FOSSIL FLOWERS OF ERICALEAN AFFINITY FROM THE LATE CRETACEOUS OF SOUTHERN SWEDEN 1

Transcription

1 American Journal of Botany 88(3): FOSSIL FLOWERS OF ERICALEAN AFFINITY FROM THE LATE CRETACEOUS OF SOUTHERN SWEDEN 1 JÜRG SCHÖNENBERGER 2 AND ELSE MARIE FRIIS Department of Palaeobotany, Swedish Museum of Natural History, Box 50007, SE Stockholm, Sweden Charcoalified fossil flowers of a new genus and species (Paradinandra suecica) with affinities to Ericales s.l. (sensu lato) are described from the Late Cretaceous (Santonian-Campanian) from Southern Sweden. The flowers are pentamerous, hypogynous, and actinomorphic. Aestivation of sepals and petals is imbricate-quincuncial. The androecium consists of an outer whorl with single episepalous stamens and an inner whorl with paired epipetalous stamens. Pollen is small and probably tricolpate. Three carpels form a syncarpous ovary with numerous campylotropous ovules on parietal placentae. The styles are free for most of their length. The structure of mature fruits and seeds is unknown. Clear distinction of sepals and petals, possible dehiscence of anthers by restricted slits, presence of a nectary, and the general floral construction (salverform corolla) with a canalized access to the floral center clearly indicate insect pollination of the fossil flowers. Comparisons with extant taxa demonstrate that Paradinandra suecica shares many similarities with Ericales s.l. and in particular with members of Ternstroemiaceae, Theaceae, and Actinidiaceae. However, it is neither identical to any one genus of these families nor to any of the previously described ericalean taxa from the Cretaceous and thus provides further evidence of the diversity of Cretaceous ericalean plants. Key words: Ericales s.l.; flowers; fossils; insect pollination; Late Cretaceous; Paradinandra suecica; Sweden; Ternstroemiaceae. During the last 20 yr our knowledge about angiosperm fossils from the Cretaceous has increased at a rapid rate (for a review see Crane, Friis, and Pedersen, 1995). By the Late Cretaceous, floral construction and architecture had reached an evolutionary level almost comparable to that of many recent angiosperms. This allows us in many cases to compare these fossils with living angiosperms and draw direct conclusions not only about their systematic relationships, but also about floral biology and pollination (e.g., Basinger and Dilcher, 1984; Crepet, Friis, and Nixon, 1991). The ongoing study of plant fossils from Late Cretaceous (Santonian-Campanian) deposits from Åsen in southern Sweden has revealed many extremely well-preserved fossil flowers, fruits, and seeds. Specimens belonging to the following major lineages of angiosperm evolution have so far been described: Chloranthaceae (Chloranthistemon Crane, Friis, and Pedersen, 1989; Eklund, Friis, and Pedersen, 1997), Proteales (Platananthus Friis, Crane, and Pedersen, 1988), Saxifragales (Archamamelis Endress and Friis, 1991), Fagales (Antiquocarya, Caryanthus, Manningia Friis, 1983), Hydrangeaceae (?) (Scandianthus Friis and Skarby, 1982), Ericales (Actinocalyx Friis, 1985a), and Escalloniaceae (?) (Silvianthemum Friis, 1990). The present study describes fossil floral structures including floral buds and flower fragments from the Åsen locality. Organization and construction of these flowers clearly indicate that they were insect pollinated. The specimens reflect a syndrome of features that supports a placement in the Ericales s.l. sensu APG (1998). Delimitation and systematic position of the Ericales sensu Cronquist (1981) have undergone many chang- 1 Manuscript received 7 December 1999; revision accepted 4 May The authors thank Stig Lindbom for collecting the fossil material; Anton Igersheim and Yvonne Arremo for technical assistance; Arne Anderberg, Alex Bernhard, Peter Crane, Michael Donoghue, Walter Judd, Peter K. Endress, Maria von Balthazar, and an anonymous reviewer for valuable comments on the manuscript. This work was supported by the Swedish Natural Science Research Council. 2 Author for reprint requests, current address: Institute of Systematic Botany, University of Zurich, Zollikerstrasse 107, CH-8008 Zurich, Switzerland ( jsberger@systbot.unizh.ch). 467 es lately. Not only are they now placed within the asterid clade, but they are also circumscribed in a broader sense including several taxa previously referred to different dilleniid orders (Kron, Chase, and Hills, 1991; Anderberg, 1992; Downie and Palmer, 1992; Hufford, 1992; Olmstead et al., 1992; Anderberg, 1993; Chase et al., 1993; Judd and Kron, 1993; Olmstead et al., 1993; Swensen and Chase, 1995; Morton et al., 1996; Soltis et al., 1997; Nandi, Chase, and Endress, 1998). Angiosperm fossils from the Tertiary are often so similar to modern groups that they can be placed in modern genera. Ericales s.l. have an extensive fossil record from that period of time (e.g., Collinson, 1978; Friis, 1985b; Manchester, 1994). Several ericalean taxa have also been reported from the Late Cretaceous, although the details of their relationships within the group are often less sure (Actinocalyx with sympetalous flowers Friis, 1985a; fruits and seeds of different ericalean affinities Knobloch and Mai, 1986; Paleoenkianthus with awned anthers Nixon and Crepet, 1993; stamens and flowers of possible ericalean affinities, not yet formally described Crepet and Nixon, 1996; Parasaurauia with free styles that emerge from an apical depression in the ovary Keller, Herendeen, and Crane, 1996; flowers and fruits of possible ericalean affinities, not yet formally described Herendeen et al., 1999; Takahashi, Crane, and Ando, 1999a). MATERIALS AND METHODS The fossils examined in this study were isolated from deposits of Late Santonian Early Campanian age exposed in the Ho ganäs AB kaolin quarry (now used as a garbage dump) at the Åsen locality in the Kristianstad Basin, Scania (56 9 N, E). The sediments consist of unconsolidated sands and clays, from which the plant fossils were extracted by sieving of bulk samples in water. More details on the site and standard preparation methods for the material are given in Friis, Crane, and Pedersen (1988). The material studied in this paper occurs in two samples (Åsen 2 and Åsen 3; collected by S. Lindbom). The fossils are charcoalified (fusanized), with their original three-dimensional form intact or rarely slightly compressed. A discussion of this type of preservation is given in Friis, Crane, and Pedersen (1988). The fossil material comprises a few more or less complete floral buds

2 468 AMERICAN JOURNAL OF BOTANY [Vol. 88 [S /S , S S , S106016, S , S107080; all specimens and preparations of fossil material are deposited in the collections of the Swedish Museum of Natural History (S)], a few ovaries with androecium and perianth sometimes partially preserved (S106021, S106022, S106253, S106254, S106256), as well as many abscised corolla tubes with adhering filaments and in few cases also with anthers attached (S S106014, S106378, S S107079). All the fossils are astonishingly small ( 3.5 mm in length). However, this is not only true for most other floral remains from the same locality (e.g., Friis and Skarby, 1981; Friis, 1984, 1985c), but it is also the case for most mesofossils from other Cretaceous deposits in Europe, North America, and central and eastern Asia (e.g., Nixon and Crepet, 1993; Friis, Pedersen, and Crane, 1994; Eklund and Kvaček, 1998; Frumin and Friis, 1999; Herendeen et al., 1999; Takahashi, Crane, and Ando, 1999a). In preparation for scanning electron microscopy (SEM) specimens were mounted on SEM stubs, sputter coated with Au, and then studied with a Phillips 515 scanning microscope. Two of the buds (S and S ) were carefully dissected with the help of fine needles and tweezers under a stereomicroscope. The different organs then were remounted (on separate stub S and stubs S S , respectively), sputter coated, and then studied in detail with scanning electron microscopy. Two of the buds (S , section slides S S ; S , section slides S S ) and two corolla tubes (S , section slides S S ; S , section slides S S ) were embedded in 2-hydroxyethyl methacrylate (Kulzer s Technovit 7100; Heraeus Kulzer GmbH, Philipp-Reis-Strasse 8/13, D Wehrheim/Ts., Germany) and cut at 3 6 m with a rotary microtome. This is a widely used routine method for anatomical and histological investigations of animal and plant tissues. For description of embedding method and products used see Igersheim (1993) and, in particular, Igersheim and Cichocki (1996), who describe embedding and sectioning of charcoal specimens in detail. Parts of the section series were drawn with a drawing tube. Shape, size, and arrangement of floral organs were reconstructed from the sections of the best-preserved bud, which is also the holotype (S ). RESULTS The following description of the flowers is mainly based on two of the floral buds (S , SEM, Fig. 4; S106194, SEM, Figs. 2, 3 and microtome sections). Both are extraordinarily well preserved and allow detailed study of morphology and anatomy. One of the buds (S106015) represents a slightly older pre-anthetic stage, which is indicated by its size and by the presence of immature pollen grains in the anthers. In the sectioned specimen no pollen grains were found. Floral organization and morphology The flowers are borne in the axils of subtending bracts. The peduncle is short and rather thick (Fig. 1). Four to six small, scale-like structures are present in the axils of the two imbricate bracteoles, which are at least half as long as the whole bud (Figs. 2, 3). The flowers are pentamerous and the organ whorls alternate. The flowers are hypogynous, actinomorphic, and bisexual. The buds are 3.5 mm long and 1.2 mm wide. Calyx The sepals are completely free from each other and were probably initiated in a spiral sequence. This is indicated by their different insertion levels on the floral axis (Fig. 38m) and a divergence angle of about 137 between subsequent organs, which results in a quincuncial-imbricate aestivation (two sepals overlap their neighbors, two are overlapped by their neighbors, and one is half-overlapped). The sepals are broadly lanceolate with obtuse apices (reconstruction from section series, Figs. 37, 38). Abaxially, the sepals have unicellular, simple trichomes up to 0.5 mm long (Figs. 2, 5) concentrated along a well-developed median vein, which is prominent in the upper third of the sepal (Fig. 7). Each sepal has four or six additional veins extending only along a part of the sepal s length (Fig. 37). The central area of each sepal, where the veins are found, is made up of several cell layers, whereas the lateral parts are very thin and membranaceous. The abaxial epidermis is slightly papillate (Figs. 6, 7). Corolla The corolla is thought to be sympetalous, but this cannot be demonstrated unequivocally neither from sections of buds (Fig. 37h, i) and abscised corolla tubes (Fig. 20), nor from specimens studied with the SEM (Figs. 18, 19). The sections indicate a short united zone at the very base of the corolla. Union of the petal bases is also suggested by the fact that abscised corollas are preserved as distinct tubular structures. However, for most of its length the corolla, which opens incompletely during anthesis, consists of free petal lobes. The petals are mitriform with their broadest part shortly below their middle (reconstructed from sectioned bud; Fig. 37). Petal aestivation in the bud is imbricate-quincuncial (Figs. 37, 38). Androecium All specimens studied have 15 stamens. The filaments are united at their very base and are probably fused to the base of the corolla (Figs. 8, 37i). Also in this case it is difficult to establish with certainty whether the organs are really united or whether they only adhere to each other. The stamens probably were initiated in two whorls as is indicated by their arrangement in the bud (Figs. 37, 38). The outer episepalous whorl consists of five stamens and the inner epipetalous whorl consists of ten paired (doubled) stamens. The filaments are massive at their base and taper towards the point at which the anther is attached (Figs. 8 10, 21). The anthers are basifixed and the joint between filament and connective is relatively thin (Figs. 15, 16). The anthers are dithecal, tetrasporangiate, and X-shaped, i.e., the two thecae are basally and apically separated (Figs. 11, 15 17, 23). The type of dehiscence is not completely clear as no well-preserved anthetic anthers were found. In pre-anthetic anthers a furrow that runs along nearly the whole length of the thecae is present (Fig. 12). However, enlarged epidermal cells, which are especially prominent at the distal ends of the thecae, may indicate dehiscence by restricted apical slits or pores (Figs. 12, 13). The anthers are stacked on three levels in the bud (reconstructed from section series). All the anthers are more or less of the same size, whereas the filaments differ markedly in length (Fig. 37). The five filaments of the outer stamen whorl are on average 0.75 mm long and the filaments are upright. One stamen of each stamen pair of the inner whorl has a slightly longer filament than its neighbor. The pattern is irregular, i.e., short and long stamens of this whorl do not always alternate. The five longer filaments are on average 0.55 mm long, and they are upright as well. The filaments of the five shorter stamens of the inner whorl are on average 0.45 mm long and thus only slightly shorter. However, the upper parts of these shortest filaments are bent outwards in the bud in a way that the anthers of these five stamens are positioned on an even lower level. This results in a stacking of the 15 anthers on three levels within the bud (Figs. 37, 38d h). Because no complete anthetic flowers were found, it is not possible to establish whether this difference in stamen length is retained during later development or whether it is simply a way of dense packing of the floral organs within the bud, which is

3 March 2001] SCHÖNENBERGER AND FRIIS LATE CRETACEOUS ERICALEAN FLOWERS 469 Figs Paradinandra suecica. Floral morphology and transverse section of sepal. 1. Pedunculate flower in axil of subtending bract. S Floral bud. Arrowhead indicates scale-like structures in axil of bracteole. S Same bud as in Fig. 2, from side. 4. Floral bud. Sepals partly broken off. S Part of sepal with unicellular trichomes. S Papillate epidermis of sepal. S Transverse section of sepal from bud in Figs. 2 and 3. Star indicates prominent median vein; arrowheads point to papillate epidermal cells. S Scale bars in Figs mm; in Figs. 5, m; in Fig m. Figure Abbreviations: B, bracteole; G, gynoecium; is, incomplete septum; L, locule; N, nectary; P, petal; S, sepal; sb, subtending bract. lost later in ontogeny. In abscised corolla tubes with attached filaments the filaments are normally broken off at different levels, which makes it difficult to recognize any pattern of anther placement. At least in some specimens there is evidence of some filaments being longer than others (Figs. 21, 22). Pollen Immature pollen grains were found within the anthers of one of the buds (Fig. 14). Mature pollen grains are present on many of the abscised corolla tubes. The pollen grains are similar in all specimens studied and are always restricted to the inside of the corolla tubes. Similar pollen has not been observed on other fossil remains from the same sample, and it is therefore most likely that pollen and corolla tubes correspond to the same flower. The pollen was studied using SEM only, and details of pollen ultrastructure and apertures are therefore not fully explored. The pollen is small (10 14 m in length) and probably tricolpate, with long colpi. The exine is finely foveolate (Figs ). Nectary A shallow nectary disc is present around the base of the ovary. It is emarginate as it slightly extends towards the narrow spaces between the filaments (Figs. 28, 31, 32, 37h, i). Gynoecium The gynoecium is tricarpellate and syncarpous (Figs. 28, 31). The three styles are elongate and slightly flattened (Figs. 28, 37c e). They are free over most of their length; only their very bases seem to be united (Fig. 36c). An inconspicuous ventral slit is present over the whole length of the styles (Fig. 30). The stigma, as seen in the bud, is small

4 470 AMERICAN JOURNAL OF BOTANY [Vol. 88 Figs Paradinandra suecica. Floral morphology and transverse sections of stamens. 8. Part of corolla tube with attached filaments, anthers broken off. S Part of corolla tube with adhering filaments. Note elongate filament. S Stamen with attached anther. S X- shaped anther, from abaxial side. S Anther from side with pore-like opening at apical end. S Close-up of apical end of theca showing enlarged cells along stomium. S Immature pollen in opened anther. S Transverse section of one of the five shorter epipetalous stamens at the level of the joint between anther and filament (arrowhead). Pollen sacs are collapsed. S Transverse section of episepalous stamen at the level of joint between anther and filament (arrowhead). Pollen sacs are collapsed. S Transverse section of epipetalous stamen at the level of the connective. Anther is tetrasporangiate and pollen sacs are collapsed. S Scale bars in Figs. 8, mm; in Figs , m; in Fig m.

5 March 2001] SCHÖNENBERGER AND FRIIS LATE CRETACEOUS ERICALEAN FLOWERS 471 Figs Paradinandra suecica. Floral morphology and transverse section of corolla tube. 18. Abscised corolla tube from side. S Base of abscised corolla tube. S Transverse section of corolla tube and filaments. S Apical view of corolla tube with attached filaments and anthers. S Apical view of corolla tube with attached filaments. Arrowhead indicates anther within tube. S Close-up of anther within corolla in Fig Tricolpate (?) pollen grains on adaxial surface of corolla tube. S Close-up of slightly foveolate pollen exine. S Scale bars in Figs mm; in Fig m; in Figs m; and in Fig m. and simple; no papillae were found (Fig. 29). At the top of the ovary three small, apically open cavities are present. They extend from the basal (united) part of the styles down into the incomplete septa between the apical ends of the locules (Figs. 33, 36a e). The dorsal vascular bundles of the carpels are prominent on the outside of the globose ovary (Fig. 31). The carpel margins fail to meet in the center over most of the length of the ovary. The ovary therefore is unilocular and the placentation is parietal (Figs. 32, 34, 37g). Numerous ovules are borne on the intruding margins of the carpels. The ovules are curved (campylotropous) and have a reticulate surface (Figs. 32, 34, 35). On some of the ovaries scattered unicellular trichomes are present. Structure of mature fruits and seeds is unknown. Floral construction The general shape of the flowers is salverform. They are tubular in the lower part and spreading distally (Fig. 18). The upper part consists of the free petal lobes. The access to the floral center and the nectary is canalized and further narrowed by the fleshy filaments (Figs. 8, 9, 21). DISCUSSION Systematic affinity and comparison with extant plants The combination of floral characters and the general appearance of the flowers are, on first sight, not clearly indicative of any extant angiosperm family. However, two of the characters, the stamen arrangement with a single episepalous stamen and

6 472 AMERICAN JOURNAL OF BOTANY [Vol. 88 Figs Paradinandra suecica. Floral morphology and transverse sections of gynoecium. 28. Gynoecium with three styles and nectary disc. S Immature stigma. S Part of style. Arrowheads point to ventral slit. S Apical view of gynoecium, styles broken off. S Opened ovary showing parietal placentation. Star indicates open space in center of ovary (same specimen as in Fig. 31). 33. Base of styles. Arrowhead points to cavity in apical part of ovary. S Lateral view of opened ovary with numerous ovules. Star indicates open space in center of ovary. 35. Campylotropous ovules with reticulate surface. S Schematic drawing and series of transverse sections showing cavities in apical part of ovary. Lines

7 March 2001] SCHÖNENBERGER AND FRIIS LATE CRETACEOUS ERICALEAN FLOWERS 473 epipetalous stamen pairs and the campylotropous ovules, are rather distinctive. A comparable stamen arrangement occurs in 20 eudicot families (Ronse Decraene and Smets, 1996), while campylotropy is found, predominantly or as an exception, in 65 families belonging to different orders of both monocots and dicots (Bouman and Boesewinkel, 1991). The combination of the two characters is, however, not very common among angiosperm families, but does occur in the Ericales s.l. Epipetalous stamen pairs are present in Ebenaceae, Sapotaceae, Styracaceae, and Ternstroemiaceae (Ronse Decraene and Smets, 1996). The same stamen arrangement as observed in the fossil flowers is also present as the basic androecial pattern in young flowers of Saurauia subspinosa in the Actinidiaceae (Brown, 1935). Campylotropous ovules occur in Diapensiaceae, Ericaceae, Myrsinaceae, Primulaceae, Theophrastaceae, and Ternstroemiaceae. Other floral characters such as the presence of two bracteoles, free or basally united petals, a compound ovary with almost completely free styles together with the general appearance of the flowers indicate a systematic position of the fossil flowers near the Theaceae, Ternstroemiaceae, and Actinidiaceae (Table 1). These three families were traditionally placed in the Theales within the subclass Dilleniidae (Cronquist, 1981). Recent molecular studies indicate that the Theales in this sense are not monophyletic (Swensen and Chase, 1995; Morton et al., 1996). Two of the theaceous subfamilies, Theoideae and Ternstroemioideae, fall into the Ericales s.l. and are raised to family level. They form two independent clades that are not sister taxa and are most closely related to the core Ericales (Morton et al., 1996). The Actinidiaceae are also referred to the Ericales s.l. in analyses of morphological and molecular data (Chase et al., 1993; Olmstead et al., 1993; Morton et al., 1997; Soltis et al., 1997; Nandi, Chase, and Endress, 1998) and are probably the basal clade of the core Ericales (Anderberg, 1992, 1993; Judd and Kron, 1993; Kron, 1996; Morton et al., 1996). Morphologically, the flowers of Theaceae, Ternstroemiaceae, and basal core Ericales, including the Actinidiaceae, share many similarities among each other (Judd et al., 1999) and with the fossil flowers. The Ternstroemiaceae have representatives with both epipetalous stamen pairs (Visnea Payer, 1857; Corner, 1946; Ronse Decraene and Smets, 1996) and campylotropous ovules (Keng, 1962; Tsou, 1995) and are of particular interest for comparison with the fossil material. Within Ternstroemiaceae two main subgroups are recognized (Melchior, 1925; Keng, 1962). They have been variously named, but, to avoid confusion, we simply refer to them here as the Ternstroemia group and the Adinandra group, respectively, based on their name-giving genus. Melchior (1925) separated the two groups based mainly on the arrangement of the perianth organs. In the Ternstroemia group sepals and petals are opposite, whereas in the Adinandra group they alternate. According to Keng (1962) species of the Ternstroemia group have filaments that are often much shorter than the anthers and have only two to few ovules per carpel, whereas in the Adinandra group filaments are often longer than anthers and there are numerous ovules per carpel. The fossil flower with its alternating sepals and petals, filaments longer than anthers, and numerous ovules per carpel, fits well in the Adinandra group (Table 1). Following Keng (1962), the Adinandra group consists of ten genera, of which four are monotypic. Among these is the genus Visnea, which also has epipetalous stamen pairs (Payer, 1857; Corner, 1946; Ronse Decraene and Smets, 1996) in a pattern similar to that of the fossil flowers. The genus Cleyera differs from other taxa of this group in having clearly parietal placentation (Keng, 1962) and anthers, which open by restricted apical slits (Melchior, 1925). These characters are also present in the fossil flowers. There are thus many important morphological similarities between the flowers of the Ternstroemiaceae (especially the Adinandra group) and the fossil flowers. However, there are also important differences: (1) The filaments of the fossil flowers are several times longer than the anthers, which contrasts with the condition in most Ternstroemiaceae, where filaments are only slightly longer or shorter than the anthers (Walter Judd, personal communication, University of Florida, Gainsville, Florida, USA). Regarding this feature the fossils are more similar to Actinidiaceae or Theaceae. (2) The pollen observed in the fossils is probably tricolpate, not tricolporate, as is the general condition in the Actinidiaceae, Theaceae, and Ternstroemiaceae (Erdtman, 1952; Cronquist, 1981). Ferguson and Davison (1986) reported tricolpate pollen in Actinidia deliciosa and Schmid (1978) described the pollen of Actinidia chinensis as tricolpate or possibly tricolporate with obscure germinal pores. Most other Ericales s.l. have tricolporate pollen, but there are a few families where tricolpate grains occur: Balsaminaceae, Lecythidaceae, and Primulaceae (Erdtman, 1952). (3) The presence of a disc-shaped, intrastaminal nectary distinguishes the fossil flowers from Ternstroemiaceae where nectaries have not been reported. In the Theaceae, either the base of the filaments or the base of the ovary is rarely nectariferous (Judd et al., 1999). Within Actinidiaceae, the corolla base of Saurauia subspinosa is nectariferous (Brown, 1935). In many other families of the Ericales s.l. intrastaminal nectary discs are common. The absence of a nectary in most extant Actinidiaceae, Theaceae, and Ternstroemiaceae may be a secondary feature induced by the evolution of their prevailingly polystaminate pollen flowers, in which pollen, and not nectar, is the reward for the pollinators. Vogel (1978) mentioned Theaceae as one of the families that still exhibits nectarogenous transitions to pollen flowers. (4) The salverform shape of the fossil flowers as observed in the abscised corolla tubes is another feature, which distinguishes the fossils from Actinidiaceae, Theaceae, and Ternstroemiaceae. The flowers of these families are often bowl shaped. Sepals, petals, and stamens are spreading at anthesis, and the floral center is open. In the fossil flowers access to the floral center (and the nectary) is canalized by the narrowed tubular part of the corolla and the thick fil- connecting Figs. 36b e indicate plane of schematic longitudinal section in Fig. 36a. Arrowheads indicate one of three cavities in apical part of ovary. (a) Schematic longitudinal section of gynoecium. Lines b e indicate approximate levels of transverse section in Figs. 36b e. (b) Uppermost transverse section. Styles free from each other; line. (c) Section through united styles with three cavities. (d) Section through top of ovary. Three cavities are visible. (e) Lowermost section through apical parts of locule (appearing three-loculed on top of ovary). Arrowhead indicates one of the cavities (the sections are not exactly transversal, therefore only one of the three cavities is present at this level) S /16. Scale bar in Fig mm; in Figs. 29, m; in Figs , m; and in Fig m.

8 474 AMERICAN JOURNAL OF BOTANY [Vol. 88 Fig. 37. Paradinandra suecica. Series of transverse sections (S S ) of floral bud (S ) and schematic diagram showing relative sizes and shapes of reconstructed floral organs, levels a i corresponding to figured sections a i. Scale bar 1 mm.

9 March 2001] SCHÖNENBERGER AND FRIIS LATE CRETACEOUS ERICALEAN FLOWERS 475 Fig. 38. Paradinandra suecica. Line drawings (a m) of transverse section series (S S ) of floral bud (S ) and floral diagram (n). Colors indicate different organs: gray bracteoles, green sepals, red petals, yellow episepalous stamens (light yellow filaments of episepalous stamens), lilac epipetalous stamens (light lilac filaments of epipetalous stamens), light blue nectary, blue gynoecium. Scale bar 1 mm.

10 476 AMERICAN JOURNAL OF BOTANY [Vol. 88 TABLE 1. Comparison of floral characters of Paradinandra suecica with extant taxa. a Character Paradinandra suecica Adinandra group sensu Keng (1962) Ternstroemiaceae Ternstroemia group sensu Keng (1962) Theaceae: Camellioideae, sensu Keng (1962) Actinidiaceae Size of flowers small generally small generally small generally large small to large Bracteoles two two or three two or three two to several two to several Sepals/petals alternate alternate opposite alternate alternate Petals basally united (?) distinct or often basally united basally united distinct or often basally united distinct or often basally united Stamens/corolla basally fused (?) basally fused partly basally fused partly basally fused separate or basally fused Filaments basally united distinct or basally distinct (?) often basally united often basally united united No. of stamens 15 ten to numerous numerous numerous ten to numerous Stamen arrangement two whorls, antepetalous stamen pairs one or more whorls, antepetalous stamen pairs in Visnea often two whorls two to six whorls often two whorls, often antepetalous clusters Filament/anther filament much longer filament slightly longer filament shorter than filament much longer filament much longer than anther than anther anther than anther than anther Anther attachment basifixed basifixed basifixed (?) (?) Anther dehiscence short, apical slits (?) longitudinal slits; Cleyera with short apical slits Pollen 10 to 14 m, exine slightly foveolate, tricolpate (?) usually less than 25 m, exine nearly smooth, tricolporate mostly versatile mostly versatile longitudinal slits longitudinal slits basal pores/short slits usually less than 25 m, exine nearly smooth, tricolporate over 35 m, exine finely granulate or finely reticulate, tricolporate Nectary intrastaminal disc none (?) none (?) base of filaments or base of ovary rarely nectariferous less than 25 m, (?) tricolporate, tricolpate in A. deliciosa base of corolla rarely nectariferous No. of carpels three two to six two or three mostly five three to many Styles nearly distinct distinct to united mostly united distinct to united distinct to united Placentation parietal axile or parietal (especially Cleyera) ovules pendulous from apex of axile placen- axile axile tae Number of ovules numerous numerous two or few two or few ten to many Ovule curvature campylotropous campylotropous campylotropous mostly anatropous antropous a Data from: Lechner (1915), Melchior (1925), Brown (1935), Erdtman (1952), Keng (1962), Dickison (1972), Cronquist (1981), Ferguson and Davison (1986), Ronse Decraene and Smets (1996), Takhtajan (1997), and Judd et al. (1999). ament bases. In the genus Ternstroemia there are at least two species with conical corolla tubes, which are correlated with buzz pollination (Bittrich, Amaral, and Melo, 1993). Flowers with corolla tubes and canalized access to the floral center evolved also in other families of the Ericales s.l., e.g., Ericaceae, Polemoniaceae, and Primulaceae. The incomplete understanding of corolla and androecium structure in the fossil flowers also poses some problems for evaluations of its systematic affinities. If correctly interpreted, the petals are united at their very base in pre-anthetic stages. The abscised corollas are clearly tubular, and it is possible that the united part of the corolla is longer in anthetic flowers. It is, however, difficult to establish even from transverse sections whether the petals are really united or just closely adhering to each other. It is also not clear whether the filament bases are free or fused to the corolla. Interestingly, both features are variable in extant members of the Ternstroemiaceae, Theaceae, and Actinidiaceae (Table 1). In the general systematic literature (e.g., Cronquist, 1981; Takhtajan, 1997), the petals of these families are described either as distinct or shortly connate, and the stamens are often described as free or adnate to the base of the petals. In his treatment of Theaceae (including Ternstroemiaceae), Melchior (1925) reported that petals are rarely totally free from each other. In some genera (e.g., Pyrenaria and Anneslea of Theaceae; Ternstroemia and Adinandra of Ternstroemiaceae) petals appear to be constantly united to different degrees, while other genera apparently also include species with free petals (e.g., Stewartia and Gordonia of Theaceae; Eurya of Ternstroemiaceae). In Actinidiaceae the petals are free or basally united. In Actinidia, as well as in Saurauia, both conditions seem to be present (Gilg and Werdermann, 1925; Dickison, 1972; Takhtajan, 1997). There is also considerable variation in the degree of fusion of the stamens with the corolla in the three families. In some genera the filaments are constantly free from the corolla (e.g., Anneslea, Actinidia), in others they are fused to the corolla to various degrees (e.g., Adinandra), while in some genera both conditions are present (e.g., Stewartia, Saurauia). Another feature of the fossil flowers that is difficult to interpret is the type of anther dehiscence, which we infer to be by short, apical slits. Similar dehiscence is found in Cleyera of the Adinandra group (Melchior, 1925). Ternstroemia crassifolia also has similar poricidal anthers (Ramirez et al., 1990), while all other Ternstroemiaceae and Theaceae apparently have anthers dehiscing by longitudinal slits. The anthers of Actinidiaceae also open by pores or short slits. Cronquist (1981) states that the openings are morphologically basal and only seemingly apical due to inversion of the anthers during floral ontogeny as is the case in all core Ericales (Anderberg, 1992; Judd et al., 1999).

11 March 2001] SCHÖNENBERGER AND FRIIS LATE CRETACEOUS ERICALEAN FLOWERS 477 TABLE 2. Comparison of age, systematic affinity, and floral characters of Cretaceous taxa referred to Ericales. a Characters Paradinandra suecica Actinocalyx bohrii Parasaurauia allonensis Palaeoenkianthus sayrevillensis Age late Santonian/early Campaniapanian late Santonian/early Cam- early Campanian late Turonian Suggested systematic among Theaceae, Ternstroemiaceae, Diapensiaceae Actinidiaceae Ericaceae affinity Actinidiaceae Sepals five, distinct, imbricate-quincunciacunciaquincuncial five, distinct, imbricate-quin- five, distinct (?), imbricate- five, united, imbricate-(?) Petals five, united (?), imbricatequincunciacuncial five, united, (?) five, distinct, imbricate-quin- five, united, valvate Stamens 15 in two whorls, antepetalous stamen pairs, fused to five in one whorl, fused to corolla ten in two whorls, free from corolla eight in one whorl, free from corolla corolla (?) Anthers basifixed, X-shaped, not inverted basifixed, sagittate (?), not basifixed, X-shaped b, invert- basifixed, sagittate, inverted inverted ed (?) Anther dehiscence short, apical slits (?) longitudinal slits short, basal slits (?) short basal slits Pollen tricolpate (?) tricolporate unknown tricolporate Carpel number three three three four Style structure basally united distinct distinct distinct Ovary apex three apical cavities slightly pointed apical depression convex Placentation parietal axile basal axile unknown Ovules numerous, campylotropous numerous, campylotropous numerous, (?) (?) Nectary intrastaminal disc absent absent absent Floral indumentum unicellular trichomes on sepals and gynoecium none multicellular trichomes on sepals unicellular and glandular (?) trichomes on sepals a Data from: Friis (1985); Nixon and Crepet (1993); and Keller, Herendeen, and Crane (1996). b The anthers of Parasaurauia allonensis were described as sagittate by Keller, Herendeen, and Crane (1996), but their figures (Figs. 9 15) clearly indicate that they are x-shaped, i.e., the two thecae are basally and apically separated. The three cavities in the apical part of the ovary and the short, united part of the styles have not been described for any extant member of the Ericales s.l. Some Actinidiaceae have ovaries with an apical depression from which the styles arise. Without detailed morphological and ontogenetical studies it is, however, impossible to conclude whether these structures are homologous. Pollination Clear distinction of sepals and petals, possible dehiscence of anthers by restricted slits, presence of a nectary, and the general floral construction (salverform corolla) with a canalized access to the floral center, clearly indicate that the fossil flowers were insect pollinated. A salverform corolla is especially prominent among flowers pollinated by Lepidoptera, but there are also many salverform flowers that are bee pollinated (Endress, 1994). Both Lepidoptera and Hymenoptera were probably already present during the Late Cretaceous (for overviews see Crepet, Friis, and Nixon, 1991; Grimaldi, 1999). The small size of the flowers, their relatively short floral tubes, and the presence of a nectary might indicate pollination by nectar-foraging butterflies or smaller bees rather than by larger bees or Lepidoptera with a longer proboscis such as hawk moths. Extant members of Actinidiaceae, Theaceae, and Ternstroemiaceae are mainly pollinated by pollen-foraging bees, but thrips and flies have also been reported as pollinators (Knuth, Appel, and Loew, 1904). Different species are adapted to buzz pollination by bees (Bittrich, Amaral, and Melo, 1993; Proctor, Yeo, and Lack, 1996). Buzz pollination is often correlated with anthers opening by apical pores or restricted slits and usually rather small pollen with a smooth exine (Buchmann, 1983; Endress, 1994). The pollen of the fossil flowers is very small, and the exine is only slightly foveolate. Further, the anthers probably opened by restricted apical slits. The presence of a distinct nectary and the salverform shape of the flowers, however, do not suggest buzz pollination for the fossil flowers. Floral nectar is almost never produced in buzz-pollinated flowers, although some exceptions have been reported in the Ericaceae (e.g., Arctostaphylos and Vaccinium; Buchmann, 1983). Final conclusions on specific pollinators or pollination mechanism in the fossil flowers cannot be drawn based on the information currently available. All characters taken together, the flowers from the Late Cretaceous described here most closely resemble those of the Adinandra group in Ternstroemiaceae. However, the fossil species do not belong to any of the extant genera described for this family. It probably represents a separate, now extinct phylogenetic lineage within the Ericales s.l., most likely among Ternstroemiaceae, Theaceae, and basal core Ericales. Fossil record of Ericales s.l. Different lineages of Ericales s.l. were clearly established during the Late Cretaceous and so far four distinct ericalean genera, including the new taxon in this study, have been formally described from the Late Cretaceous (Table 2). In addition to these taxa, which represent perhaps four different families in the Ericales s.l., a number of unnamed, putatively ericalean taxa have been reported from the Late Cretaceous. They were mainly found in mesofossil floras from Europe and eastern North America. Recently possible ericalean flowers have also been reported from coniacian deposits in Japan, also indicating a wide geographical distribution of ericalean plants in the Cretaceous. The general organization of the flowers of most Cretaceous taxa referred to the Ericales follows a common pattern: the flowers are small, bisexual, actinomorphic, and hypogynous; the pentamerous perianth consists of sepals and petals; the androecium consists of five to 20 (often multiples of five) stamens (eight in Palaeoenkianthus sayrevillensis), which are arranged in whorls; and the syncarpous gynoecium is often tri-

12 478 AMERICAN JOURNAL OF BOTANY [Vol. 88 merous (tetramerous in P. sayrevillensis) and contains numerous ovules. However, beyond this general floral bauplan morphology and structure of the floral organs are extremely diverse in fossil ericalean taxa (Table 2) and probably were paralleled by a broad diversity of pollinators and pollination mechanisms. The flowers of Actinocalyx bohrii (Friis, 1985a) were found at the same locality in southern Sweden as the fossils described here. Actinocalyx shares many similarities with extant Diapensiaceae and is in some respects also similar to the flowers described here (Table 2). Its flowers were probably insect pollinated as is indicated by their sympetaly and the canalized access to the floral center. From the same locality a few other so far unnamed flowers, fruits, and seeds are thought to belong also to the Ericales s.l., i.e., to Ternstroemiaceae or Theaceae (Friis, 1984). Close in age to the fossils from the Åsen locality is Parasaurauia allonensis and a few other flowers and fruits with possible ericalean affinity (Keller, Herendeen, and Crane, 1996; Herendeen et al., 1999) from the late Santonian Allon locality of central Georgia in North America. The floral characters of Parasaurauia allonensis (Table 2) are most similar to those of extant Actinidiaceae. Within this family the flowers of P. allonensis are most closely comparable to those of Saurauia, from which they differ mainly in the number of stamens (ten in the fossil vs. 15 to numerous in Saurauia). A variety of fossil taxa are reported from the Late Cretaceous (Turonian) of New Jersey (Crepet, 1996; Crepet and Nixon, 1996; Weeks, Nixon, and Crepet, 1996). Preliminary estimates suggest that there are at least 15 species and several genera with affinities to modern Ericales from that locality (Crepet, 1996). So far only one species has been named and described in detail: Palaeoenkianthus sayrevillensis, a species compared to basal Ericaceae, probably near extant Enkianthus (Nixon and Crepet, 1993). The floral features of P. sayrevillensis (Table 2), including sympetaly, awned anthers, and probably viscin threads, indicate a complex insect-pollination mechanism. Knobloch and Mai (1986) described a variety of fossils from the Late Cretaceous of central Europe. Among others, fruits and/or seeds possibly related to Ternstroemiaceae (e.g., Eurya, Visnea), Actinidiaceae (Saurauia) and Ericaceae (e.g., Leucothoe) are present. However, as most of these fossils are poorly preserved and hardly any floral characters are present, they are difficult to compare with other fossils and flowers of extant plants. Their systematic affinities therefore remain to be established with certainty. Recently flowers with capsular fruits and ribbed seeds, which possibly belong to the Ericales s.l., have been reported from the Coniacian of northeast Japan (Takahashi, Crane, and Ando, 1999b). So far no detailed description or comparison with extant plants has been provided and their systematic affinity remains uncertain. The obvious relative abundance of reported fossils from Late Cretaceous floras raises the question whether ericalean species were relatively more abundant during that time than they are today. This may well be the case. However, currently only a small percentage of the whole angiosperm diversity occurring in Late Cretaceous assemblages has been described. Therefore, information on the systematic composition of Late Cretaceous floras and the relative abundance of specific groups remains highly inconclusive. The morphological and systematical diversity, which is present in the ericalean fossil record from the Late Cretaceous and from the Tertiary, where the record of Ericales s.l. is extensive (e.g., Collinson, 1978; Friis, 1985b; Manchester, 1994), indicates that Ericales s.l. must have undergone a considerable differentiation already during the Cretaceous. Combined with the modern conception of asterid affinity (e.g., APG, 1998), the fossil record of Ericales s.l. implies that at least some basal groups of the asterids originated early in the diversification of the higher eudicots. Order Ericales s.l. FORMAL DESCRIPTION Family incertae sedis Paradinandra, gen. nov. The name Paradinandra refers to the similarities of the fossil flowers with those of different species of the Adinandra group [Adinandrieae sensu Keng (1962)]. Generic diagnosis Flower small, in axil of subtending bract, short pedunculate, bibracteolate, actinomorphic, hypogynous, pentamerous; calyx probably initiated in a spiral, all other floral parts whorled, whorls alternating; calyx of five distinct and imbricate sepals; corolla of five basally united (?) petals, imbricate; androecium of 15 stamens, diplostemon, inner whorl with stamen pairs, filaments basally united and fused to the corolla (?); anthers basifixed, x-shaped, dithecal, tetrasporangiate, probably opening by restricted apical slits; pollen small, tricolpate (?) with long colpi, exine finely foveolate; intrastaminal nectary disc; gynoecium trimerous, syncarpous, superior; with three almost completely free elongate styles; ovary unilocular, placentation parietal (ovary with incomplete septa); ovules numerous, campylotropous, surface reticulate. Comments on the new genus Mature fruits and seeds as well as most vegetative parts are unknown. Type species Paradinandra suecica, spec. nov. The specific epithet refers to Sweden where the fossil material was collected. Specific diagnosis As for the genus with the following additions: small scales present in the axils of the bracteoles, sepals broadly lanceolate, aestivation quincuncial, abaxial epidermis slightly papillate, with a prominent middle vein and simple trichomes abaxially, margins membraneous; petals mitriform, aestivation quincuncial; anthers stacked on three levels in the bud; filaments massive basally and tapering apically; thecae with enlarged epidermal cells along the stomium; styles with ventral slits; ovary with simple trichomes in older stages. Dimensions Measurements given for sectioned bud (holotype, S ): peduncle 0.6 mm long; flower 3.5 mm long and 1.2 mm wide (bud, including bracteoles); sepals mm; petals mm; filaments mm long; anthers mm; pollen m in polar length; ovary 0.4 mm in diameter; styles 0.65 mm long. Holotype S (sample Åsen 2), microtome sections S , Figs. 2, 3, 7, 15 17,

13 March 2001] SCHÖNENBERGER AND FRIIS LATE CRETACEOUS ERICALEAN FLOWERS 479 Type locality Ho ganäs AB quarry at Asen near Axeltorp, Scania, Sweden. Type stratum Fluviatile-lacustrine sequence. Age Late Cretaceous (Late Santonian-Early Campanian). LITERATURE CITED ANDERBERG, A. A The circumscription of the Ericales, and their cladistic relationships to other families of higher dicotyledons. Systematic Botany 17: Cladistic interrelationships and major clades of the Ericales. Plant Systematics and Evolution 184: APG (The Angiosperm Phylogeny Group) An ordinal classification for the families of flowering plants. Annals of the Missouri Botanical Garden 85: BASINGER, J.F.,AND D. L. DILCHER Ancient bisexual flowers. Science 224: BITTRICH, V., C. E. AMARAL, AND G. A. R. MELO Pollination biology of Ternstroemia laevigata and T. dentata (Theaceae). Plant Systematics and Evolution 185: 1 6. BOUMAN, F., AND F. D. BOESEWINKEL The campylotropous ovules and seeds, their structure and functions. 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