Systematic and Phylogenetic Consideration of the Ranunculaceae and Berberidaceae

Jan. 20, 1938.] M , KUMAZAWA -RANUNCULACEAL AND BERBER IDACEAE. 9

Systematic and Phylogenetic Consideration of the Ranunculaceae and Berberidaceae.

Masao Kumazawa.

Received September-10, 1937.

I. The Ranunculaceae is one of the largest families among the Dieotyle- dons, comprising probably about fifty genera and thousands of species, distributed widely all over the world. Among them, nearly thirty genera have been found wild or cultivated in the territory of the Japanese Empire. The endemic genera are Glaucidium SIEI3oLTet ZUCCARINI,Aneronopsis SIEBOLTet ZUCCARINI,Miyakea MIYABEet TATEWAKIand Megaleranthis Ouwi, all of which are monotypic. The Berberidaceae is closely related to the family mentioned above, and is a smaller family comprising more than ten genera, some of which are monotypic or include a small number of species, distributed mostly over Asia and North America. According to the system of ENGLER-DIELS(1936), which is now most often referred to, the Ranunculaceae is divided into four tribes, i.e. Paeonieae, Hydrastideae, Ilelleboreae and Anemoneae; the Berberidaceae into two subfamilies, Podophylloldeae and Berberldoldeae, the latter subfamily further into two tribes, Epimedieae and Berberideae. From the systematic point of view, however, both families seem to include extremely heterogenous types, and the systematic affinities of some genera are now left undecided. Even from the morphological and biological points of view, there are many interesting characters which are not common to the ordinary members of the Dicotylendons : some genera or species have the medullary bundles, the fused cotyledons, the trimerous floral elements, the short- lived tap roots and the V-shaped xylem. These characters as well as the developmental mode of pollen grains and of endosperm, are common to some of the Monocotyledons and to the Ranales, to which the present families belong, so that the phylogenetic relationship between the Ranales and the Monocotyledons-especially the Helobiae-has been suggested by numerous authors, and it is the view usually accepted that the ranalian families are the representatives of the primitive Angiosperms; moreover, 10 TIIL' BOTANICALMAGAZINE. [ ~'o1.Lli, No, 613. some features of the IRanales have often been noticed by some authors in the phylogenetic consideration of the origin of the Angiosperms. In these respects, the Ranuneulaceae and its allies as the representatives of the ranalian families are so interesting that the morphology and anatomy of the floral and vegetative organs have been studied by numerous authors from various points of view. The morphology, anatomy and biology of the Berberidaceae were studied by CITLRNE(1893), TISCIILER (1902), I-IIMMELBAUR(1913),SCIIMIDT(1928), CIIAI'MAN(1936) and others. Although the morphology and anatomy of these families have been studied by such a large number of authors, our present knowledge regarding these families is not SOSufficient as to make further studies unnecessary, especially in respect of the systematic affinities. For years past, therefore, the writer has been working, under the suggestion of Professor V. OGUIIAof the Tokyo Imperial University, oii the comparative anatomy and morphology of the two families, the results of which have been set forth in the series of papers (1930-1938). In this paper, a general colsideration will be made regarding the systematic affinities, though some remarks regarding these have often been made in the previous papers.

II. The genus which is farthest deviated from the ordinary type of the Ranunculaceae seems to the writer to be represented by the genus Paeoala, which has been included by LOTSY(1911) and LANGLET(1932) in the Berberidaceae ; by BARTLING(1830), WORSDELL(1908) and HLINTZE(1927) in a separate family Paeoniaceae. The carpellar structure of Paeoa2a mentioned in the writer's previous paper (1938), however, evidently shows the ranunculaceous affinities rather than the berberidaceous. However, as was already described (KUMA- ZAWA,1935), the vegetative structure of Paeonia is clearly distinguished from all the ranunculaceous or berberidaceous genera in respect of the scalarif orm-perforation of vessels and of the narrow secondary ray tissue appearing close to one another from the innermost part of the secondary xylem ; moreover, the ovular structure of the genus, as already stated (KUMAzAwA,1938), is also quite unique among the Ranunculaceae, tile outer integument being very strongly developed and thick, the nucellar tissue absorbed before the flower comes to bloom, and the internal epidermis of the inner integument metamorphosed into the palisade tissue (Mantel- gewebe). If the characteristic features stated by WORSDELL(1908), as well as the vegetative and ovular structure noticed by the present writer as of phylogenetical significance, are considered, it seems most reasonable Jan.20, 1038.1 M. KUMA%AWA--RANUNCULACEAEAND BERBERIDA.CEAE. 11 to the writer that the genus is separated from the Ranunculaceae or Ber- beridaceae and represents the family Paeoniaceae. According to HETNTZE (1927), who studied the floral morphology and ecology, the Paeoniaceae is the most primitive type of what lie called Paeoniales, in which the Ranun- culaceae, Berberidaceae, Menispermaceae and Lardizabalaceae are included. According to EN~GLER-DEILS(1936), the genera (]laucidlizczn and Ilydrastis constitute a tribe Hydrastidea~ of the Ranuiiculaceae ; and they constitute a berberidaceous subfamily Glal.icidioideae or Ilydrastidoideae according to HIMMELBAUR(1913) or MIYAJI (1930), however, they were ineluedd, together with the other genera, in the Podophylloideae, a subfamily of the Berberidaceae by LOTSY(1911), I-IEINTZE (1927) and WETTSTEIN(1935) . Most of these authors believe that Glaucidiu in and Ilydrastis, as well as Poclophyllum and Diphylleia, are the transitional types between the Ranunculaceae and Berberidaceae. The present writer (1930 b) offered the opinion that the subfamily Glaucidioideae and :Podo- phylloideae of the HIMMELBATJR'SSystem may be included in a transitional family Podophyllaceae. In fact, Glaucidium and Hydrastis are closely related genera (KUMA- ZAWA,1930 b, 1936 a, 1936 b) , although they differ from each other in the nature of the fruit and in the ovular structure (KUMAZAWA,1938). The gap between Glaucidium-Hydrastis and Podophyllum-Diphylleia is, however, very large, not only in the vegetative features whicli were described in the previous papers (KUMAZAWA,1930 b, 1936 a, 1937 b), but also in the floral features, especially in the dehiscing type of the anther (KuMAZAWA,1937 c), and also in the carpellar structure (KUMAZAWA 1938). So that the writer now comes to the opinion that Glaucidiuin and Ilydrastis are to be reasonably excluded from the family Podopliyllaeeae, correcting his opinion offered before. It is a matter for consideration whether Glaucidium and Hyclrastis are included in the Ranunculaceac as a subfamily Glaucidioideae, or they constitute a separate new family Glaucidiaceae ; but at piesent the writer puts them provisionally uniter the Ranunculaeeae as a subfamily Glaucidioideae. The ranunculaceous genera, except Paeonia, Glaucid iuin and H yd rastis, are divided into two groups, i.e. into tribes Helleboreae and Anemoneae by PRANTL(1887, 1891), LOTSY(1911) and ENGLEII-DIELS(1936), into subfamilies Helleboroideae and Anemonoideae by WETTSTLIN(1935) ; into several groups, i.e. into tribes IIelleboreae, Anemoneae and Ranunculeae by BROULAND(1935), into subfamilies Ilelleboroideae, Adonioideae, Thalictroideae, Anemonoideae and Ranuiiculoideae by IIEIx Tzu (1927). Especially the system of LANGLET'sis most open to criticism, for he, coii- sidei ing the caryotype of each genus, put the multiovular genera such as 12 THE BOTANICALMAGAZINE. [vol.LII, No. 613, i!sopyrum, Aquilegia and Coptis together with the uniovular genus Thalic- truJU,, into the Thalictroideae, and the niultiovular genera such as Helle- 1)orus, Trollius, Delphi~2min, Nigella, Aeon itum, Ciricifuga also together with the uniovular genera such as Ranunculus, Clematis, Anemone, into the IRanunculoideae. It seems to the writer more reasonable that these genera should be grouped into two subfamilies Helleboroideae and Ane- m.onoldeae as in WETTSTEIN'Ssystem. Although both groups are not distinguished, in the strict sense, from each other by the position and IlunIber of ovules or by most of the other floral and vegetative features, they are probably distinguished by the nature of the fruit, follicle or achene ; the Helleboroideae has the follicle, except Actaea whose fruit is baccate and indehiscent, and the Anem.onoideae the achene containing a single seed. The genus Callianthemum, which is considered as of the helleborean affinities by PRANTL(1891) , S cIIRODINGER(19'09) , h0TSY (1911) , WETTSTEIN (1935) and ENGLER-DIELS(1936), seems to be close to Adonis of the Ane- moiloideae in its affinities. This view regarding the affinities of Callian- themu4n ;+.scolnci(lent with that of IfEINTZE and of ZANGLET. LOTSYsays that the Helleboreae and Aneinoneae may be treated as two separate families, and NAKAIis of the same opinion. I f a separate family Helleboraceae is accepted, Glauciclium and Ilydrastis should, of course, represent a distinct family Glaucidiaceae.

III. Among all the berberidaceous genera in the ENGLER's system, the genus Nandina is considered phylogenetically farthest deviated. In this genus, the aerial stein elongates monopodially until it terminates in all inflorescence, producing two to four (rarely up to six) foliar and one to three scale leaves every year. When the nionopodial stem terminates in an inflorescence, the axillary bud, embraced by a foliar leaf in the upper part of the axis, elongates to represent a new axis which also terminates iii an inflorescence in the following year. The slender shrubby stem of the adult plant is, therefore, represented by a sympodial axis. As was described in the previous paper (KTJMAZAWA,1938), the outer integument of Nandina is strongly developed and the mieropyle is not ob- served from outside ; moreover, the nucellus is absorbed before the flower comes to bloom and the external epidermis and the internal one change into the thin-walled columnar tissue. These vegetative and ovular characters, as well as the dehiscing type of anther described before (KUMAZAwA, 1937 c ), are quite unique among the berberidaceous genera. This genus, together with the other herbaceous genera such as Epi- med ium, Achlys, Je ff ersonia, etc., was included in the tribe Epimedieae Jew.20,193.J M.1iUMAZAII7A-1?ANUNCULACEAEAND BERBERIDACEAE. 13 by PRANTL(1891), TISCIILER(1902), HIMMELBAUR(1913) and ENGLER- DIELS (1936), but a subfamily Nandinoideae was established by KEINTZE (1927), and a family Nandinaceae by NAKAI(1936) for the genus. The present writer now supports the view of NAKAI's, believing the genus 11TCCrzdiota to be a representative of the distinct family Nandinaceae. It is the opinion usually expressed that Nandina and Paeonia represent the genera which are most primitive among the members of the Ber- beridaceae and Ranunculaceae. According to the writer's opinion, however, these two genera are iiot to be assumed to be mother forms from which the other genera of the Berberidaceae or Ranunculaceae have been derived directly, but they seem to belong respectively to two independent lilies of evolution separated from other members of these families. In comparing the two genera with each other, we find features which are plljrlogcnetically more primitive in the genus Paeonia than in the other. Podophyllum and Diphylleia are usually included in the Podo- pliylloideae of the Berberidaceae by most of the recent authors such as L®TSY(1911) , IIIM 1\IELBAUR(1913) , WETTSTEIN(1935) , and E NGLER-DIELS (1936) ; LOTSY and WETTSTEINinclude Glaucidiur and H ydrastis in one and the same subfamily together with Podophyllum and Diphylleia. TISCHLER(1902) is the first author who established a family Podophyllaceae consisting of Pod ophyll um and Diphylleia. The two genera Poclophyllum and Diphylleia are related to each other in their vegetative structure, as noticed in the previous paper (KUMALAWA 1930 b), but they differ from each other in the dehiscing type of anther (KUMAZAWA,1937c), in the structure of pollen grains (KUMAZAWA,1936 a ) and also in the type of vernation (KUMAZAWA,1937 b). Although in his paper of 1930 the present writer included Pod ophyllum and Diphylleia in one subfamily Podophylloideae under the Podophyllaceae, yet he now hel ds the opinion that, taking into consideration the characters which are mentioned above; Diphylleia may more reasonably be excluded from the group. If the genus Diphylleia is excluded from the Podophyllaceae, its systematic treatment is a matter for consideration. IIEINTZE (1927) put the genera Pod ophyllum, Glaucidium and Hyd rastis into the Podoph.ylloi- deae, and the genus Diphylleia into the Epimedieae, but it may depend on the method of treatment whether the genus represents a tribe Dipliylleieae under the Epimedioideae. In this respect, further consideration or criticism may be expected. The berberidaceous genera of the ENGLER'ssystem, except Nandina, Podophyllum, and Diphylleia, are, in the writer's opinion, to be grouped under two subfamilies, Berberidoideae and Epimedioideae, although they 14 THE BOT11N1CALMAGAZINE. [Vol.LII, No. G1.3. are grouped under two tribes herberideae and Epimedieae in the ENGLER'S system. The herberidoideae and Epinledioideae resemble each other in having the anther with valves, but are clearly different from each other 1n the living form, the mode of branching system and the structure of pollen grains. Berberis and Mahonia which constitute the herberidoideae are shrubs and their aerial axes elongate quite monopodially, the inflorescence being produced at the terminal of the short shoot in Berberis, or in the axillary part of the scale in Mahonia, while the genera of the Epimedioi- deae are all rhizome-perennials. The most striking differences between the two subfamilies are found in the pollen grain structure, as already stated (KUMAZAWA,1936 a). The pollen grains iii the herberidoideae have no germinal apparatus of the primary origin, while those in the Epimedioi- deae usually have three germinating furrows which run I)arallel to one another. Therefore, there may be a large phylogenetic gap between the two. If the smalll families are accepted, a family Epimediaceae may be considered. The writer proposes to establish, underr the Epimedioideae, three tribes Epimedieae (Epiredin m, Lc ontice, Ca ulophyllum, Jefferson ia, Plagio- legma), Achlyieae (Achlys) and Ranzanieae (Ranzania). Among the genera of these tribes, Ranzania is most interesting in its affinities and is believed to be a form, phylogenetieally equally deviated both from Berberis°°- Mahonia and from otherr genera of the Epimedioideae, as already dis- cussed in detail. ( KUMA7AWA,1937 c).

The writer wishes his sincere thanks to Professor Y. OGUimAand Professor T. NAKAT,both of the Tokyo Imperial University, for their encouragement and advice throughout the course of the series of works. BiologicalLaboratory, The Fourth Higher School,Kanazawa.

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KUMAZAWA, M. (1930 a) . Studies on the structure of Japanese species of Ranunculus. Journ. Fac. Sci. Imp. Univ. Tokyo. Sec. 3. Bot. 2, Part 3. -- (1930 b). Morphology and biology of Glaucidiurn palnatum SIEB, et Zucc. with notes on affinities to the allied genera Ilyclrastis, PodophyUurn and Diphyllcia. Ibid. Part 4. (1932 a). Morphological studies of Aneronopsis, Aetaca and Cimici f uga. Ibid. Part 6. (1932 b). The medullary bundle system in the .Ranunculaceae and allied plants. Bot. Mag. Tokyo, 46. (1935). The structure and affinities of Paeonia. Ibid. 49. (1936 a). Pollen grain morphology in Ranunculaceae, Lardizabalaceae arid Berberidaceae. Jap. Journ. Bot. 8. (1936 b). Podophyllum pleianthum HANCE. A morphological study with sup- plementary notes on allied plants. Bot. Mag. Tokyo, 50. (1937 a). On the morphology and anatomy of Achlys japonica MAXIM. Ibid. 51. (1937 b). Comparative studies on the vernation in the Ranunculaceae and Berberidaceae. Journ, Jap. Bot. 13. (1937 c). Ranzania japonica (Berberidac.). Its morphology, biology and systematic affinities. Jap. Journ. Bot. 9. -- (1937 d). Developmental history of the abnormal structure in the geophilous organ of Aconitun. Bot. Mag. Tokyo, 51. (1938). On the ovular structure in the Ranunculaceae and Berberidaceae. Journ. Jap. Bot. 14. LANGLET, 0. F. (1928). Einige Beobachtungen uber die Zytologie der Berberidaceae. Svensk. Bot. Tidskr. 22. -- (1932). Uber Chromosomenverhaltnisse and Systematik der Ranunculaceae. Ibid. 26. LoTSY, J. P. (1911). Vortrage uber botanische Stammesgeschichte. 3. Jena. MIYAJI, Y. (1927). Uber die somatischen Chromosomen einiger Ranunculaceen. Bot. Mag. Tokyo, 41. (1930). Beitrage zur Chromosomenphylogenie der Berberidaceen. Planta, 11. NAKAI, T. (1.936). Flora sylvatica Koreana. 21. PRANTL, K. (1887). Beitrage zur Morphologic and Systematik der Ranunculaceen. ENGLERSBot. Jahrb. 9. (1891). Ranunculaceae, Berberidaceae. ENGLERS naturl. Pflanzenf am. Teil 3, Abt. 2. RASZNER,E. (1931). Primitive and abgeleitete Merkmale in Blutenbau einiger Ranun- culaceen. Planta, 15. SCHMIDT, E. (1928). Untersuchungen fiber Berberidaceen. Beih. Bot. Centralbl. Abt. 2, 45. SCHNARF, K. (1931). Vergleichende Tmbryologie d.er Angiospermen. Berlin. SCZIRODINGER,R. (1909) . Der Blutenbau der zygomorphen Ranunculaceen and seine Bedeutung fur die Stammesgeschichte der Helleboreen. Abhandl, d, k, k, zool.- bot. Gesells. Wien. 4. WETTSTEIN, R. (1935). Handbilch der systematischen Botanik. Aufl. 4. Wien-Leipzig. WoRSDELL, W. C. (1908). The affinities of Paeonia. Journ, of Bot. 46. ZIMMERMANN,W. (1930). Die Phylogenie cler Pflanzen. Jena.