New Genus Sarbaicarpa Gen. Nov. (Hamamelidales) from the Cenomanianðturonian of Western Kazakhstan N

ISSN 0031-0301, Paleontological Journal, 2009, Vol. 43, No. 10, pp. 1281Ð1297. © Pleiades Publishing, Ltd., 2009.

New Genus Sarbaicarpa gen. nov. (Hamamelidales) from the CenomanianÐTuronian of Western Kazakhstan N. P. Maslova Borissiak Paleontological Institute of Russian Academy of Sciences, ul. Profsoyuznaya 123, Moscow, 117997 Russia e-mail: [email protected] Received December 3, 2008

Abstract—Anatomically preserved infructescences of Sarbaicarpa shilinii gen. et sp. nov. are described from the CenomanianÐTuronian of Kazakhstan and assigned to the Hamamelidales on the basis of their microstructure. The infructescence consists of about 30 free broadly cuneate fruits. The fruits are monocarpellate, without stylode, and basally with hairs. The seed is solitary and anatropic. Two types of sterile elements are present: (1) semispherical structures that are comparable in size to the fruits and densely covered with rounded trichomes and (2) narrow linear structures reaching more than a half of the fruit length. The new genus is characterized by a mosaic of platanaceous and hamamelidaceous characters. The plant remains are found associating with fossil leaves of the typically Platanus aspect.

Key words: Hamamelidales, reproductive structures, CenomanianÐTuronian.

DOI: 10.1134/S0031030109100104

INTRODUCTION 2007; Maslova and Herman, 2004; Maslova et al., 2005, 2007). As far as the new genus shows a mosaic The systems of angiosperm plants proposed by combination of characters of these two families, and no Takhtajan (1966, 1997) and Cronquist (1981) consider molecular data are available for the genus, I follow the the families Platanaceae and Hamamelidaceae within systems of Takhtajan and Cronquist and consider the the order Hamamelidales, which occupies a key posi- Platanaceae and Hamamelidaceae within the Hama- tion within the Hamamelidae. The recently published melidales. The existing problem unequivocally needs system of angiosperms based on molecular data abol- additional studies. ished the order Hamamelidales and classiﬁes the families Platanaceae and Hamamelidaceae within the orders To date, 16 genera of the Platanaceae have been Proteales and Saxifragales, correspondingly, thereby described on the basis of staminate and pistillate having destroyed the earlier concept about probable infructescences (Krassilov, 1973, 1976; Manchester, relationships between the two families (APG, 2003). 1986, 1994; Crane et al., 1988, 1993; Friis et al., 1988; The discrepancy between systems based on morpho- Pedersen et al., 1994; Krassilov and Shilin, 1995; logical and molecular data is far from being under- Magallón-Puebla et al., 1997; Maslova, 2002; Maslova stood, and this is in particular true for the position of the and Krassilov, 2002; Maslova and Kodrul, 2003; Mind- families in question. Whereas paleobotanical proofs of ell et al., 2006). relationships between the Platanaceae and Proteales as Data on the geological history of the Hamameli- well as Hamamelidaceae and Saxifragales are virtually daceae are much less numerous; nonetheless, nine fos- lacking, data in support of the origin of the Platanaceae sil genera have been described on the basis of reproduc- and Hamamelidaceae from a common stock are consid- tive structures (Endress and Friis, 1991; Manchester, erably representative. Thus, leaf remains are known 1994; Magallón-Puebla et al., 1996, 2001; Maslova and combining characters of the Platanaceae and Hamamel- Krassilov, 1997; Maslova and Golovneva, 2000a, idaceae (Golovneva, 1994; Maslova, 2002; and others). 2000b; Zhou et al., 2001; Maslova and Herman, 2004). Such leaves were found associating with both platana- Five of them are capitate inﬂorescences and infructes- ceous and hamamelidaceous reproductive structures cences, morphologically similar to platanaceous heads. (e.g., Maslova, 2002; Maslova and Herman, 2004). The present description of Sarbaicarpa gen. nov. Of particular interest are reproductive structures contributes to our knowledge about the diversity of fos- combining characters of the two families (Crepet et al., sil capitate reproductive structures, showing a mosaic 1992; Maslova et al., 2005, 2007). The supposed phy- combination of platanaceous and hamamelidaceous logenetic relationships between these families were characters. Of interest is the association between these earlier discussed (Crepet et al., 1992; Maslova, 2003, infructescences and leaf remains, which main morpho-

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1282 MASLOVA type is typical of the modern plane tree. Leaf remains Comparison. Sarbaicarpa gen. nov. is charac- of this morphotype accompany heads of some members terized by a mosaic of characters, some of which are of the Platanaceae (Krassilov and Shilin, 1995; diagnostic of Platanus L. as well as of several members Maslova and Herman, 2006), Hamamelidaceae of the Hamamelidaceae. The new genus is close to (Maslova and Herman, 2004), and reproductive struc- modern Platanus by the capitate infructescence, tures combining characters of the two families and, absence of a developed perianth, presence of hairs at therefore, only determinable up to the order Hamamel- the base of the fruit, more or less synchronously matur- idales (Maslova et al., 2005). Sarbaicarpa gen. nov. is ing fruits in the infructescence, a solitary seed in the recorded from the same deposits as the earlier fruit, and the presence of sterile elements in the described staminate inflorescences of Sarbaya, infructescence. Members of the modern genus Plata- assigned by its authors to the Platanaceae (Krassilov nus differ from the new genus by a much greater num- and Shilin, 1995). ber of flowers per inflorescence (up to 300), numerous apocarpous carpels in one flower (fiveÐnine), hairy fruits (most species), smaller sizes and different shape MATERIAL AND METHODS of sterile structures, and orthotropic seeds. The main The material comes from gray CenomanianÐTuro- difference of ancient platanaceous genera from Sar- nian clays of Sarbai quarry in western Kazakhstan, near baicarpa gen. nov. is a greater number of carpels in the town of Rudnyi. The plant remains were collected and flower: five in Friisicarpus (Friis, Crane et Pedersen) described by Shilin (1986). The flora includes Asple- N. Maslova et Herman1 and Macginicarpa Manchester nium dicksonianum Heer, Gleichenia sp., Sphenopteris (Manchester, 1986) and dividable on four (four or sp., Sequioa heterophylla Velen., Cedrus sp., Platanus eight) in Quadriplatanus Magallón-Puebla, Herendeen pseudoguillelmae Krass., P. cuneiformis Krass., Dal- et Crane (Magaláon-Puebla et al., 1997). Friisicarpus bergites simplex (Newb.) Sew., and Ilex sp. Later, the has orthotropic seeds. The carpel of Quadriplatanus infructescence under description was discovered and contains a solitary and non-orthotropic seed. In addi- kindly provided by Shilin to the present author for the tion, fossil members of the Platanaceae differ from the study. Collection, no. 5266 is kept at the A.A. Borisiak new genus by their developed and often differentiated Paleontological Institute of the Russian Academy of perianths. Sciences, Moscow (PIN). The collection contains two fragments of anatomi- Considering members of the Hamamelidaceae, Sar- cally preserved infructescences. After preparation, indi- baicarpa gen. nov. shows the maximal similarity to vidual structures were photographed under a CITOVAL modern Altingioideae and related fossil members and stereomicroscope (LM). Isolated fruits and a fragmen- to members of the Hamamelidoideae. The similarity to tary head were cleaned from rock remains with fluoric modern Altingioideae includes the number of flowers acid and mounted on SEM stubs. Some structures were per head, lacking perianth, presence of monocarpellate also studied under SEM after maceration with nitric gynoecium, anatropic seed, morphology of spermod- acid and alkali. Microphotographs were made under a erm, and the presence of sterile structures in the CamScan SEM in PIN. infructescence. Although bicarpellate gynoecium dominates, monocarpellate forms are also present in this subfamily (Wisniewski and Bogle, 1982; Bogle, 1986). SYSTEMATIC PALEOBOTANY The main distinguishing feature of Sarbaicarpa gen. Order Hamamelidales Wettstein nov. from modern Altingioideae is a solitary seed in the Genus Sarbaicarpa N. Maslova, gen. nov. fruit. Among fossil members of the Altingioideae, Anadyricarpa N. Maslova et Herman resembles the Etymology. From the Sarbai locality and the new genus by the presence of monocarpellate gyno- Latin carpus (fruit). ecium; regretfully, the type and number of seeds in its Type species Sarbaicarpa shilinii N. Maslova fruit is unknown because of the insufficiently preserved sp. nov. fossil remain (Maslova and Herman, 2004). The Diagnosis. Sessile spherical infructescence recently described Kasicarpa N. Maslova, Golovneva 10 mm in diameter, consists of about 30 relatively et Tekleva from the Turonian of Chulym-Yenisei loosely arranged fruits, about 30 radiating from central Depression has a monomeric gynoecium with a solitary core. Fruit widely cuneate, monocarpellate, without seed and combines characters of platanaceous and stylode. Fruit wall with solitary large glands. Fruit hamamelidaceous reproductive structures (Maslova et al., naked, basally with hairs. Seed solitary and anatropic. 2005). The main differences between Kasicarpa and About eight semispherical sterile structures are situated the new genus are the presence of a developed perianth, between fruits, nearly as large as fruits, covered with absence of sterile structures in the infructescence, asyn- numerous rounded trichomes, which leave rounded pits after abscission. Several narrow linear sterile structures 1 Maslova and Herman (2006) proposed the new name Friisicarpus (Friis, Crane et Pedersen) N. Maslova et Herman for the earlier surround fruit reaching half of its length. described Platanocarpus Friis, Crane et Pedersen (Friis et al., 1988), Genus composition. Type species. which is a later invalid homonym of Platanocarpus Jarmolenko.

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NEW GENUS SARBAICARPA GEN. NOV. (HAMAMELIDALES) 1283 chronously maturing fruits, and orthotropic seed of the 60 μm in diameter) are situated in the central area of the former genus. The similarity between Sarbaicarpa gen. seed. The cells diminish toward the periphery. The mid- nov. and modern Hamamelidoideae includes the pres- dle sclerenchyma layer is oneÐthree cells thick. Cells of ence of a solitary anatropic seed in the fruit and a devel- the middle layer are palisade, polygonal in plan, about oped endosperm. 10 μm in diameter, and with very thick walls (Figs. 4f, Remarks. Capitate infructescences of Sar- 6e, 6f). The inner layer of the spermoderm is unicellular baicarpa gen. nov. associate with leaves of the morpho- and formed by cells of 20Ð30 μ in diameter, with undu- type typical of the modern plane tree and with stami- lated walls (Figs. 4g, 4h). The seed suture is formed by nate inflorescences of Sarbaya (Krassilov and Shilin, small sclerenchyma cells with thickened walls and 1995). nearly lacking cellular content (Fig. 4e). In section, an Sarbaicarpa shilinii N. Maslova, sp. nov. undivided sclerenchyma layer is visible in the area of Etymology. In honor of the paleobotanist the suture (Figs. 6f, 6g). The endosperm is well developed (Fig. 6h) and formed of rectangular or nearly iso- P.V. Shilin (Almaty, Kazakhstan), who collected and μ studied the fossil flora of the Sarbai locality in western diametric cells 10Ð20 m in diameter (Fig. 6i). Kazakhstan. Remains of a hair bunch are visible at the base of the Holotype. PIN, no. 1/5266; capitate infructes- fruit. Hairs are mostly preserved which are adpressed to cence; western Kazakhstan, Sarbai locality, Zhirkinde- the fruit wall to a lesser or greater degree (Fig. 2d). Free kskaya Formation, CenomanianÐTuronian, Fig. 1a. hairs are preserved much more rarely (Fig. 2e), appar- Diagnosis. As for the genus. ently because of their fragility. Since the fruits are quite loosely situated in the infructescence, hairs were not Description (Figs. 1Ð8). The sessile capitate densely packed and mechanically suffered in course of infructescence 10 mm in diameter is situated on a rela- fossilization. It is difficult to judge about their length; tively thick and longitudinally ribbed axis with the maxi- apparently, they exceeded a half of the fruit length. mal diameter of 1.5 mm (Fig. 1a). The surface of the axis is covered with oval bases of trichomes (Figs. 1d, 1e). The sterile structures are irregularly situated between the fruits. There are up to eight relatively large The head consists of a central core about 2 mm in μ μ diameter and monocarpellate fruits radiating from the (950Ð1300 m long and 1100Ð1300 m wide) sterile structures (Figs. 1c, 7a), consisting of a small peduncle core and relatively loosely situated (Fig. 1b). The μ approximate number of fruits in the head does not up to 180 m wide (Fig. 7c) and a thick relatively flat- exceed 30. tened semispherical part (Fig. 7b). These structures are covered with numerous rounded trichomes about The microstructure of individual fruits was studied 10 μm in diameter (Figs. 7d, 7e), which leave distinct under SEM. Perianth elements are lacking. The length of rounded bases after shedding. The inner surface of the the fruit is 1600Ð2200 μm, and the width varies from 600 μ cuticle bears relatively large cuticular thickenings sur- to 900 m. The fruits are broadly cuneate (Figs. 2aÐ2c), rounding the apertures of the trichomes (Fig. 7f). with a relatively narrow conical base (Fig. 2c). The stylode is lacking. Rare relatively large peltate glands One more type of sterile structures which are μ present in the infructescence is represented by needle- about 30 m in diameter occur predominantly in the μ lower part of the fruit (Figs. 3e, 3f). The cuticle of the shaped, thin, about 60 m wide, linear, basally attached fruit wall is relatively thick and with a distinct trans- and distally free structures, reaching at least a half of verse striation (Fig. 3a). The external wall of the fruit is the fruit length (Figs. 8a, 8b). The maximal number of composed of twoÐfour layers of morphologically simi- such structures per infructescence is about 15. Because lar cells differing in size. The epidermis of the external of their linear outline, they are highly fragile and frag- wall of the fruit is formed by isodiametric nearly mentarily preserved; their apices are broken. The cuti- rounded cells 10Ð20 μm in diameter (Fig. 3d). Towards cle of these structures bears a distinct longitudinal stri- the inner areas, several (three or less) layers of cells are ation (Fig. 8c). The epidermis is composed of distinct present, the cells are rectangular in plan and 50 × 80 μm rows of elongated cells with strongly cutinized anticli- in size (Fig. 3c). nal walls (Fig. 8d) The fruit contains a solitary anatropic seed 900Ð Material. Holotype PIN, no. 1/5266 and frag- 1100 μm long and up to 500 μm wide in its widest part mentary infructescence PIN, no. 2/5266. (Figs. 4a, 4b, 4d, 5a). All seeds in the infructescence are approximately identical in size and shape. They are DISCUSSION elongated ovate, strongly convex ventrally, and slightly flattened (Fig. 6a). The seed cuticle is relatively thick General architecture of the infructescence. The and with a distinct transverse striation (Fig. 6b). The heads of Sarbaicarpa gen. nov. are sessile, with a lon- spermoderm includes three cellular layers. The external gitudinally striate axis and oval bases of trichomes. cover of the seed is composed of one layer of cells, There are up to 30 fruits, radiating from the central core which are variable in size, polygonal, more often tet- of the head. They are loosely situated and do not fuse ragonal, and predominantly orientated along the longi- with each other. The diameter of the infructescence of tudinal axis of the seed (Fig. 4e). The largest cells (40Ð Sarbaicarpa gen. et sp. nov. is 10 mm. The evolution-

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300 μm ‡ b c

30 μm 10 μm d e

Fig. 1. Sarbaicarpa shilinii gen. et sp. nov., western Kazakhstan, Sarbai locality, Zhirkindekskaya Formation, CenomanianÐTuro- nian: (a, b) LM; (cÐg) SEM; (a) holotype PIN, no. 1/5266, capitate infructescence on an axis, ×5; (b) holotype PIN, no. 1/5266, two fruits, ×18; (c) PIN, no. 2/5266, fragmentary head, note fruits and a spherical sterile structure (arrow); (d) PIN, no. 2/5266, axis surface with trichome bases; (e) PIN, no. 2/5266, oval base of a trichome. ary trend of heads increasing in size is known in both greater number of flowers. Quadriplatanus has about the Platanaceae and Hamamelidaceae. Thus, the diam- 40 tetramerous flowers (Magallón-Puebla et al., 1997); eter of the infructescences in different species of Creta- inflorescences of Friisicarpus and some species of Pla- ceous Friisicarpus varies from 3 to 6 mm (Friis et al., tananthus Manchester have a slightly greater (50) num- 1988; Crane et al., 1993). Heads of Eocene Macginica- ber of pentamerous flowers (Manchester, 1986; Friis et rpa reach 10Ð16 mm (Manchester, 1986; Pigg and al., 1988); about 100 flowers occur in inflorescences of Stockey, 1991). Heads of the modern plane tree often some species of Late Cretaceous Platananthus; the exceed 30Ð35 mm. The size of capitate infructescences number of flowers can reach 300 in heads of the modern of the Altingioideae also varies. The smallest infructes- plane tree. cences reaching up to 7 mm are found in Turonian Microaltingia Zhou, Crepet et Nixon (Zhou et al., Capitate inflorescences and infructescences are usu- 2001). The infructescence of Miocene Liquidambar ally very dense, making difficult if ever possible the changii Pigg, Ickert-Bond et Wen is about 25 mm in determination of the number of flowers in the head. diameter (Pigg et al., 2004). Heads of modern species Thus, heads of the modern plane tree are very dense, of Liquidambar reach 30 mm in diameter. flowers are tightly adpressed to each other, and margins between individual flowers are virtually indistinguish- Sarbaicarpa gen. nov. resembles members of the able. Fossil platanaceous genera with a developed peri- Altingioideae (Hamamelidaceae) by the number of anth, e.g., Platananthus or Friisicarpus, show distinct fruits in the infructescence (up to 30). Thus, up to margins between flowers, nonetheless, the heads are 25 flowers are known in modern Altingia Nor. and 26Ð40 in dense. The main type of hamamelidaceous inflores- Liquidambar (Bogle, 1986; Ickert-Bond et al., 2005). cences is a spike or a compound spike (Endress, 1977). Miocene L. changii has approximately 25Ð30 fruits. Racemes or compound and variously shortened Speaking about fossil members of the Platanaceae, the racemes are known in some genera. Inflorescences of genera Sarbaya Krassilov et Shilin (Krassilov and Shi- some members of the Hamamelidoideae and Exbuck- lin, 1995) and Archaranthus N. Maslova et Kodrul landioideae are shortened in such a degree that they (Maslova and Kodrul, 2003) have a smaller number of look as heads. Thus, Exbucklandia R. Brown has dis- flowers in inflorescences (about 24 and 15, correspond- tinctly developed capitate inflorescences (Kaul and ingly). As a rule, platanaceous heads consists of a Kapil, 1974). Capitate inflorescences are also known in

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300 μm 300 μm 300 μm ‡ b c

300 μm 300 μm d e

Fig. 2. Sarbaicarpa shilinii N. Maslova, western Kazakhstan, Sarbai locality, Zhirkindekskaya Formation, CenomanianÐTuronian: (a) holotype PIN, no. 1/5266, fragments of two fruits, remnants of elongated sterile structures are visible at the base; (b, c) holotype PIN, no. 1/5266, fruits; (d) holotype 1/5266, hairs adpressed to the fruit surface; (e) PIN, no. 2/5266, free hair. three modern genera of the Altigioideae: Altingia, Liq- 2007). The architecture and density of infructescences uidambar, and Semiliquidambar Chang (Bogle, 1986). and the shape of fruits make Sarbaicarpa gen. nov. Pistillate inflorescences and infructescences of modern close to Liquidambar acalycina. members of the Platanaceae and Altingioideae (Hamamel- idaceae) are remarkably different by their general mor- The recently described Bogutchanthus N. Maslova, phology. However, such structures can be virtually identi- Kodrul et Tekleva (Maslova et al., 2007), which shows cal in fossil state. The spectrum of their morphological a peculiar combination of platanaceous and hamameli- variations can only be deduced from the anatomy. daceous characters, is also characterized by flowers loosely situated in the head. Infructescences of modern Liquidambar vary in density dependent on the fusion between carpels. The Perianth. Perianth is lacking in Sarbaicarpa gen. majority of species have cuneate or fusiform fruits with nov. Mature fruits of Sarbaicarpa gen. nov. show no two locules. The fruits are more or less fused basally fragments of perianth elements which could have testi- and free distally. However, fruits of L. acalycina Chang fied to the presence of a perianth at earlier stages of the and the related genus Altingia are relatively loosely sit- flower development and their later disappearance. uated, do not fuse with each other and disintegrate Apparently, the flower of Sarbaicarpa gen. nov. was under mechanical pressure (Ickert-Bond et al., 2005, originally naked.

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30 μm 30 μm ‡ b

30 μm 10 μm c d

30 μm 10 μm e f

Fig. 3. Sarbaicarpa shilinii N. Maslova, western Kazakhstan, Sarbai locality, Zhirkindekskaya Formation, CenomanianÐTuronian, holotype, no. 1/5266, SEM: (a) transversely striate cuticle of the fruit; (b, d) epidermal cells of the fruit; (c) cells constituting fruit wall; (e) fragment of the external wall of the fruit, note a gland (arrow); (f) gland on the fruit surface.

The modern plane tree also has a naked flower Among modern Hamamelidaceae, members of the according to the opinion of some scientists. Contrari- Altingioideae are characterized by naked flowers, which wise, the majority of fossil members of the Platanaceae lack perianth elements even at early ontogenetic stages had well-developed and often differentiated perianths (Wisniewski and Bogle, 1982). Many genera of other sub- (Friisicarpus, Macginicarpa, Platananthus, Quadri- families of the Hamamelidaceae also have naked flowers. platanus, Hamatia Pedersen, Friis, Crane et Drinnan, Thus, within the Hamamelidoideae, Distylium Sieb. et Tanyoplatanus Manchester, and Archaranthus). Zucc. lacks a perianth, and Sycopsis dunnei Hemsl. and

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Parrotiopsis Schneider have a highly reduced perianth Recently published Turonian Kasicarpa has a (Bogle, 1970). Within the Exbucklandioideae, naked flow- monomeric gynoecium and is characterized by a mix- ers characterize Chunia Chang, and a calyx is only present ture of platanaceous and hamamelidaceous characters, in flowers of Exbucklandia at early ontogenetic stages namely, those of the subfamilies Altingioideae and (Bogle, 1986). Hamamelidoideae (Maslova et al., 2005). Other distinguishing features of this genus are a developed differ- Most of known fossil flowers of the Hamameli- entiated perianth, orthotropic seed, and the platana- daceae have well-developed perianths. Lindacarpa N. ceous morphology of the spermoderm. Maslova of the Altingioideae has a perianth that is attached slightly above the base of the gynoecium and It should be noted that although modern members of embraces the flower along a nearly entire length the Proteales also have a monomeric gynoecium, other (Maslova and Golovneva, 2000a). In Anadyricarpa, floral characters of the Proteales differ from those of perianth elements form a floral tube, which persists in Sarbaicarpa gen. nov. mature fruits (Maslova and Herman, 2004). Variously The fruit of Sarbaicarpa gen. nov. is broadly developed perianths are found in ancient Hamameli- cuneate with a conical base. Such a shape is described doideae, such as Allonia Magallón-Puebla, Herendeen in fruits of Coniacian Lindacarpa (Altingioideae). The et Endress (Magallón-Puebla et al., 1996), Archamame- new genus resembles modern Liquidambar acalycina lis Endress et Friis (Endress and Friis, 1991), and by the general outlines of the fruit. Carpels of this spe- Androdecidua Magallón-Puebla, Herendeen et Crane cies are similar to those of Late Turonian Microaltingia (Magallón-Puebla et al., 2001). of the Altingioideae (Zhou et al., 2001) and Miocene Liquidambar changii (Pigg et al., 2004). Gynoecium. Modern Platanus is characterized by an apocarpous gynoecium of unstable number of ele- Rare peltate glands were observed on the fruit wall ments (fiveÐeight or, more rarely, threeÐnine carpels) of Sarbaicarpa gen. nov. Similar, but more numerous, arranged in two or three circles and supplied with rela- structures are present on the surface of stamen thecae tively long stylodes. Extinct members of the Platan- and carpels of Quadriplatanus georgianus Magallón- aceae are characterized by a constant number of carpels Puebla, Herendeen et Crane (Platanaceae) from the in the flower. Friisicarpus and Macginicarpa had five ConiacianÐSantonian of southeastern North America carpels per flower, and Quadriplatanus, Sarbaya, and (Magallón-Puebla et al., 1997). Archaranthus had strictly tetramerous flowers. Mono- A bunch of hairs is present at the base of the fruit of meric gynoecium, a characteristic feature of Sar- Sarbaicarpa gen. nov., but it is difficult to judge about baicarpa gen. nov., is unknown in modern and fossil their length, because the hairs are too fragile. The hairs Platanaceae. are only situated at the base of the fruit; the rest of the fruit surface lacks hairs. Such bunches of hairs, A syncarpous half-inferior ovary of two carpels is although developed in a greater degree, are known in one of the key characters of the Hamamelidaceae. This the modern plane tree as an anemochorous adaptation. character dominates in the Hamamelidoideae, Exbuck- Different species of Platanus show variously developed landioideae, Rhodoleioideae, and Altingioideae. How- bunches of hairs. Thus, P. occidentalis L. has numerous ever, unstable number of carpels is known in some gen- hairs reaching the half of the fruit length, and the sur- era of the Hamamelidaceae. For instance, Exbucklan- face of the fruit is also covered with shorter hairs. dia of the Exbucklandioideae has one to five carpels, P. kerrii Gagnep. has naked fruits and rare hairs at the with a dominating bicarpellate gynoecium (Kaul and fruit base nearly reaching the fruit apex (Takhtajan, Kapil, 1974). One to three carpels are present in flowers 1991). of Parrotiopsis of the Hamamelidoideae (Kapil and Kaul, 1972). Monocarpellate gynoecia are found Seed. The fruit of Sarbaicarpa gen. nov. contains a among dominating bicarpellate gynoecia in Altingia solitary anatropic seed, which tightly fits to the walls and Liquidambar (Wisniewski and Bogle, 1982; Bogle, and occupies virtually entire volume. Among the Pla- 1986). A monocarpellate gynoecium only occurs in tanaceae, fruits of modern Platanus (Boothroyol, 1930; some genera of modern Hamamelidaceae and never Cronquist, 1981) and fossil Macginicarpa and Friisi- prevails. However, the Late AlbianÐEarly Cenomanian carpus (Manchester, 1986; Friis et al., 1988; Crane et genus Anadyricarpa (Altingioideae) is exclusively al, 1993) also have a solitary, but orthotropic seed. The characterized by a monocarpellate gynoecium. This only exception is Quadriplatanus georgianus, which character as well as the shape and size of the infructes- has non-orthotropic ovules (Magallón-Puebla et al., cences and the number of fruits per head make this 1997). Unfortunately, the insufficiently preserved genus closer to Sarbaicarpa gen. nov. On the other material did not allow a detailed description of the seed hand, Anadyricarpa has a perianth that nearly com- morphology. It was only reliably found that the seed pletely embraces the gynoecium resulting in a floral has a narrow median bar resembling a narrow wing, and tube, which persists in mature fruits; its fruit is nar- no micropyle was found in the area opposite to the rowly elliptical unlike the broadly cuneate fruit of Sar- point of the seed attachment. baicarpa gen. nov. In addition, no sterile structures are Anatropic seeds characterize of all members of the found in heads of Anadyricarpa. Hamamelidaceae, which are significantly variable by

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100 μm 100 μm ‡ b

30 μm 100 μm c d

100 μm 30 μm e f

30 μm 10 μm g h

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Fig. 4. Sarbaicarpa shilinii N. Maslova, western Kazakhstan, Sarbai locality, Zhirkindekskaya Formation, CenomanianÐTuronian, holotype PIN, no. 1/5266, SEM: (a, b, d) fruit with a solitary seed; (c) transverse section of fruit wall and seed; (e) seed fragment; (f) spermoderm section, note remnants of the anticlinal walls of polygonal cells of the external spermoderm layer and layer of small palisade sclerenchyma cells; (g) inner layer of the spermoderm, formed by cells with undulate anticlinal walls; (h) longitudinal section of the spermoderm showing cells of three layers. the number of ovules per ovary. All members of the The similarity between Sarbaicarpa gen. nov. and Hamamelidoideae have one ovule in the ovary. Genera members of the Altingioideae and Platanaceae also of other subfamilies have 5Ð8 (Disanthus Maxim., includes the morphology of the mechanical layer, com- Exbucklandia, Mytilaria Lecomte, and Chunia), 10Ð20 posed of relatively small thick-walled palisade sclere- (Rhodoleia Champ. ex Hook), 20Ð30 (Liquidambar), ids, nearly lacking cellular content. Similarly to mem- and 28Ð47 (Altingia) ovules (Endress, 1989a). Sar- bers of the Altingioideae and Platanaceae, the number baicarpa gen. nov. is comparable with members of the of cellular layers in Sarbaicarpa gen. nov. varies from Hamamelidoideae by the number of ovules (one) and one to three. The Hamamelidoideae differs by a thicker seed type (anatropic). mechanical tissue, with a greater number of cellular Anatropic seeds of modern Altingioideae bear more layers and variable structure of sclereids (Takhtajan, or less developed rounded or distal wings, whereas the 1991). Melikian (1973a, 1973b) concluded that the thin majority of hamamelidaceous genera have ballistic seed wall in Liquidambar and Altingia is more special- wingless seeds (Tiffney, 1986). Wings in Altingioideae ized in comparison to relatively thick walls in other vary from a large distal wing in Liquidambar formo- members of the Hamamelidaceae s.s., which are con- sana Hense and L. styraciflua L. to a shorter wing in L. sidered more primitive according to many other bota- orientalis. L. acalycina has a small rounded or triangu- nists. lar wing, resembling that in Altingia and Semiliquidam- Sarbaicarpa gen. nov. has a relatively thick bar. The seed of Miocene Liquidambar changii has a endosperm, which makes the new genus similar to rounded wing (Pigg et al., 2004); and the seed of Late members of the Hamamelidoideae. Unlike the Hama- Turonian Microaltingia lacks a developed wing, but has melidoideae, the endosperm in the Altingioideae is very a distinct ring rib (Zhou et al., 2001). The seed of Sar- scanty. In modern species of Platanus, the endosperm baicarpa gen. nov. lacks such structures. is nearly completely digested by a growing embryo and The morphology of the spermoderm of Sarbaicarpa is represented by a thin layer at the periphery of the gen. nov. is similar to that of modern Altingioideae. The mature seed (Poddubnaya-Arnol’di, 1982). spermoderm of the new genus is relatively thin, formed Sterile elements. Two types of sterile structures are by a few layers, and well differentiated. The seed sur- known: phyllomes and staminodes. Staminodes are face of Sarbaicarpa gen. nov. resembles that of modern reduced stamens, able (to a greater or lesser extent) to Liquidambar acalycina (Ickert-Bond et al., 2005). produce sterile pollen. Phyllomes are sterile structures These authors noted that in species of Liquidambar in pistillate flowers, different from staminodes. Their cells of the seed surface are nearly isodiametric. Sar- functions are still a matter of discussion. Sterile struc- baicarpa gen. nov. has epidermal cells diminishing tures in reproductive organs of modern and especially from the medial area toward the periphery of the seed. fossil plants are difficult to interpret. Thus, Tong (1930)

300 μm 200 μm ‡ b

Fig. 5. Sarbaicarpa shilinii N. Maslova, western Kazakhstan, Sarbai locality, Zhirkindekskaya Formation, CenomanianÐTuronian (a) and modern Liquidambar formosana L. (b), SEM: (a) holotype PIN, no. 1/5266; (b) collection of N. Maslova.

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30 μm 10 μm c d

3 μm 30 μm e f

30 μm 30 μm 10 μm g h i

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Fig. 6. Sarbaicarpa shilinii N. Maslova, western Kazakhstan, Sarbai locality, Zhirkindekskaya Formation, CenomanianÐTuronian, holotype PIN, no. 1/5266, SEM: (a) anatropic seed after maceration; (b) cells of the seed surface showing cuticle striation, perpen- dicular to the longer axis of the cells; (c) fragment of seed surface; (d) remnants of the anticlinal walls of a trapezoid cell of the external layer of the spermoderm, thick-walled sclerenchyma cells of the second layer of the spermoderm are visible in plan; (e) thick-walled sclerenchyma cells of the second layer of the spermoderm; (f, g) longitudinal section of the seed in the area of the suture, note an entire sclerenchyma layer; (h) endosperm; (i) endosperm cells. believed that there are no crucial differences between Bogle (1982) showed that these structures appear later staminodes and phyllomes and considered them as one than stamens and carpels during ontogenesis. The func- type of sterile structures in the flower. tion of phyllomes is still unclear, though, for example, Sterile structures vary in size, shape, and position they are glandular in Rhodoleia (Bogle, 1987). within the flower (intrafloral) or outside it (extrafloral). Sarbaicarpa gen. nov. is characterized by two mor- As far as such structures are very small and occur in phologically different types of extrafloral sterile struc- small and dense inflorescences, the study of their mor- tures. The former type includes relatively large ele- phology and typology is complicated. Thus, Croizat ments, which are comparable in size with the fruits and (1947) believed that phyllomes were situated at the consist of a small peduncle and a massive and slightly periphery of the flower and came directly from the oblate semispherical part. They are irregularly distrib- receptacle. Later, it was shown that these structures are uted within the infructescence. They are less numerous supplied with the same conductive bundles as stamens than needle-shaped sterile structures: about eight per and carpels, and there are no proofs of the extrafloral infructescence. From eight to twelve extrafloral phyl- nature of phyllomes (Bogle, 1986). lomes occur in modern species of Liquidambar; they The position of sterile elements is not always reli- are uniform within a species and vary in shape and size ably determinable, and their homologation is not among the species (Ickert-Bond et al., 2005). Such always unequivocal, that is particularly true in case of large sterile structures are unknown in modern and fos- fossil material. When phyllomes are situated between sil members of the Platanaceae and Hamamelidaceae. the stamen circle and ovary, one can suppose that they Flowers of Late Turonian Microaltingia (Altingio- are rudiments of these floral elements (Vink, 1957). ideae) have two or three circles of fleshy rounded phyl- Some authors believe that they are elements of the lomes, situated concentrically at the margin of the calyx (Clarke, 1858; Hooker and Thomson, 1858; hypanthium and bearing stomata. They are slightly Oliver, 1867), underdeveloped styles in sterile flowers similar in shape to sterile structures of the second type occurring among normal flowers (Harms, 1930), stami- of Sarbaicarpa gen. nov., but much smaller in absolute nodes (Tong, 1930), papillae (Schmitt, 1965), or necta- sizes as well as comparing to the length of the carpel. ries (Leeuwen, 1938). The surface of the semispherical sterile structures of Krassilov (1989) believed that intrafloral phyllomes Sarbaicarpa gen. nov. is covered with numerous were originally sterile and their similarity to elements rounded trichomes, which leave distinct rounded bases of perianth, stamens, and carpels was derived, as well after shedding. Distinct cuticular thickenings around as functions acquired in relation to insect pollination. the trichome aperture are visible on the inner surface of Extrafloral phyllomes were interpreted as bracts the cuticle of these structures. Similarly, leaves of mod- supporting flowers (Guillaumin, 1920), bracteoles or ern Platanus have rounded bases of trichomes on the modified leaves associating with inflorescences (Gif- adaxial surface, which have apertures on the inner sur- ford and Foster, 1989), or groups of undeveloped flow- face of the cuticle, armored with additionally deposited ers (Ickert-Bond et al., 2005). cutin (Carpenter et al., 2005). Cuticular formations sur- rounding stomatal apertures are also detected on the inner Extrafloral phyllomes are known in modern mem- surface of the leaf cuticle of modern Liquidambar. bers of several hamamelidaceous subfamilies, such as Altingia and Liquidambar of the Altingioideae, Extrafloral structures of the first type in Sarbaicarpa Exbucklandia of the Exbucklandioideae, and Rhod- gen. nov. most probably attracted insect-pollinators. It oleia of the Rhodoleioideae, as well as in Platanus. is not excluded that these structured could have pro- They vary in size and shape; the latter character is spe- duced nectar, and numerous gland trichomes probably cific of some species. Thus, needle-shaped phyllomes had a secretory function. Nectar production is unknown are known in Liquidambar formosana and L. acaly- in modern Platanus and fossil Platanaceae. Several cina; wider and cone-shaped, in L. styraciflua; and fused scales situated between the androecium and wide and slightly emerging, in L. orientalis. Smaller gynoecium produce nectar in some hamamelidaceous verrucate structures were found in the same position in genera: Loropetalum R. Brown ex Reich., Tetrathirium Altingia (Ickert-Bond et al., 2005, 2007). According to Benth., Maingaya Oliv., Corylopsis Sieb. et Zucc., For- Bogle (1986), phyllomes in some species of Liquidam- tunearia Rehd. et Wils., and Rhodoleia (Endress, bar are superficially similar to abortive pistils, but no 1967). In Hamamelis, staminodes produce nectar receptacle-resembling structures or indices of ovule (Endress, 1967). Nectaries are situated at the base of formation were detected. Moreover, Wisniewski and petals in Disanthus (Mizushima, 1968; Endress, 1989).

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300 μm 300 μm ‡ b

100 μm 100 μm c d

30 μm 30 μm e f

Fig. 7. Sarbaicarpa shilinii N. Maslova, western Kazakhstan, Sarbai locality, Zhirkindekskaya Formation, CenomanianÐTuronian, SEM: (a) PIN, no. 2/5266; (bÐf) holotype PIN, no. 1/5266; (a) fragmentary head, note fruits and a semispherical sterile structure (arrow); (b) semispherical sterile structure after maceration; (c) peduncle of a semispherical sterile structure; (d, e) surface of a semispherical sterile structure before (d) and after (e) maceration; (f) inner surface of the cuticle, note cuticular thickenings.

Nectar disks of Exbucklandia are occasionally errone- morphology and the moment of appearance during the ously interpreted as a calyx (Endress, 1989a). There is ontogenesis; however, there are no data about their a hypothesis that sterile structures of Liquidambar secretory activity or histology (Wisniewski and Bogle, styraciﬂua can be glands or nectaries judging from their 1982).

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300 μm 100 μm ‡ b

30 μm 30 μm c d

Fig. 8. Sarbaicarpa shilinii N. Maslova, western Kazakhstan, Sarbai locality, Zhirkindekskaya Formation, CenomanianÐTuronian, holotype PIN, no. 1/5266, SEM: (a, b) fruit and two linear sterile structures; (c) linear sterile structure, note transversely striated cuticle; (d) epidermal cells of a linear sterile structure, inside view.

Extrafloral sterile structures of Sarbaicarpa gen. tures occurred in one infructescence. These structures nov. of the second type are narrow, parallel-margined, resemble the fruits by the degree of cutinization: both needle-shaped elements, reaching at least a half of the are relatively strongly cutinized, the cuticles are striate, fruit length. Since fruits were relatively loosely situated but the fruit cuticle is transversely striate, and the cuti- in the infructescences of Sarbaicarpa gen. nov. and the cle of the needle-shaped sterile structures is longitudi- needle-shaped structures were very fragile, their apices nally striate. It is difficult to hypothesize about the func- were broken during fossilization. It is difficult to tion of these structures, particularly because no apices deduce whether the apices differed from the basal parts are preserved. It is unlikely that they were staminodes, and showed a more elaborated morphology. No regular- since no pollen grains were found either on them or ity was detected in the arrangement of these structures. other elements of the infructescence. The idea that they They were situated chaotically among the fruits, occa- could have been perianth elements is contradicted by sionally, in pairs (Fig. 8a); in total, about 15 such struc- the fact that they are irregularly situated among fruits.

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Their shape is similar to that of needle-shaped extraflo- the assignment of Cretaceous leaf remains superficially ral phyllomes in Liquidambar formosana and L. acaly- resembling leaves of the modern plane tree to the genus cina; however, they are much longer than phyllomes in Platanus is unjustified. modern species of Liquidambar and differ by strongly cutinized striate surfaces. There is a possibility that they are comparable with bracts, supporting inflores- CONCLUSIONS cences in some members of the Hamamelidaceae and 1. Infructescences of the new genus Sarbaicarpa attracting insects by their bright coloring (e.g., Parroti- gen. nov. combine platanaceous and hamamelidaceous opsis, Kapil and Kaul, 1972); however, it cannot be said characters. Characters shared by the two families with confidence because of their irregular distribution. include the shape of the compound inflorescence (Pla- Sterile structures in fossil flowers have been tanaceae/Altingioideae and some members of the extremely rarely recorded. Maslova and Krassilov Exbucklandioideae), no perianth (modern Plata- (1997) found two types of such structures differing in nus/Altingioideae, some members of the Hamameli- size and shape in Evacarpa N. Maslova et Krassilov doideae and Exbucklandioideae), a solitary seed in the (Altingioideae). The smaller and narrower structures fruit (Platanaceae/Hamamelidoideae), similar architec- were interpreted as phyllomes, and larger and wider ture of the spermoderm (modern Platanus/modern structures were interpreted as staminodes, which appar- members of the Altingioideae), and sterile structures in ently produced no pollen. Viltyngia N. Maslova, a infructescences (modern Platanus/Altingioideae, genus combining characters of the hamamelidaceous Rhodoleioideae, and some members of the Exbucklan- subfamilies Exbucklandioideae, Hamamelidoideae, dioideae). and Altingioideae, probably had staminodes which pro- The characters only ascribed to the Hamameli- duced a considerable amount of pollen (Maslova and daceae and found in Sarbaicarpa gen. nov. are a mono- Golovneva, 2000b). Aggregations of stuck underdevel- carpellate gynoecium, which occurs, though does not oped pollen grains, which are much smaller than fertile dominate in some members of the Altingioideae and the pollen, were found on the surface of the gynoecium. Hamamelidoideae, an anatropic seed, which is present Staminodes are known in SantonianÐCampanian in all members of the Hamamelidaceae, and a devel- Archamamelis of the Hamamelidoideae (Endress and oped endosperm, which is a character of the Hamameli- Friis, 1991) and in Eocene staminate heads related with doideae. The presence of a hair bunch at the fruit base Hamamelis and Corylopsis by several characters is only known in the Platanaceae (modern Platanus and (Manchester, 1994). Heads from the Turonian Raritan some fossil members of the family). Formation of New Jersey, which show both platana- 2. Sarbaicarpa gen. nov. is distinctive by a combi- ceous and hamamelidaceous characters, contained in nation of characters more or less characteristic of the their staminate flowers normal stamens and staminodes four subfamilies of the Hamamelidaceae: the Altingio- bearing nectary glands (Crepet et al., 1992; Crepet et ideae, Hamamelidoideae, Exbucklandioideae, and al., 1996). Staminodes in staminate flowers of Bogutch- Rhodoleioideae. The new genus resembles the Altin- anthus resembled mature stamens in shape and were gioideae by such characters as the shape of the capitate situated between mature stamens and perianth ele- infructescence, no perianth, a monocarpellate gyno- ments, probably partially fusing to their bases (Maslova ecium (it rarely occurs in modern members of the Alt- et al., 2007). ingioideae), micromorphology of the seed surface, Associating staminate inflorescences and leaves. spermoderm morphology, and sterile structures in the infructescence. The common features with members of Staminate heads of Sarbaya of the Platanaceae were the Hamamelidoideae are the absence of the perianth earlier described from the same deposits (Krassilov and (in some members, such as Distylium, Sycopsis dunnei, Shilin, 1995). They are characterized by tetramerous and Parrotiopsis), a monocarpellate gynoecium flowers without a perianth and tricolporate pollen (occurs in Parrotiopsis), a solitary seed in the fruit, and grains. a developed endosperm. Sarbaicarpa gen. nov. is simi- Lobate leaves earlier assigned to Platanus lar to Exbucklandia and Chunia (Exbucklandioideae) pseudoquillelmae Krass. and P. cuneiformis Krass. by capitate infructescences, naked flowers, a monocar- (Shilin, 1986) were found associating with the pellate gynoecium, and sterile elements in the infructescence of Sarbaicarpa gen. nov. Among typi- infructescence. Sarbaicarpa gen. nov. resembles the cally Platanus-like characters, these leaves show some Rhodoleioideae by the total absence of the perianth (or peculiarities that make them closer to members of the weak development in some species of Rhodoleia) and Altingioideae. In particular, these are repeated interca- the presence of sterile structures. To conclude, the find lary veins that are situated between secondary veins of the CenomanianÐTuronian infructescence of Sar- and reach approximately a half of the distance to the baicarpa gen. nov. confirms the earlier expressed leaf margin and well-developed marginal glands. hypothesis (Maslova and Golovneva, 2000; Maslova, Krassilov and Shilin (1995) showed that the epidermal 2003) about the close relationships between the Altin- morphology of these leaves shows characters of the gioideae and other subfamilies of the Hamamelidaceae, Fagaceae. Maslova et al. (2005) already discussed that and, particularly, the Hamamelidoideae and Exbuck-

PALEONTOLOGICAL JOURNAL Vol. 43 No. 10 2009 NEW GENUS SARBAICARPA GEN. NOV. (HAMAMELIDALES) 1295 landioideae and supports the supergeneric system of the 6. R. J. Carpenter, R. S. Hill, and G. J. Jordan, “Leaf Cutic- Hamamelidaceae, proposed by Endress (1989a, ular Morphology Links Platanaceae and Proteaceae,” 1989b). Int. J. Plant Sci. 166, 843Ð855 (2005). 3. The mosaic combination of morphological and 7. B. Clarke, “On the Structure and Affinities of Myri- anatomical characters in the CenomanianÐTuronian caceae, Platanaceae, Altingiaceae, and Chloranthaceae,” infructescence Sarbaicarpa gen. nov. and the associa- Ann. Mag. Nat. Hist., Ser. 3 1, 100Ð113 (1858). tion between these reproductive structure and leaves 8. Comparative Seed Anatomy, Vol. 3: Dicotyledons, showing the typical morphology of the modern plane CaryophyllidaeÐDilleniidae, Ed. by A. L. Takhtajan tree and some altingioid characters confirm the earlier (Nauka, Leningrad, 1991) [in Russian]. expressed opinion about the close relationships 9. P. R. Crane, S. R. Manchester, and D. L. Dilcher, “Mor- between the Platanaceae and Hamamelidaceae. Earlier, phology and Phylogenetic Significance of the a body of paleobotanical evidence was amassed in Angiosperm Platanites hybridicus from the Palaeocene favor of relationships between the Platanaceae and of Scotland,” Palaeontology 31, 503Ð517 (1988). Hamamelidaceae (Crepet et al., 1992; Crepet and 10. P. R. Crane, K. R. Pedersen, E. M. Friis, and A. N. Drin- Nixon, 1996; Maslova and Herman, 2004; Maslova et al., nan, “Early Cretaceous (Early to Middle Albian) Pla- 2005, 2007). tanoid Inflorescences Associated with Sapindopsis Leaves from the Potomac Group of Eastern North Amer- 4. Paleobotanical studies have shown a considerable ica,” Syst. Bot. 18 (2), 328Ð324 (1993). heterogeneity of Cretaceous platanoids, which include 11. W. L. Crepet and K. Nixon, “The Fossil History of Sta- more than one family. The taxonomic solution for these mens,” in (eds) The Anther: Form, Function, and Phy- fossil finds apparently demands a completely new logeny, Ed. by G. D’Arcy and R. C. Keating (UP, Cam- approach: their classification within extinct families, in bridge, 1996), pp. 25Ð57. various degrees related to the modern family Platan- 12. W. L. Crepet, K. C. Nixon, E. M. Friis, and J. V. Freuden- aceae. This approach contradicts the existing opinion stein, “Oldest Fossil Flowers of Hamamelidaceous about the wide occurrence of the modern families Pla- Affinity, from the Late Cretaceous of New Jersey,” Proc. tanaceae and Hamamelidaceae in the Cretaceous. Natl. Acad. Sci. USA 89, 8986Ð8989 (1992). 13. L. Croizat, “Trochodendron, Tetracentron, and Their ACKNOWLEDGMENTS Meaning in Phylogeny,” Bull. Torrey Bot. Club. 74, 60Ð 76 (1947). I am grateful to V.P. Shilin (Almaty, Kazakhstan) for 14. A. Cronquist, An Integrated System of Classification of providing the fossil material for this study and to Prof. Flowering Plants (Columbia Univ. Press, New York, V.A. Krassilov (PIN, Moscow, Russia; Institute of Evo- 1981). lution, Haifa, Israel) for valuable discussion of the 15. P. K. Endress, “Systematische Studien über die ver- obtained results. wantschaftlichen Beziehungen zwischen den Hamamel- The study was financially supported by the Russian idaceen und Betulaceen,” Bot. Jahrb. 87, 431Ð525 Foundation for Basic Research, project no. 07-04- (1967). 00687, PalSIRP Sepkoski Grant RUG1-1648-XX-06 16. P. K. Endress, “Evolutionary Trends in the Hamamel- (Mod 01), and Systematic Research Funding of the idalesÐFagales Group,” Pl. Syst. Evol., Supplement 1, Linnaean Society. 321Ð347 (1977). 17. P. K. Endress, “Aspects of Evolutionary Differentiation of the Hamamelidaceae and the Lower Hamamelididae,” REFERENCES Pl. Syst. Evol. 162, 193Ð211 (1989a). 1. “Angiosperm Phylogeny Group 2003. 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