilaterally symetric spermatozoid (I). 7. Channel thylakoid absent (O); present (1) 8. Ability to distinguish D-methionin absent (O); present (1). Table 2. Character matrix used for this analysis. "'.j>. (1) (2) (3) (4) (5) (6) (7) (8) (9) (10) (11) (12) (13) (14) (15) (16) (17) (18) (19) (20) (21) Anthoceros 1 1 l 1 1 1 1 1 0 0 0 0 I 0 011 0 1 0 0 Folioceros I I I 1 1 1 1 I 0 0 0 0 1 0 Oil 0 I 0 0 Phaeoceros 1 1 1 I I l 1 I 0 0 0 0 0 Oi l 0 0 0 0 0 Leiosporoceros 1 1 1 l 1 1 I 1 0 0 0 0 0 0 0 ? ? 0 0 Hattorioceros 1 1 1 1 I 1 I 1 0 0 0 0 0 0 0 ? ? 0 0 Megaceros I I 1 1 1 1 1 1 0 0 0 0 0 0 0 1 0 0 0 Notoceros 1 I I 1 1 1 1 1 ? 1 0 0 1 0 0 1 0 0 0 Dendroceros 1 1 1 1 1 1 1 1 1 I 1 I 0 0 0 1 0 0 0 Apoceros 1 I 1 I 1 1 1 I 1 I I I 1 0 0 I 0 0 0 1 Notothylas 1 1 I I l 1 1 I 0 0 0 0 0 0 0 0 0 1 1 011 0 ~ ::i:: ::::: "'0 Hepaticae 0 0 0 0 0 0 0 0 ? Oi l I ? 011 Oi l Oi l 011 ? 0 0 ? 0 :l. Musci 0 0 0 ? 0 0 0 I ? ? 0 ? ? 011 Oi l ? ? 0 0 ?