Journ. Hattori Bot. Lab. No. 64: 59-66 (June 1988)

FAMILY RELATIONS-STRUCTURAL BASES IN THE JUNGERM ANNIALES

JIRf VANA

ABSTRACT: The most elaborate available system of the order is that of Schuster (1984).40 families are grouped in 15 suborders. In the present paper the problem of delimitation and relationship of the higher categories (families, suborders) as well as the problem of primitive and derivate groups are discussed. A detailed analysis of the suborder Jungermanniineae is provided.

Within the present system of the order J ungermanniales three categories are used for expressing the mutual relationship of the individual genera, viz. subfamily, family and suborder. Thus, from the general point of view, three levels of relationship can be distinguished; yet, the system itself does not say anything about affinities within the level itself (genera in the subfamily, subfamilies in the family and fa milies in the sub­ order), similarly as the relationship or linking-up of the individual suborders. This, consequently, leaves enough room for various interpretations by various authors and thus also for the differences of the systems used. Mutual relationships of the individual suborders is suggestive of their evolution. In essence one can say that there are three groups of suborders within the order Junger­ manniales: a) the so-called "ptilidioid" complex - i.e., the evolutionary line Herbertineae - Ptilidiineae - Lepidolaenineae and Porellineae; b) the so-called "jungermannioid" complex - i.e., the bush schema of the suborders probably developed again from an ancestor of the Herbertineae: Lepidoziineae, Cephaloziineae, Antheliineae, Jungermanniineae, Balantiopsidineae, Lophocoleineae and Brevianthineae; c) isolated suborders, often of unclear relationship: Lepicoleineae, Perssoniellineae, Pleurozi­ ineae and Radulineae. Similarly there exists within the individual suborders a certain linking-up of the individual families (or their ancestors) ; there exist certain initial, basic, more primitive families which form the basis of the more derived, advanced groups (e.g., Herbertaceae in the suborder Herbertineae, Geocalycaceae in the suborder Lophocoleinease, Lopho­ ziaceae in the suborder Jungermanniineae, etc.).

DELIMITATION OF THE HIGHER TAXONOMIC CATEGORIES At present there are several studies available dealing with the views of or even genus concept in liverworts (or ) from the general point of view. Yet, there are practically no studies devoted to general specification problems of higher taxonomic units (family, order, or subfamily, suborder). Schuster (1984, p. 930) states

1 Department of Botany, Charles University, Bemitska 2, CS-128 01 Praha 2, Czechoslovakia. 60 Journ. Hattori Bot. Lab. No. 64 1 988 correctly: "The students of both the Hepaticae and Musci faces a major problem: the dearth of 'good' ordinal criteria." It is true that the concept of higher taxonomic categories (families, orders) is largely given by the state of our knowledge of mutual relations of lower taxonomic categories (species or genera); this results also in a change of views with changes in concepts. If a broad genus is divided into several new, more narrowly accepted genera, there automatically appears the necessity of mutually defining their mutual relation­ ship by forming a higher taxonomic category. In many cases the present suborders in Schuster's system (1973, 1984) practically correspond with the concept of families in certain previous systems. Similarly also Schuster (1984, p. 932) himself, after criticism of Sljakov's (1972) approach to the concept of higher taxonomic categories, admits that " time, probably, is on side of the Schljakov classification." Schuster (1953, p. 301) based his pioneer classification of the order Jungerman­ niales into suborders on I. Gross morphology of the gametophyte (leaf insertion and type); 2. Type of rhizoid initials; 3. Type of vegetative reproduction; 4. Type of de­ velopment of sporeling; 5. Degree of preservation of sporophyte seta; 6. Sporejelater ratio; and 7. Biological and ecological features of the major groups. The present delimitation of families and subfamilies is also predominantly based on the anatomical and morphological characters of the gametophyte, reproductive organs and sporophyte. The sporophyte characters considered from the point of view of evolution as more constant, less influenceable by environmental changes, usually are not - due to considerably simple sporophyte in this order - the main, defining characteristic for delimitation of higher level units, but act as parallel or supplementary characters in the complex of characteristics. All systems attempt to produce even in higher taxonomic categories (beginning with subfamily) integrated, phylogenetically related, homogenous groups. Gradual development of our knowledge helps us to approach ever closer to this aim. Yet, from aspect of classification there appear certain problems, the most serious of which seems the application of a certain rank and definition and characteristics of the taxonomic units. The differences between the above mentioned recent systems consist mainly in the application of various ranks (usually families or subfamilies) to certain units. The phenomenon is quite understandable, as there practically does not exist any criterion (and even if it existed, there would be problems with its application) which would de­ termine which characters are sufficient for differentiation at the family level, and, on the other hand, which characters delimit a subfamily only, etc. A similar situation exists in the case of definition, delimitation of a certain category (family, subfamily, suborder etc.). There are only a few phylogenetically isolated groups (e.g., Perssoniel­ laceae, Pleuroziaceae, Radulaceae) which can be clearly defined by one or a few char­ acters. Most units are characterized by a complex of characters none of which may be absolutely valid (mechanical absolute application leads to artificial conceptions). The above arguments are clearly documented, e.g., by the situation in the suborder Jun­ germanniineae. - GYMNOMITR IOID " LINE (GYM NOM ITRIA CE AE)

A ~

~ ~ • = a - - ~ i -~ =: ~ i ~ =lQ ~ TABLE 1. Synapomorphous character states and diagnostic features of the "gymno­ :If ~ • E I! -:;; ~ = mitrioid" line (suborder Jungermanniineae). Numbers correlate with those in Fig. 1.

1. Stem paraphyllose :-­ < 19 _ 2. Leaves chlorophyll-free :>. Z < 3. Leaves undivided :> 4. Leaf insertion oblique 'Ti 5. Oil-bodies absent from all mature cells I'> §. 6. Underleaves ± absent -< 7. Coelocauly (Tylimanthus-type) present !l Capsule sphaerical 8. eo· 9. Perianth lacking or low, not attaining apices of bracts, perigynium present ::l V> 10. Terminal branching (Frullania-type) totally absent S· 11. Leaves bilobed (or± unlobed), never trilobed S- 12. Leaves erect to erect-appressed, unlobed to shallowly (to 0, 1-0,2 their length) bilobed .....e> t: 13, Leaves margined with thinner- or thicker-walled cells ::l 14. Cuticle coarsely papillose ~

15. Gynoecia lacking bracteoles 3I'> ::l li i 16. Leaves closely imbricate, the stem hidden ::l ;;;. 17. Oil-bodies lacking in marginal decolorate cells 18. Perianth lacking, perigynium absent (weak vestigal, never tubular perigynium ± ~ present) 19. Leaf lamina plicate II~IS 1.2.3.4

FIG. I. Cladogram of the "gymnomitrioid" line of the suborder Jungermanniineae. ~ See Tab. 1 for synapomorphies. 0- "SCAPANIOIO " LINE N

~ ..-----A----. ,A, ~ ~ ,. i ~ ~ I ~ - z -z i - i ~ 5 ! ! ~ -=c; ~ ~ == TABLE 2. Synapomorphous character states and diagnostic features of the "scapanioid" line (suborder Jungermanniineae). Numbers correlate with those in Fig. 2.

1. Leaves bilobed to 0, 3 their length 2. Leaves conduplicate 3. Ventral leaf margin modified to form a water-sack ..... 4. Gemmae solitary, parenchymatous, pluricellular o ~ !!:; 5. Leaves complicate-bilobed ? 6. Antheridial stalk I-seriate 7. Terminal branching (Frullania-type) lacking ~ 0- 8. Rhizoids scattered :=! . 9. Leaves bitobed, lobe apices obtuse to apiculate ;atxI 10. Gemmiparous shoots absent, no underleaves r 11. Leaves distinctly keeled ~ ?" 12. Cells ± thick-walled Z 13. Leaves distinctly keeled (cf. 11) ? 14. Leaf cells with vaxy cuticle ~ 15 . Perianth flattened ]6. Elaters I-spiral to annulate 17. Exospor surface finely granulate to vermiculate 18. Leaf lobes rotundate to broadly ovate 19. Gemmae angulate to stellate

1.3. 4

FIG. 2. Cladogram of the "scapanioid" line of \0 the suborder Jungermanniineae. See 00 00 Tab. 2 for synapomorphies. -JUNGERMANNIOIO" LINE TABLE 3. Synapomorphous character states and diagnostic features of the "jungermannioid" line (suborder Jungermanniineae). Numbers ... ~ correlate with those in Fig. 3. ~ - - i ~ ~ - I. Perianth sometimes reduced (or vestigal), perigynium or marsupium ± present !OI § i E s ~ ,. I t!OI 2. Leaf-like androecial bracts with only dorsal half of the bract base ventricose I T i i i I' =I "I 71 3. Rhizoid-bearing marsupium (lsotachis-type) present 21 21 4. Spore/elater diameter ratio I, 3- 1, 5: 1 25 ~ 24 5. Antheridial stalk I-seriate 6. Perianth strongly laterally compressed, with wide mouth ;,.<. 7. Epidermal cells of capsule wall with ± 2-phase development z;,. ' 8. Branching predominantly postical-intercalary 9. Leaves unlobed, rarely shallowly bifid ;p 10. Gemmae usually always present §. 11 . Underleaves mostly absent, if present, reduced, lanceolate '< ~ 12, Antical merophytes deeply interlocking [ 13. Gemmae polygonal-stellate o· ::l 14. Antheridial bracts I-androus :i''" 15 . Capsule cy lindrical & 16, Leaves with margins ± incurved, strongly concave (1).... t: 17. Gynoecium with bracts edentate ::l 18 . Bracteole lacking ~ 19. Spore/elater diameter ratio ± 1 : 1 ~ 20. Rhizoids scattered ::l ::lro ' 21 . Leaves opposite e> 22. Plagiochilo id leaves and cnemis present '" 23 . Shoot tips autonomously arched towards substrate 24. Only postical-intercalary branching present 25. U nderleaves lanceolate or absent 26. Antheridial bracts l-androus (cf. 14) 27, Antheridial bracts "scapanioid", with dorsal lobe 28. Perianth reduced or lacking, modified to free laciniae, surrounded by the FIG. 3. Cladogram of the "jungermannioid" line of the suborder Jungermanniineae. See Tab. 3 for erect, connivent bracts 0\ synapomorphies. w 64 Journ. Hattori Bot. Lab. No. 64 1 988

The above mentioned suborder includes three developmental lines, viz. the "jun­ germannioid", the "gymnomitrioid" and the "scapanioid" one. According to the "con­ servative" c1assifi:.:ation three families would correspond to this concept. Yet here the present systems already considerably differ. In all systems the "gymnomitrioid" line (Fig. 1) corresponds to the family Gymnomitriaceae. The "scapanioid" line (Fig. 2) represents in systems of Engel (1982) and Grolle (l983a) also a single family Scapani­ aceae, but Schuster (1980, 1984), on the other hand, divides it into the families Scapani­ aceae, Blepharidophyllaceae and Delavayellaceae. The problem is most complicated in the largest "jungermannioid" line. Histori­ cally this line (Fig. 3) was divided in various systems into the "jungermannioid" group (family Nardiaceae according to Miiller 1939-1940) and the "Iophozioid" group (fami­ ly Lophoziaceae). This concept was followed until 1970 when Schuster (I 970) published his proposal of the concept of a single broad family J ungermanniaceae comprising 9 subfamilies. The proposal was basically accepted by other authors (Grolle 1972, Vana 1973) until Steere and Inoue (1975) suggested exclusion of the family Mesoptychiaceae and separated again both original families Jungermanniaceae and Lophoziaceae. The thus modified system has since been accepted by Enge! (1982), Grolle (1983a) and Vana and Inoue (1983). The still not uniformly conceived problem [Schuster (1984) still main­ tains his opinion, Grolle (l983a, b) published two studies with different conceptions, etc.] are summarized by Enge! (1982, p. 287) who writes the following (before enumerat­ ing the 8 differences between the families Jungermanniaceae and Lophoziaceae): "In recent years several authors have combined the family (= Lophoziaceae) with the Jungermanniaceae: this procedure overly distends the Jungermanniaceae with hetero­ genous elements. Rather than maintain an inflated family Jungermanniaceae, with some 33 genera, the Lophoziaceae and Jungermanniaceae are treated here as distinct families differing primarly by the following features. It will be noted that several of the features are not clear-cut, but rather represent significant tendencies which, taken en masse, lend support to recognition of 2 families." The definition of individual subfamilies also remains disputable. As demonstrated by the attached cladograms (Figs. 1- 3), there are clearly separated the Mylioideae and Notoscyphoideae within the "jungermannioid" line (if Lophoziaceae, Mesoptychiaceae and Jungermanniaceae are considered as separate families). If we decide not to separate the primitive types of the families Lophoziaceae (Chandonanthoideae) and Jungerman­ niaceae (Scaphophylloideae) as independent subfamilies (in accordance with the pre­ sent systems), it remains to evaluate the very problematic complex lamesoniel/a (and related genera) - (together with Protosyzygiel/a) - Nothostrepta - Hattoria - Gottschelia (and the relation of the genera Anastrepta and Roivainenia to this complex). I assume that the problem, if it is the case of a single subfamily (Jamesonielloideae­ cf. Inoue 1966) or a complex belonging to 6 subfamilies (Schuster 1984), will be dif­ ficult to solve without the use of further biosystematic approaches and will essentially remain the question of personal opinion. Within the family Gymnomitriaceae the separation of the subfamil y Stephaniel- J. VANA : Family relations in the Jungermanniales 65 loideae is clear, but we might even separate the genus Prasanthus into the separate sub­ family. Without a subjective criterion of a "degree" of relationship one cannot univocal­ Iy determine which of the four groups within the broadly accepted Scapaniaceae (De­ lavayelloideae, Blepharidophylloideae, Douinioideae and Scapanioideae) are "still" subfamilies and which are " already" families. A similar situation exists also in the other suborders. Let me mention, for example, the different concepts of the family Pseudolepicoleaceae (suborder Herbertineae), the problem of subfamilies within the family Geocalycaceae (suborder Lophocoleineae), etc.

CONTEMPORARY PROBLEMS AND PERSPECTIVES The presently used system of families within the order Jungermanniales results from long-term studies based on the methods of classical and comparative anatomy and morphology. As such the system is basically accepted by all bryologists and we can say that it corresponds to our present knowledge of phylogeny within the order. In some cases modern methods (study of spermatozoid morphology, study of chemical substances - cf. Schuster 1984, pp. 919-920) confirmed the justification of certain parts of this system; this speaks in favour of its reliable basis. Within their modifications of the system the individual authors differ in the following: a) Estimation of the taxonomic value of some groups and the number of families connected with it [Sljakov (1972) - 39 families, Engel (1982) - 43, Grolle (1983a) - 39, Schuster (1984) - 40]. b) Classification of certain genera or even subfamilies into higher units. c) Modification of the suborder system (Sljakov 1972) or even their rejection (Grolle J983a). It is quite clear that the existing system is not invariable and is bound to change. Obviously, new significant findings must find their application in the system. It is my personal view that solution of the unclear places in the system should be undertaken after accumulation of further, nowadays mostly unknown data by means of various biosystematic methods. Potential discussion about the placement of a certain genus to a certain subfamily, a certain subfamily to a certain family, etc., become - at the level of the present-day knowledge - more or less a question of academic discussion.

ACKNOWLEDGMENTS : The author is grateful to Dc. B. Crandall-Stotler (Carbondale) for revising the English language of the manuscript.

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onyms from the recent literature. J. Bryol. 12: 403-459. INouE, H . 1966. A monograph of the hepatic genus Syzygiella Spruce. J. Hattori Bot. Lab. 29: 171-213 . LINDBERG, S. O. 1875. Hepaticae in Hibernia mense Julii lectae. Acta Soc. Sci. Fenn. 10: 467-559. MULLER , K . 1939-1940. VI. Lebermoose. Erganzungsband. In: RABENHORST'S Kryptogamen·Flora, Vol. 6, Fasc. 1-2. Akademische Verlagsgesellschaft Leipzig. SCHUSTER, R . M. 1953. Boreal Hepaticae. A manual of the liverworts of Minnesota and adjacent regions. Amer. Mid I. Naturalist 49: 257-684. SCHUSTER , R . M. 1970. Studies on Hepaticae. XVIII. The family Jungermanniaceae, s. lat. : a reclas­ sification. Trans. Brit. Bryol. Soc. 6 : 86-107. SCHUSTER, R. M. 1973. Phylogenetic and taxonomic studies on Jungermanniidae. J. Hattori Bot. Lab. 36(1972): 312-405. SCHUSTER, R. M. 1980. The phylogeny of the Hepaticae. In: G . C. S. CLARKE & J. G. DUCKETT (eds.), systematics. Syst. Ass. Spec. Vol. 14: 41-82. " 1979". Academic Press, London, New York, Toronto, Sydney, San Francisco. SCHUSTER, R . M. 1984. Evolution, phylogeny and classification of the Hepaticae. In: R . M . SCH USTER (ed.), New manual of bryology 2 : 892-1070. The Hattori Botanical Laboratory, Nichinan. SLJAKOV, R . N. 1972. 0 vyssich taksonach peeenocnikov - klassa Hepaticae s. str. Bot. Zurn. SSSR 57: 496-508. SPRUCE, R . 1884-1885. Hepaticae of the Amazon and of the Andes of Peru and Ecuador. Trans. Proc. Bot. Soc. Edinburgh 15 : 1-588. STEERE, W. C. & H. INOUE 1975. Contribution to our knowledge of Mesoptychia sahlbergii. Bull. Natn. Sci. Mus. Tokyo ser. B, 1 : 59-72. VANA, J. 1973. Studien iiber die Jungermannioideae (Hepaticae). 1. Allgemeine Charakteristik. Folia Geobot. Phytotax. 8 : 18 1-208. VANA , J. & H. I;--';OUE 1983. Studies in Taiwan Hepaticae V. Jungermanniaceae. Bull. Natn. Sci. Mus. Tokyo ser. H, 9 : 125-142.