Lauraceous flowers from the Late Cretaceous of North Carolina, U.S.A.

Botanical Journal of the Linnean Society (2000), 132: 397–428. With 46 figures doi:10.1006/bojl.1999.0295, available online at http://www.idealibrary.com on

Lauraceous flowers from the Late Cretaceous of North Carolina, U.S.A. HELENA EKLUND Department of Palaeobotany, Swedish Museum of Natural History, Box 50007, SE-104 05 Stockholm, Sweden, and Department of Systematic Botany, Evolutionary Biology Centre, Villav. 18D, SE-752 36 Uppsala, Sweden Received February 1999; accepted for publication June 1999

Three new taxa with clear affinity to extant Lauraceae are described from the Santonian/ Campanian (c.83 Myr, Late Cretaceous) Neuse River locality in North Carolina, U.S.A. A new lauraceous genus, Neusenia, is established to accommodate an excellently preserved flower with tetrasporangiate anthers and psilate pollen grains. Two additional lauraceous taxa are described but not named due to incomplete preservation. The fossil taxa described in this paper represent a variety of evolutionary lineages within Lauraceae with respect to inflorescence structure and anther morphology, including both distinctly pedicellate flowers and sessile, closely crowded flowers, as well as tetrasporangiate and disporangiate anthers. In light of the co-occurrence of both tetrasporangiate and disporangiate anthers in the Neuse River flora, the plesiomorphic state of lauraceous anthers is discussed. Mapped on a recent cladogram of Laurales, tetrasporangiate anthers appear to be primitive within Lauraceae. Thus, disporangiate 2-valvate anthers must have evolved independently at least three times in Laurales (in Lauraceae, Hernandiaceae, and Atherospermataceae/Gomortegaceae). In Hernandiaceae and Atherospermataceae/Gomortegaceae such anthers are interpreted to have originated from tetrasporangiate 2-valvate anthers through reduction of the septum in each theca, while in Lauraceae they may have originated in the same way and/or from reduction of two pollen sacs in a tetrasporangiate 4-valvate anther.  2000 The Linnean Society of London

ADDITIONAL KEYWORDS:—Alseodaphne – Cinnamomum – Nectandra – Neocinnamomum – Ocotea – palaeobotany – Persea – Phoebe – Potoxylon – Umbellularia – valvate stamens. CONTENTS

Introduction . . . . . . . Material and methods . . . Systematics . . . . . . . Descriptions . . . . . . . Neusenia tetrasporangiata Taxon A . . . . . . Taxon B . . . . . . Discussion . . . . . . . Systematic relationships .

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Comparison with fossil flowers . . Are disporangiate or tetrasporangiate in Lauraceae? . . . . . . . Conclusions . . . . . . . . . . Acknowledgements . . . . . . . References . . . . . . . . . .

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INTRODUCTION

The Lauraceae is a large family with poorly understood intrafamilial relationships. Delimitation of genera and suprageneric taxa is difficult due to extensive character combinations and reticulate variation (e.g. Rohwer, 1993). Previous authors have suggested that widespread homoplasy or extinction of taxa with unusual character combinations may account for the difficulties in recognizing phylogenetic groupings (e.g. Kostermans, 1957; Rohwer, 1993). The family is, however, easily delimited and forms a clearly monophyletic group (e.g. Renner, 1999). The family members are characterized by a woody habit (except for the parasitic Cassytha L.) and small flowers typically with a trimerous organization. The perianth consists of two whorls of tepals, and the androecium usually has three whorls of fertile stamens and an inner fourth whorl of staminodes. Anthers are di- or tetrasporangiate and dehisce by apically hinged valves. The filaments of the third staminal whorl are often associated with paired glandular appendages. Pollen grains are typically inaperturate with extremely thin exine. The gynoecium consists of a single unilocular carpel with an anatropous, pendulous ovule. Lauraceae are today widely distributed in tropical to subtropical areas, with a few occurrences in temperate regions, and include about 50 genera and approximately 2500–3500 species. The fossil pollen record of Lauraceae is extremely poor (e.g. Muller, 1981). This can be explained by the poorly developed exines that apparently only rarely survive fossilization. Therefore the historical diversity of the group is best investigated through an analysis of macrofossil data. The macrofossil record of Lauraceae is extensive. About 40 genera and more than 500 lauraceous species have been reported from the Early Cretaceous through to the Late Tertiary (Eklund, 1993). These fossil taxa are based on leaves, fruits, flowers, and wood, and although the actual number of species is probably much lower than 500 due to synonymy and incorrect determinations of poorly preserved fossils, many reports of floral structures are well documented and an early abundance and diversity of the family is evident. Cretaceous reports of Lauraceae include flowers, fruits, inflorescences, leaves, and wood recovered from the Mid- and Late Cretaceous of Europe, Asia and North America (flowers: Drinnan et al., 1990; Kvacˇek, 1992; Herendeen, Crepet & Nixon, 1994; Eklund & Kvacˇek, 1998; fruits: Mickle, 1996; e.g. leaves: Berry, 1914; Neˇmejc & Kvacˇek, 1975; Crabtree, 1987; Upchurch & Wolfe, 1987; Upchurch & Dilcher, 1990; wood: Herendeen, 1991). The Tertiary record is even richer in plant parts with lauraceous affinity. Leaves and wood from the Early Tertiary are particularly common, but reproductive structures such as flowers, fruits, and cupulate structures also occur (leaves: Bandulska, 1926; Weyland, 1934, 1938; Kra¨usel, 1938; Dilcher, 1963; Kvacˇek & Bu˚zˇek, 1966; Sturm, 1971; Ferguson, 1974; Takhtajan, 1974; Kovach & Dilcher, 1984; Mai & Walther, 1985; e.g. wood: Barghoorn & Spackman, 1950; Wheeler, Scott & Barghoorn, 1977; Scott & Wheeler, 1982; flowers: Heer,

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1856; Conwentz, 1886; Berry, 1916; Weyland, 1938; Taylor, 1988; fruits/cupulate structures: Reid & Chandler, 1933; Scott, 1954; Kirchheimer, 1957; Chandler, 1964; Mai & Walther, 1985). The present work adds further information on the Late Cretaceous diversity of Lauraceae. Three new taxa are described from the Neuse River Locality in North Carolina, USA. Neusenia tetrasporangiata gen. et sp. nov. is based on a single excellently preserved flower bud, and shows close similarity to extant Neocinnamomum H.Liu in particular, but also to Alseodaphne Nees, Cinnamomum Schaeff., Nectandra Rol. ex Rottb., Ocotea Aubl., Persea Mill., Phoebe Nees, Potoxylon Kosterm., and Umbellularia. (Nees) Nutt. Taxon A comprises three partly charcoalified and less completely preserved specimens. Taxon B is described from fragmentary flowers, but nevertheless shows clear affinity to Lauraceae.

MATERIAL AND METHODS

The fossil material was provided by Dr F. Hueber. It was collected by Mr Edward Womble at the Neuse River Cut-off, southwest of Goldsboro, Wayne County, North Carolina (35°21′N,78°1′W). The fossil-bearing sequence, which belongs to the nonmarine Black Creek Formation, consists of sands, silts and clay with lignitic horizons. Previous works have indicated a Campanian age for the upper part of the Black Creek Formation (Christopher, Owens & Sohl, 1979; Hueber & Watson, 1988), and a later Santonian age for the basal part (e.g. Raubeson & Gensel, 1991). Fossil plant material occurs abundantly at the Neuse River locality and includes leaves, large logs, and other macrofossils, as well as a rich assemblage of smaller plant remains extracted by bulk sieving. The fossils are usually lignified and more or less compressed, but rare charcoalified specimens occur as well. The flora obtained by sieving includes abundant conifer twigs (e.g. Androvettia statenensis Hueber & Watson 1988; A. carolinensis, Brachyphyllum squamosum, B. sp., Geinitzia reichenbachii, and Moriconia cyclotoxon Raubeson & Gensel 1991), well-preserved angiosperm reproductive structures (Spirematospermum chandlerae Friis 1988; Platananthus hueberi and Platanocarpus carolinensis Friis, Crane & Pedersen 1988; Liriodendroidea alata, L. carolinensis, and L. latirapha Frumin & Friis 1996; Grexlupus carolinensis Mickle 1996); numerous undescribed flowers, fruits and seeds, and a diversity of angiosperm woods. Among the isolated reproductive structures are numerous lauraceous fruits described as Grexlupus carolinensis (Mickle, 1996). These fruits are completely enclosed by a conspicuously wrinkled structure probably representing the enlarged receptacular tube. The macroflora from the South Carolinan part of the Black Creek Formation includes ferns, conifers and a variety of angiosperm leaves (Berry, 1914). Among the angiosperm leaves are three taxa with suggested lauraceous affinity (Berry, 1914). The samples studied for this work were washed over a 125 lm sieve, and the plant remains subsequently cleaned with hydrofluoric (HF) and hydrochloric (HCl) acid, washed in water, and air dried. Specimens were studied under light microscope (LM) and scanning electron microscope (SEM). Specimens to be studied using SEM were mounted on aluminium stubs using nail polish and coated with a thin gold ˚ ). layer (approximately 100 A

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All specimens are deposited in the palaeobotanical collections of the National Museum of Natural History, Smithsonian Institution, Washington, D.C., U.S.A. (USNM).

SYSTEMATICS

Neusenia Eklund gen. nov. Derivation of name. From the Neuse River that runs close to the type locality. Generic diagnosis. Pedicellate flower with six tepals in two whorls of three; outer tepals only slightly smaller than inner tepals. Tepals fused at the base forming a short perianth tube. Androecium consisting of nine fertile stamens in three whorls of three and three staminodes in an inner fourth whorl; filaments of third whorl with paired glandular appendages. Anthers tetrasporangiate. Pollen sacs arranged into two laterally separated pairs; each pair with a longer marginal pollen sac and a shorter median pollen sac. Anthers of first and second whorls with introrse median pollen sacs and introrse-latrorse marginal pollen sacs, anthers of third whorl with extrorse median pollen sacs and extrorse-latrorse marginal pollen sacs. Ovary a single carpel with a slender style. Type species. Neusenia tetrasporangiata sp.nov. Derivation of specific epithet. From the anthers with four pollen sacs. Specific diagnosis.  ligulate to triangular; outer and inner surface covered by a dense indumentum, showing conspicuous globular cells (ethereal oil cells?).  c. 3/4 the length of the anthers, with globular cells (ethereal oil cells?) and covered by indumentum. Glandular appendages kidney-shaped, adnate towards the base of filaments.  sessile, small and conical-triangular.   spherical and psilate, c. 34 lm in diameter.  slightly clavate apically and with small stigmatic area. Dimensions. Length of type specimen: 2.5 mm; breadth of type specimen: 1.9 mm. Length of outer tepals: c. 1.6 mm; breadth of outer tepals: c. 1.1 mm. Length of inner tepals: c. 2.3 mm; breadth of inner tepals: c. 1.1 mm. Length of stamens: c. 1.3 mm. Length of anthers: c. 0.75 mm; breadth of anthers; c. 0.5 mm. Length of staminodes: c. 0.6 mm. Diameter of pollen grains: c. 34 lm. Length of ovary: c. 1.3 mm. Holotype. USNM401698. Type locality. Neuse River Cut-off, southwest of Goldsboro, Wayne County, North Carolina (35°21′N,78°1′W). Type stratum. Black Creek Formation. Age. Santonian/Campanian. Material. USNM401698.

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DESCRIPTIONS

Neusenia tetrasporangiata sp. nov. (Figs 1–20) Although only a single floral bud of Neusenia tetrasporangiata was recovered, the excellent preservation allowed a complete reconstruction of the flower organization. After documenting the external features the bud was repeatedly dissected and restudied under the SEM. Flower. Isolated; inflorescence structure is unknown. It is bisexual, trimerous and small (c. 2.5 mm long and c. 1.9 mm broad), and was probably fossilized in a late bud stage (Fig. 1). A short fragmented pedicel of c. 0.4 mm is preserved, but its original length is not known. Perianth. Consists of six tepals arranged in two alternate whorls (Figs 1, 20). Outer tepals are slightly shorter than inner tepals. All tepals are erect and tightly enclosing the inner whorls of floral organs, indicating that the flower was fossilized in a late bud stage. Outer and inner surfaces of tepals show conspicuous globular cells (ethereal oil cells?) (Fig. 18) and were originally covered by dense indumentum as indicated by preserved trichomes and numerous trichome bases (Figs 18, 19). Tepals are united basally forming a short floral tube about 0.2 mm long. Androecium. Consists of nine fertile stamens and three staminodes in four alternate whorls (Figs 2–5, 7–9, 13–15, 20). Stamens are differentiated into anther and filament (e.g. Fig. 2). Anthers are tetrasporangiate and dehisce through apically hinged valves (Figs 8 & 9, 11–14). The sporangia are of unequal length and arranged in two lateral pairs; marginal pollen sacs are longer than median pollen sacs (Figs 13, 14). Anthers of first and second whorls have introrse median and introrse-latrorse marginal sporangia, while anthers of a third whorl have extrorse median and extrorse-latrorse marginal sporangia. Apical connective is c. 0.25 mm in length. Filaments of third staminal whorl are associated with paired glandular appendages that are attached close to the filament base (Figs 7, 10, 20). Staminal appendages are differentiated into a glandular head showing globular cells (ethereal oil cells?) and a short stalk. Adaxial and abaxial surfaces of anthers and filaments show conspicuous globular cells (ethereal oil cells?) (Figs 2, 15) and are covered with erect trichomes. Staminodes are conical-triangular and closely surrounding the gynoecium (Figs 3–5). Only the abaxial side was observed, and this is covered by erect trichomes and shows conspicuous globular cells (ethereal oil cells?). Pollen. Grains were observed in situ in one anther (Figs 16,17). Spherical, about 34 lm in diameter, and psilate. No aperture was observed, indicating that the pollen grains are acolpate. Gynoecium. Consists of a single carpel with a slender style (Figs 3–6, 20). Total length of pistil is about 1.3 mm from ovary base to style apex. The style is slightly clavate apically, and the small stigmatic area appears to have been papillate originally (Fig. 6). Ovules. Position and organization have not been observed. Indumentum. Elongated, simple, and apically directed trichomes are densely spaced on outer and inner surfaces of tepals, adaxial and abaxial surfaces of stamens, and abaxial surface of staminodes (Figs 5, 18, 19).

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Secretory cells. Small globular cells with a diameter of 0.01–0.02 mm occur frequently in the tissues of tepals, anthers, filaments, heads of glandular staminal appendages, and staminodes (Figs 2, 5, 10, 11, 13, 15, 18). They probably represent ethereal oil cells. Stomata. Not observed on any of the organs. Taxon A (Figs 21–37) Material. USNM401693, USNM401695, USMN401697. This taxon is represented by three more or less three dimensional, charcoalified specimens. The specimens are isolated inflorescence units consisting of three sessile and closely spaced flowers. The three flowers are collectively enclosed by two broad and strongly truncate bracts (Figs 21–25). The position of the three flowers and the two enclosing bracts make the inflorescence units zygomorphic. The outer organs of the inflorescence units are well preserved, but dissection of the specimens revealed only little information about the flowers; number and organization of tepals and stamens could not be established, but the flowers appear to have a trimerous organization. The stamens are differentiated into filament and anther; anthers are disporangiate with valvate dehiscence. The gynoecium consists of a single carpel with dense indumentum. The carpel is unilocular with a single apical ovule. Specimen USNM401693 is an inflorescence unit with three flowers (Figs 21, 22, 36, 37). It is about 1.4 mm long and 1.5 mm broad. All flowers are sessile and attached at the same height. Two flowers are collateral and each of them is enclosed by one of the two bracts (Fig. 21); the third flower is borne behind the other two flowers in a median position (Fig. 22). Tepal number and arrangement could not be clearly observed, but tepals appear to be arranged in at least two series (whorls?). Tepals of outer series are shorter and broader than tepals of inner series; tepals of inner series show distinct perforations on cuticle towards the apex (Figs 36,37). These structures may be associated with resinous inclusions. Specimen USNM401695 is an inflorescence unit with three flowers (Figs 23–27). It is about 1.9 mm long and 2.3 mm broad. All flowers are sessile and attached at the same height. Two flowers are collateral and each of them enclosed by one of the two bracts (Figs 23, 24); the third flower is borne behind the other two flowers in a median position. On the side of the zygomorphic inflorescence unit where the two collateral flowers are seated, the enclosing bracts are relatively short and strongly

Figures 1–6. SEM micrographs of Neusenia tetrasporangiata gen. et sp. nov. (USNM 401698) Fig. 1. Unopened flower bud showing two tepals of outer perianth whorl and one tepal of inner perianth whorl. Scale bar=1 mm. Fig. 2. Same specimen as in Fig. 1 after tepals were removed; note stamens on the rim of the flower. Scale bar=1 mm. Fig. 3. Same specimen as in Figs 1 & 2 after stamens were removed; note triangular staminodes and elongated style. Scale bar=1 mm. Fig. 4. Same flower fragment as in Fig. 3 after it was turned to the other side and remaining tepals and anther were removed; note central carpel with elongated style surrounded by two staminodes. Scale bar=1 mm. Fig. 5. Detail of flower fragment in Fig. 4 showing staminodes in higher magnification (arrows). Scale bar=0.1 mm. Fig. 6. Detail of flower fragment in Fig. 4 showing stigmatic area. Scale bar=0.1 mm.

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Figures 18–19. SEM micrographs of Neusenia tetrasporangiata gen. et sp. nov. (USNB 401698) Fig. 18. Detail of abaxial side of anther in Figs 2 and 15; note bulging cells and erect trichomes. Scale bar =0.1 mm. Fig. 19. Detail of abaxial side of one of outer tepals in Fig. 1 showing erect trichomes and rounded trichome bases. Scale bar=0.1 mm.

truncate with an apparently thin texture (Figs 23, 24). On the other side of the inflorescence unit, where the single flower is seated, the enclosing bracts are differentiated into a thinner apical rim of the same texture as on the opposite side of the inflorescence unit, and a basal part of a coarser texture (Fig. 25). The basal part is covered by erect trichomes. Flowers are about 1.9 mm long and 1.3 mm broad. Tepal number and arrangement could not be clearly observed, but tepals appear to be arranged in at least two series (whorls?) and show conspicuous bulging cells that probably represent ethereal oil cells (Figs 23, 24). Tepals of outer series are shorter and broader than tepals of inner series (Fig. 23); tepals of inner series show distinct perforations on cuticle towards the apex. Dissection of the inflorescence unit revealed that tepals of inner series have ciliate margins and are fused at the base (Fig. 26). Dissection of the flowers demonstrated that stamens are differentiated into anther and filament, and that anthers are disporangiate dehiscing through apically hinged valves (Fig. 27).

Figures 7–17. SEM micrographs of Neusenia tetrasporangiata gen. et sp. nov. (USNM 401698) Fig. 7. Same flower fragment as in Fig. 3 after it was turned to the other side, but before remaining anther was removed; note paired glandular appendages attached towards base of filament. Scale bar= 1 mm. Fig. 8. Fragment with stamen attached on tepal that was removed from flower fragment in Fig. 3 after it was turned to the other side; note two lateral pairs of pollen sacs; both pollen sacs of the right pair and right pollen sac of the left pair are dehisced; note also detached valve that is laying diagonally over the left pair of pollen sacs. Scale bar=1 mm. Fig. 9. Anther detached from specimen in Figs 1 & 2 showing left pair of pollen sacs; note apically hinged valves. Scale bar=0.1 mm. Fig. 10. Detail of paired glandular appendages in Fig. 7. Scale bar=0.1 mm. Fig. 11. Detail of anther in Fig. 9 showing apical part of valves. Scale bar=0.1 mm. Fig. 12. Detail of anther in Fig. 9 showing basal part of valves. Scale bar=0.1 mm. Fig. 13. Detail of stamen in Fig. 8. showing anther and two lateral pairs of pollen sacs in higher magnification; note that median pollen sacs are shorter than lateral pollen sacs. Scale bar=0.5 mm. Fig. 14. Anther detached from specimen in Figs. 1 & 2 showing the two lateral pairs of pollen sacs. Scale bar=0.5 mm. Fig. 15. Detail of flower fragment in Fig. 2 showing abaxial surface of stamen; note bulging cells on surface of anther. Scale bar=1 mm. Fig. 16. Detail of stamen in Fig. 8 showing in situ pollen grains. Scale bar=0.1 mm. Fig. 17. Detail of pollen grain in Fig. 16 showing unsculptured surface. Scale bar=10 lm.

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Figure 20. Neusenia tetrasporangiata gen et sp. nov. Floral diagram.

Specimen USNM401697 is a fragmentary preserved inflorescence unit with incomplete supporting bracts (Figs 28–35). Flowers of this specimen have relatively large and strongly hairy carpels (Figs 28, 29, 31, 33, 34), and appear to be in a later developmental stage than flowers of specimens USNM401693 and USNM401695. Dissection of the specimen revealed three more or less compressed and poorly preserved flowers. They are 2.5–2.8 mm long and 1.3–1.6 mm broad. Observations from one of the flowers indicate that the perianth consists of two whorls of three tepals; while the outer tepals are short with ciliate margins, the inner tepals are longer with ciliate margins (Figs 31, 32). Outer tepals are fused for a short distance at the base forming a short floral tube. Another flower shows that also the inner tepals are fused at the base (Fig. 31). Stamens are poorly preserved, and their number could not be established. They are differentiated into anther and filament, and anthers are disporangiate with valvate dehiscence (Fig. 30). The gynoecium consists of a single unilocular carpel with an apically attached ovule (Fig. 33). Inner surface of carpel wall shows irregularly shaped cells with thickened cell walls (Fig. 35). Taxon B (Figs 38–44) Material. USNM401649, USNM401652, USNM401662, USNM401699, USNM401717–401720. This taxon is represented by numerous fragmentary preserved flowers and one fruit. The perianth is trimerous with six tepals in two whorls of three. Outer tepals are about 0.6 mm long and much shorter than inner tepals which are always incomplete (Figs 38, 39). Inner tepals especially show conspicuous and densely distributed globular cells that probably represent ethereal oil cells (Figs 38, 40, 41). The androecium is incomplete and number of stamens could not be established.

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All anthers are detached, but a few filaments and associated paired glandular appendages have been observed (Figs 42, 43). Staminal appendages are differentiated into a head and a short stalk; heads are half-spherical with a mouth shaped fold close to the distal part of the stalk (Figs 42, 43). One specimen is a more or less globular fruit borne on a slightly thickened pedicel; the three smaller tepals of outer perianth whorl are still attached (Fig. 44).

DISCUSSION

Systematic relationships Classification within Lauraceae has been difficult and the family is not easily subdivided into morphologically well circumscribed subunits. Phylogenetic reconstruction based on morphological characters has not really been attempted and the difficulties in classification suggest that there may be extensive homoplasy in morphological features. The three most recent classifications of the family are by Kostermans (1957), Rohwer (1993), and van der Werff & Richter (1996). Kostermans (1957) recognized two subfamilies; Cassythoideae Kosterm., including the parasitic genus Cassytha, and Lauroideae Kosterm., including all other genera. Lauroideae was subdivided into five tribes based on inflorescence structure, presence/ absence of involucre, and presence/absence of a cupule at the fruit base. Further subdivision into nine subtribes was based on number of pollen sacs per anther. Van der Werff & Richter (1996) subdivided the family into three tribes based on inflorescence features in combination with wood and bark structure. The first tribe, Laureae Le Maout & Decne., is characterized by the presence of an involucre of bracts enclosing the partial inflorescences. The basic inflorescence structure is racemose, but the inflorescence axis is often shortened giving the inflorescence an umbellate appearance. Flowers have a single bracteole at the pedicel base. The second tribe, Perseeae Nees, includes genera with paniculate-cymose inflorescences. The primary branching of the inflorescence is paniculate with alternate or opposite branches. The terminal units of the inflorescences are basically cymes with opposite flowers. According to J. Rohwer (pers. comm.) there are, however, many reductions that may sometimes even lead to botryoid inflorescences. The pedicel bears two opposite bracts. The third tribe, Cryptocaryeae Nees, includes genera with paniculate to more or less cymose inflorescences similar to those of tribe Perseeae, but flowers are not arranged in strict cymes. Number and positions of bracts on the pedicel is variable. In a preliminary classification Rohwer (1993) recognized two tribes based on inflorescence type, presence/absence of inflorescence involucra, and the direction of anther dehiscence of third whorl. Thus, flowers of Perseeae Nees have thyrsoid inflorescences without involucra, and extrorse anthers of third whorl, and flowers of Laureae Le Maout & Decne. have (di)botryoid inflorescences with involucra, and introrse anthers of third whorl. Perseeae was further subdivided into three informal groups and nine subgroups. Rohwer (1993) described the Cryptocarya group as an artificial group including the genera in which the fruit is completely enclosed by the enlarging receptacular tube. This is in contrast to the Beilschmiedia group, in which the flower tube does not enlarge after anthesis and where the naked fruit is seated

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exposed on the pedicel. The largest and least homogeneous group is the Ocotea group, which includes all genera with presumed primitive characters but also several advanced lineages. A molecular-based phylogenetic analysis (Rohwer in press), however, shows conflicting results with the above suggested classifications, in that a subdivision based on inflorescence structure is not indicated. Instead, there seems to be an early division into a Gondwanan group and a Laurasian-South American group (Rohwer, in press). Nevertheless, the classification by Rohwer (1993) is well structured and provides detailed information about the genera included in the different groups. Therefore, I will follow this in the discussion below concerning the systematic affinities of the fossils. Neusenia tetrasporangiata sp. nov. Based on the tripartite flower organization with six tepals in two whorls, nine fertile stamens in three whorls, three inner staminodes, paired glandular staminal appendages, tetrasporangiate anthers with valvate dehiscence, and a unicarpellate ovary, Neusenia is assigned to Lauraceae, which is the only extant family possessing the same suite of characters. Stamens with valvate anthers and paired glandular staminal appendages also occur in the closely related families Monimiaceae and Hernandiaceae, but in these families anthers are invariably disporangiate. Neusenia is known only from a single isolated flower, and there is no information on inflorescence structure and fruit morphology. Comparisons with extant genera are therefore restricted to the floral features. Anthers with four pollen sacs are present in 29 out of 52 genera (Table 1 this work; Rohwer, 1993). Of these, 20 genera show major differences from the fossil in various respects, e.g. two genera have invariably unequal outer and inner tepals (Caryodaphnopsis Airy Shaw, Nothaphoebe Blume), four genera have differently arranged pollen sacs (i.e. apical or latrorseintrorse+lateral-extrorse; Paraia Rohwer, H.G. Richt. & van der Werff, Pleurothyrium Nees ex Lindl., Povedadaphne W.C. Burger, Williamodendron Kubitzki & H.G. Richt.), seven genera have introrse anthers of the third staminal whorl (Actinodaphne Nees, Cinnadenia Kosterm., Eusideroxylon Teijsm. & Binn., Litsea Lam., Neolitsea Merr., Parasassafras G. Long, Sassafras Presl), in one genus, filaments of the third whorl are united into a tube (Systemonodaphne Mez), in one genus, stamens of the first whorl are transformed into a third whorl of tepals (Dicypellium Nees & C. Mart.), eight genera have fewer or more than nine fertile stamens (Chlorocardium Rohwer, H.G. Richt. & van der Werff, Cinnadenia, Dicypellium, Dodecadenia Nees, Eusideroxylon, Litsea, Neolitsea, Williamodendron), and three genera have more than three pairs of staminal glands (Chlorocardium, Litsea, Urbanodendron Mez). Further, eight genera have unisexual flowers (Actinodaphne, Cinnadenia, Dodecadenia, Hypodaphnis Stapf, Litsea, Neolitsea, Parasassafras, Rhodostemonodaphne Rohwer & Kubitzki), and nine genera lack staminodes (Chlorocardium, Cinnadenia, Dicypellium, Dodecadenia, Hypodaphnis, Neolitsea, Rhodostemonodaphne, Parasassafras, Sassafras). The unisexual flowers and absence of staminodes alone may not be reasons to exclude relationships with Neusenia, but in all cases except Hypodaphnis, these reductions co-occur with other differences. Thus, following the classification of Rohwer (1993) the floral characters of Neusenia indicate strongest affinity to Umbellularia of tribe Laureae, and to most genera of the Eusideroxylon, Ocotea and Persea subgroups of tribe Perseeae (Table 1). Umbellularia (Laureae), Potoxylon (Cryptocarya subgroup of Perseeae), Cinnamomum, Neocinnamomum,

Eusideroxylon

Eusideroxylon Potoxylon









Hypodaphnis

Hypodaphnis

Cryptocarya

Alseodaphne Caryodaphnopsis Notaphoebe Persea Phoebe

Persea

Ocotea

Aniba Dicypellium Paraia Systemonodaphne Umbellularia Urbanodendron

Ocotea

Cinnamomum Nectandra Neocinnamomum Ocotea Pleurothyrium Rhodostemonodaphne

Perseeae

Povedodaphne Williamodendron

Mezilaurus Actinodaphne Dodecadenia Litsea Neolitsea Parasassafras Sassafras

Laureae

T 1. Lauraceous genera with tetrasporangiate anthers; classification according to Rohwer, 1993

Chlorocardium Cinnadenia

Genera insertae sedis

LATE CRETACEOUS LAURACEOUS FLOWERS 409

410

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Figures 21–27. SEM micrographs of taxon A (Figs 21, 22. USNM401693; Figs 23–27. USNM401695). Fig. 21. Inflorescence fragment showing three sessile and crowded flowers supported by two large bracts; note that two flowers are borne next to each other and the third flower in a median position behind them. Scale bar=1 mm. Fig. 22. Other side of same inflorescence fragment as in Fig. 21 showing median flower borne in front of the two lateral flowers. Scale bar=1 mm. Fig. 23. Inflorescence fragment showing two lateral flowers supported by two large bracts; note bulging cells on surface of

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Nectandra, Ocotea (all Ocotea subgroup of Perseeae), Alseodaphne, Persea and Phoebe (all Persea subgroup of Perseeae) have flowers with tetrasporangiate anthers that dehisce extrorsely in the third staminal whorl. Pollen sacs are arranged in two pairs above each other (Alseodaphne, Cinnamomum, Ocotea, Persea, Phoebe, Umbellularia), in an arc (Nectandra, Neocinnamomum, Persea), or in a horizontal or subapical row (Neocinnamomum, Potoxylon). Tepals are equal to subequal in all genera except in Persea where they may also be strongly unequal. Paired glandular appendages are restricted to filaments of third staminal whorl. Because these genera are very similar in most floral characters it is difficult, without information on fruit and inflorescence features, to establish exactly to which extant genus the fossil shows the closest affinity. However, some differences can be found in staminode and pollen morphology. In contrast to the sessile, almost triangular staminodes of Neusenia, staminodes of Cinnamomum, Persea, and Phoebe are distinctly stipitate, and the staminodes of Nectandra and Ocotea club shaped to columnar (Rohwer, 1993). Umbellularia differs from Neusenia in having distinct staminodes with glandular apices. The remaining genera with staminodes comparable to those of Neusenia are thus Alseodaphne, Neocinnamomum and Potoxylon with more or less heart shaped, ligulate or triangular staminodes, respectively (Rohwer, 1993; pers. observ. from herbarium material). Shang & Tang (1995) recognized seven lauraceous pollen types based on sculpture and structure of exine. Alseodaphne, Ocotea, Persea, and Phoebe have pollen of the Persea type, i.e. exine with very small, distinct, and densely distributed spines without circular protrusions at the base. Cinnamomum and Umbellularia have pollen grains of the Sassafras type, i.e. exine with smooth spines and circular protrusions at the base. Pollen of Nectandra have exine with distinct spines, and appears to fall within the Sassafras type (Raj & van der Werff, 1988; personal SEM observations from herbarium material). Neocinnamomum and Potoxylon are unique among the tetrasporangiate genera in having pollen grains of the Cryptocarya type, i.e. more or less smooth exine without spines or clavae (van der Merwe, van Wyk & Kok, 1990; Shang & Tang, 1995). While pollen of Neocinnamomum are psilate with a more or less spherical shape (Shang & Tang, 1995), pollen of Potoxylon are verrucate to almost smooth with a prolate shape (van der Merwe et al., 1990). Thus, the smooth and spherical pollen grains of Neusenia may indicate that the fossil is closer to Neocinnamomum than to the other genera. Taxon A Although reconstruction of the complete floral organization was not possible due to the poor preservation of the fossils, the combination of an apparent trimerous perianth, disporangiate valvate anthers, a unicarpellate gynoecium with a single apical ovule, and ethereal oil cells, indicates a lauralean affinity. Disporangiate anthers that

tepals. Scale bar=1 mm. Fig. 24. Detail of inflorescence fragment in Fig. 23 showing apex of left flower and apex of supporting bract; note perianth with shorter outer tepals and longer inner tepals. Scale bar=1 mm. Fig. 25. Other side of part of inflorescence fragment in Fig. 23 showing supporting bracts; note that this side of bracts is differentiated into an apical rim of a thinner texture and a basal part of coarser texture. Scale bar=1 mm. Fig. 26. Compressed flower detached from inflorescence fragment in Fig. 23; note ciliate margin of outer tepals. Scale bar=1 mm. Fig. 27. Anther removed from one of the flowers of inflorescence fragment in Fig. 23; note the two dehisced pollen sacs. Scale bar=0.1 mm.

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H. EKLUND

Figures 28–33. SEM micrographs of taxon A (USNM401697). Fig. 28. Inflorescence fragment showing incompletely preserved flowers and supporting bracts; note large and hairy carpel in the middle. Scale bar=1 mm. Fig. 29. Detail of inflorescence fragment in Fig. 28 showing apical part of hairy carpel. Scale bar=1 mm. Fig. 30. Fragment removed from inflorescence fragment in Fig. 28 showing incompletely preserved stamen. Scale bar=0.5 mm. Fig. 31. Flower of inflorescence fragment in Fig.

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Figures 34–37. SEM micrographs of taxon A. (USNM 401697). Fig. 34. Apical part of carpel removed from one of the flowers of inflorescence fragment in Fig. 28. Scale bar=1 mm. Fig. 35. Inner surface of carpel wall of flower removed from inflorescence fragment in Fig. 28; note irregular shape of cells. Scale bar=0.1 mm. Fig. 36. Detail of inflorescence fragment in Fig. 21 showing perforation of apical part of inner tepal; note crystal like structure inside perforation. Scale bar=0.01 mm. Fig. 37. Detail of inflorescence fragment in Fig. 21 showing perforation of apical part of inner tepal. Scale bar= 0.01 mm.

dehisce through apically hinged valves are known for the Lauraceae as well as the Gomortegaceae, Hernandiaceae, Atherospermataceae, and Siparunaceae. The closest affinity of the fossil appears to be with the Lauraceae. Flowers of Gomortegaceae and Hernandiaceae are epigynous, and flowers of the Gomortegaceae further differ from the fossil in having a syncarpous, (2–)3(–5)-locular ovary. Flowers of Atherospermataceae and Siparunaceae differ from the fossil in having an apocarpous gynoecium of several carpels and a basal position of the ovule. The presence or absence of an involucre of decussate, large, persistent bracts has often been used for establishing intrafamiliar relationships (e.g. Kostermans, 1957; Rohwer, 1993). All genera in the tribe Laureae have inflorescence units enclosed by some kind of involucre (e.g. Rohwer, 1993), and if the two large bracts surrounding the three-flowered inflorescence of taxon A represent such involucre bracts, this feature could indicate relationship, within this tribe. Within Laureae disporangiate anthers occur regularly in Iteadaphne Blume, Laurus L., and Lindera Thunb., and in some species of Sassafras and Parasassafras. The inflorescence structure is basically

28 after two other flowers were removed; note ciliate margins of tepals. Scale bar=1 mm. Fig. 32. Flower removed from inflorescence fragment in Fig. 28.; note short outer tepals with ciliate margins and longer inner tepals. Scale bar=1 mm. Fig. 33. Other surface of large and hairy carpel in Figs 28 and 29; note apical ovule. Scale bar=1 mm.

414

H. EKLUND

LATE CRETACEOUS LAURACEOUS FLOWERS

415

(di)botryoid in these genera, but mostly the distal internodes are reduced resulting in pseudo-umbellate inflorescence units (Rohwer, 1993). Although the three-flowered inforescence unit of taxon A is perhaps better interpreted as a cyme rather than a pseudo-umbel, and flowers with distinctly smaller outer tepals do not occur within extant Laureae, the presence of enlarged bracts supporting the inflorescence unit still indicate that the fossil is most closely related to the taxa in this tribe. Indeed, in the species currently called Lindera spicata Kosterm. the flowers, which are of the typical Lindera organization, are arranged in inflorescences abberant for the genus. At a young developmental stage the inflorescences look like short spikes borne in the axils of foliage leaves. Each flower is enclosed by two large, hood-shaped bracteoles that fall off at anthesis. Also at anthesis the pedicels elongate a little resulting in short racemose inflorescences. Eventually some of the ‘racemes’ elongate further and resume vegetative growth at their tip ( J. Rohwer, pers. comm.). As suggested by J. Rohwer, starting with this species it would only take one additional flower to originate from the axil of each of the two large bracteoles to arrive at an inflorescence unit as in taxon A. Taxon B Flowers with paired staminal appendages and ethereal oil cells are found in Atherospermataceae, Hernandiaceae, Lauraceae, and a few species of Monimiaceae (Peumus boldus Molina, Hortonia angustifolia Trimen, the three species of Monimia Thouars). The hypogynous flower organization of the fossil differs from that of Hernandiaceae where flowers are epigynous. While the flowers of Lauraceae typically have a perianth of six tepals in two alternate whorls of three, perianth structure in Atherospermataceae and Monimiaceae is variable. In these families tepals may be arranged in a spiral, in tetramerous whorls, or in decussate pairs. Further, while a gynoecium consisting of a single carpel is the normal condition in Lauraceae, the apocarpous gynoecium of Atherospermataceae and Monimiaceae usually has several carpels. Because the perianth and gynoecium features of the fossil are more common in the Lauraceae than in the Atherospermataceae and Monimiaceae, the fossil is tentatively assigned to Lauraceae. The combination of strongly unequal tepals and a naked fruit on a slightly enlarged pedicel is only found in four extant genera, namely Caryodaphnopsis, Dehaasia Blume, Notaphoebe, and Persea. The persistence in the fossil of outer tepals below

Figures 38–44. SEM micrographs of taxon B. Fig. 38. Flower fragment showing apical part of pedicel, two short tepals of outer perianth whorl, and one broken large tepal of inner perianth whorl; note bulging cells on tepals. Scale bar=1 mm (USNM401720). Fig. 39. Flower fragment showing pedicel, two short tepals of outer perianth whorl, and poorly preserved tepals of inner perianth whorls. Scale bar=1 mm (USNM401717). Fig. 40. Flower fragment showing poorly preserved tepals of outer perianth whorl (arrow) and broken tepals of inner perianth whorl; note bulging cells on inner tepals. Scale bar=1 mm (USNM401718). Fig. 41. Detail of flower fragment in Fig. 40 showing bulging cells on surface of inner tepal. Scale bar=0.1 mm (USNM401718). Fig. 42. Flower fragment showing filament bases attached on broken tepals; note paired glandular appendages attached towards filament bases. Scale bar=1 mm (USNM401719). Fig. 43. Detail of flower fragment in Fig. 42 showing paired glandular appendages in higher magnification; note that appendages are differentiated into a glandular head seated on a stalk; note also the mouth like horizontal furrow close to distal part of stalk. Scale bar=1 mm (USNM401719). Fig. 44. Fruit attached on pedicel; note persistent small tepals of outer perianth whorl. Scale bar=1 mm (USNM401699).

416

H. EKLUND

the fruit base indicates that Dehaasia is less closely related to the fossil than are the other genera. Of the remaining three genera the fossil may be closest to extant Caryodaphnopsis, which according to J. Rohwer (pers. comm.) have very similar fruits.

Comparison with fossil flowers Fossil flowers or flower fragments showing distinct lauraceous features and representing about 13 taxa have previously been described from the Early Cretaceous through to the Quaternary (Table 2; Heer, 1856; Conwentz, 1886; Chaney & Mason, 1933; Weyland, 1938; Taylor, 1988; Drinnan et al., 1990; Crane, Friis & Pedersen, 1994; Herendeen et al., 1994; Eklund & Kvacˇek, 1998). These fossil reproductive structures differ in number of stamens, number of sporangia per anther, in presence/absence of staminodes, and in features of the perianth. The majority have tetrasporangiate anthers, and the oldest Lauraceae-like anther recovered until now is also tetrasporangiate (see Crane et al., 1994). The fossil lauraceous reproductive structures include three dimensional charcoalified specimens as well as compression fossils, and the possibilities for detailed comparisons with other fossils and extant taxa therefore vary. In short, Neusenia tetrasporangiata shows greatest similarity to two Eocene-Oligocene species referred to extant Cinnamomum (Conwentz, 1886) in the number of floral organs and their organization, and in the tetrasporangiate anthers. Taxon A shows some similarity to the mid-Cretaceous genus Mauldinia (Drinnan et al., 1990; Eklund & Kvacˇek, 1998) in the disporangiate anthers and the inflorescence units with crowded, sessile flowers. However, the inflorescence unit of Mauldinia is characterized by being distinctly bilobed and composed of small, distichously arranged leaf-like scales. Because such inflorescence units were not observed in taxon A, it is not assigned to Mauldinia. Taxon B shares the trimerous flower organization and paired staminal appendages with most other fossils, but differs in having distinctly unequal tepals. More detailed comparisons and descriptions are given below. Fossil flowers with tetrasporangiate anthers The majority of the reported lauraceous fossils have tetrasporangiate anthers, and eight species with attached anthers have been described so far (Table 2; Conwentz, 1886; Chaney & Mason, 1933; Weyland, 1938; Taylor, 1988; Crane et al., 1994). The earliest anther with valvate dehiscence is an isolated stamen with four pollen sacs from the Early Cretaceous (Early–Middle Albian) of U.S.A. (Crane et al., 1994). Two amber embedded flowers from the Early Tertiary (Late Eocene–Early Oligocene) were referred to extant Cinnamomum, and are closely similar to Neusenia in having a perianth of six equal tepals in two whorls of three, nine fertile stamens in three whorls of three, paired staminal appendages associated with filaments of third whorl, and a unicarpellate gynoecium (Conwentz, 1886). Compressed flowers from the Early Tertiary (middle Eocene) of U.S.A., described as Androglandula tennessensis (Taylor, 1988), have psilate pollen grains and an unknown number of tetrasporangiate stamens, and may belong to the same species-complex as Neusenia. Other fossils with tetrasporangiate stamens differ from Neusenia in having fewer stamens (Trianthera eusideroxylon Conwentz, 1886; Litseopsis rottensis Weyland, 1938; Umbellularia californica Chaney & Mason, 1933), and in lacking paired staminal

LATE CRETACEOUS LAURACEOUS FLOWERS

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T 2. Summary of all known fossil flowers and flower fragments showing lauraceous features; E C=Early Cretaceous, L C=Late Cretaceous, E T=Early Tertiary, L T=Late Tertiary, Q= Quaternary Taxon

Age

Lauralean stamen Lauralean flower fragment Mauldinia mirabilis

EC EC LC

M. bohemica

LC

Perseanthus crossmanensis

Occurrence

Structure

Reference

Four ? Two

Crane et al., 1994 Crane et al., 1994 Drinnan et al., 1990

Two

LC

Stamen Flower fragment Inflorescence unit with flowers Czech Republic Inflorescence unit with flowers U.S.A. Flower

?

Neusenia tetrasporangiata Lauraceae sp. A

LC LC

U.S.A. U.S.A.

Lauraceae sp. B Androglandula tennessensis Cinnamomum felixii C. prototypum Trianthera eusideroxylon Lindera rottensis Litseopsis rottensis Cinnamomum polymorphum

L E E E E E E L

Umbellularia californica

Q

U.S.A. U.S.A. Baltic (amber) Baltic (amber) Baltic (amber) Germany Germany Switzerland, Germany U.S.A.

C T T T T T T T

U.S.A. U.S.A. U.S.A.

No. sporangia

Flower Inflorescence unit with flowers Flower Flower Flower Flower Flower Flower Flower Flower

Four Two

Eklund & Kvacˇek, 1998 Herendeen et al., 1994 This work This work

? Four Four Four Four Two Four ?

This work Taylor, 1988 Conwentz, 1886 Conwentz, 1886 Conwentz, 1886 Weyland, 1938 Weyland, 1938 Heer, 1856

Flower

Four

Chaney & Mason, 1933

appendages. (T. eusideroxylon) or staminodes (L. rottensis). They probably represent more ‘advanced’ taxa with a more reduced flower organization. Neusenia shares the tetrasporangiate and valvate anthers with the single dispersed lauralean stamen reported by Crane et al. (1994) from the Early Cretaceous Puddledock locality of the Potomac Group, U.S.A. Within extant Laurales tetrasporangiate stamens are restricted to Lauraceae. The Early Cretaceous stamen is differentiated into anther and filament. The anther is tetrasporangiate with pollen sacs in two lateral pairs that open through apically hinged valves. Trichomes are densely spaced on the filaments. The pollen sacs in the Early Cretaceous stamen are more clearly arranged into two lateral pairs than in Neusenia, but in the latter the lower pollen sacs may also have been arranged laterally before fossilization. Neusenia is similar to the middle Eocene flower described as Androglandula tennessensis (Taylor, 1988) in the tetrasporangiate anthers and unsculptured pollen grains. One obvious difference between Neusenia and Androglandula is in the much smaller pollen grains of A. tennessensis. However, due to uncertainty concerning floral organization and number of stamens in Androglandula, a more detailed comparison is not possible. Androglandula tennessensis was described by Taylor (1988) based on eight compressed flowers from the Middle Eocene of Tennessee, U.S.A. Flowers are solitary and pedicellate with a maximum diameter of 5.2 mm. All flowers are glabrous and subtended by a large ovate bract. Parenchymatous tissue throughout the flower has ethereal oil cells with a diameter ranging between 20 and 100 lm. The perianth consists of six equal elliptical-ovate tepals that are fused at the base, forming a hypanthium. The arrangement of tepals indicates that they are in two whorls. The androecium is incomplete, and number of stamens could not be counted. Stamens are short and almost sessile with tetrasporangiate anthers. Some of the stamens have

418

H. EKLUND

glandular appendages adnate to the filaments. Poorly preserved in situ pollen grains are unsculptured, monocolpate and have a diameter of 16 lm. Comparisons with extant Lauraceae showed that Androglandula is most similar to genera within Kostermans’s subtribe Cinnamominae, and in particular to the complex around the genus Ocotea or perhaps Cinnamomum (Taylor, 1988). Because the flower was found isolated and information on inflorescence structure and fruit morphology is wanting, I agree with Taylor (1988) that a more detailed generic affinity is difficult to establish. Three excellently preserved amber-embedded flowers, Cinnamomum felixii, C. prototypum, and Trianthera eusideroxylon, were described by Conwentz (1886) from the Late Eocene–Early Oligocene of the Baltic area. Neusenia shows particularly great similarity to the Cinnamomum felixii flower. Both have a perianth of six almost equal, hairy tepals, an androecium of nine fertile tetrasporangiate stamens, paired glandular appendages associated with filaments of third staminal whorl, and a gynoecium consisting of a single carpel. Differences are in the arrangements of sporangia (two pairs above each other in C. felixii, two lateral pairs in Neusenia) and in the absence of staminodes in C. felixii. Cinnamomum felixii is an isolated bisexual flower. The perianth consists of six tepals in two whorls. Tepals have erect trichomes on both surfaces. The androecium consists of nine stamens in three alternating whorls; filaments of inner whorl have paired staminal glands. Anthers are tetrasporangiate with sporangia arranged in two pairs above each other and dehisce by apically hinged valves; dehiscence is introrse in the two outer whorls and extrorse in the innermost whorl. Filaments and abaxial surface of anthers(?) have erect trichomes. Staminodes were not observed. The gynoecium is a single carpel. Because the floral features of C. felixii are very general within Lauraceae, the generic assignment must be regarded as doubtful. The absence of staminodes is aberrant with respect to Cinnamomum and many other lauraceous genera. Apart from the absence of staminodes the same character combination as in C. felixii is also present in flowers of Alseodaphne, Caryodaphnopsis, Nectandra, Neocinnamomum, Notaphoebe, Ocotea, Persea, and Phoebe. In Notaphoebe staminodes are small and in Ocotea they may be absent. Without knowledge of inflorescence structure and fruit morphology, it is not possible to establish which extant genus is closest to the fossil, but its nearest affinity is probably among the genera listed above. Neusenia also shows close similarity to Cinnamomum prototypum Conwentz (1886). Since C. prototypum has staminodes, the main difference from Neusenia is in the arrangement of the sporangia. Cinnamomum prototypum has the same flower organization as C. felixii, but is smaller and has three scaly staminodes in an inner fourth staminal whorl. It further differs in having erect trichomes on inner surface of tepals only, and a different stigma shape. The assignment of C. prototypum to Cinnamomum is considered doubtful for the same reasons that the generic assignment of C. felixii was questioned (see above). Neusenia is similar to Trianthera eusideroxylon, the third flower from the Baltic amber, in the indumentum of tepals and in the tetrasporangiate anthers Conwentz (1886). T. eusideroxylon differs, however, in number of fertile stamens, in the apparent lack of glandular staminal appendages, and in the large and three-parted stigma. The genus Trianthera was established by Conwentz (1886) to accommodate lauraceous bisexual, glandless flowers, very similar to the extant genus Eusideroxylon, but differing in morphology of the style. The isolated flower is bisexual, 3 mm long and has a 3.5 mm long pubescent pedicel. The perianth consists of six oblong-lanceolate tepals in two subequal whorls of three; all tepals are hairy on both surfaces, and tepals of

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outer whorl are shorter than inner tepals. The androecium has three fertile stamens and nine staminodes; the first and second androecial whorls consist of staminodes, the third of stamens, and the inner fourth of minute scale-like staminodes. Anthers are tetrasporangiate with sporangia in two pairs above each other; dehiscence is extrorse through apically hinged valves. There is no information about staminal appendages. The gynoecium consists of a single carpel with a short style and a large three-part stigma. Among extant Lauraceae eight genera have flowers with only three stamens (Rohwer, 1993). Of these, Gamanthera van der Werff is unisexual and has stamens that are united to a synangium, while Aiouea Aubl., Aspidostemon Rohwer & H.G. Richt., Endiandra R. Br., Licaria Aubl., and Mezilaurus Kuntze ex Taubert has disporangiate anthers. Thus, only Eusideroxylon Teijsm. & Binnend. and Williamodendron compare to the fossil in both number of stamens and pollen sacs. In Williamodendron the four pollen sacs are arranged in two apical pairs, and in Eusideroxylon in a subapical row. While tepals in Eusideroxylon are equal, outer tepals are smaller than inner tepals in Williamodendron. Staminal appendages are inconspicuous in Eusideroxylon and wanting in Williamodendron. Staminodes occur in fourth whorl in Williamodendron, and in first, second and fourth whorls in Eusideroxylon. Taken together, the fossil flowers share the unequal tepals with Williamodendron, while most other floral characters seem to indicate closer relationship with Eusideroxylon. Neusenia is similar to the Late Oligocene flower described as Litseopsis rottensis (Weyland, 1938) in its bisexual nature and the perianth with six almost equal tepals (equal in L. rottensis, outer tepals slightly shorter in Neusenia), and the tetrasporangiate anthers. Differences are, however, in the number of fertile stamens (six in L. rottensis, nine in Neusenia), and the absence of (reported) staminodes in L. rottensis; based on the information in Weyland (1938), the two fossil species do not seem to be particularly closely related. Litseopsis rottensis was described by Weyland (1938) based on a compressed flower from the Late Oligocene of Germany. Weyland (1938) introduced this fossil genus to accommodate fossil lauraceous flowers with six tetrasporangiate valvate anthers. Because of the compressed state of preservation, details of flower organization could not be studied. The flower is isolated and probably bisexual, although Weyland (1938) pointed out that the structure interpreted as the gynoecium could also be simple debris. The six stamens are tetrasporangiate with sporangia arranged in two pairs above each other; the distal valves are smaller than the proximal ones. Dehiscence is through apically hinged valves. Some stamens have appendages adnate to the lower parts of the filaments. Among extant genera the combination of six stamens with tetrasporangiate anthers occurs regularly in Dicypellium (always six fertile stamens), and occasionally in Beilschmiedia Nees, Cinnamomum, Persea, and Phoebe (Rohwer, 1993). In Neolitsea male flowers may have six tetrasporangiate stamens that are arranged in two pairs above each other. Although flowers of Dicypellium have the same number of stamens and pollen sacs as the fossil, they differ in that the first staminal whorl is transformed into a third whorl of tepals, and the pollen sacs are arranged in an arc. Neusenia shares tetrasporangiate anthers with the Quaternary flower referred to the extant species Umbellularia californica (Hook. & Arn.) Nutt. (Chaney & Mason, 1933). Fossil U. californica, which was described from the Pleistocene asphalt deposits in California otherwise differs from all Neuse River flowers in most respects. Chaney and Mason (1933) described the flower as being perigynous and pedicellate with a six-lobed and undifferentiated perianth. The androecium has two whorls of stamens; the outer stamens are shorter than the inner stamens and have paired glands

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associated with the filaments. Anthers dehisce through two pairs of lateral pores (valves?). The gynoecium consists of a single carpel with an apically curved style. In my view the description and illustration by Chaney & Mason (1933) provide too little information on floral structure and organization for comparing the fossil specimen with an extant species. Comparison of the fossil flower with extant Umbellularia californica shows that differences are in number of androecial whorls (two in the fossil, four in U. californica), position of glandular appendages (first whorl in the fossil, third stamen whorl in U. californica), and arrangement of pollen sacs (two pairs above each other in the fossil, two lateral pairs in U. californica). Fossil flowers with disporangiate anthers The fossil record of lauraceous flowers includes four species with disporangiate anthers (Table 2; Weyland, 1938; Drinnan et al., 1990; Eklund & Kvacˇek, 1998). Three species are referred to the mid-Cretaceous genus Mauldinia (Drinnan et al., 1990; Eklund & Kvacˇek, 1998; Frumin, Eklund & Friis, unpublished work), and have flowers with a ‘complete’ flower organization (i.e. two perianth whorls with three tepals each, four androecial whorls with nine fertile stamens in three whorls of three and one inner whorl with three staminodes, and one central carpel). Taxon A (see pp. 403–406) shows some similarity to Mauldinia in having inflorescence units with sessile and densely spaced flowers, but lacks the bilobed flower-bearing structures characteristic of Mauldinia and is therefore not assigned to this genus. Compressed flowers from the Early Tertiary (Late Oligocene) of Germany, described as Lindera rottensis (Weyland, 1938), are unisexual, pedicellate, and arranged in three-flowered inflorescence units. Based on the fossil record it seems that the earliest, Cretaceous taxa with disporangiate stamens had sessile flowers arranged in inflorescence units unknown among extant taxa. The later, Tertiary, species appears more derived with pedicellate and reduced (unisexual) flowers. Neusenia shares the ‘complete’ flower organization with Mauldinia (Drinnan et al., 1990). Otherwise, the differences in number of sporangia and inflorescence structure (i.e. sessile versus pedicellate flowers), indicate that closer relatives to Neusenia can be found among extant Lauraceae. Taxon A shows some similarity to Mauldinia in the disporangiate anthers, the small inflorescence units with sessile, crowded flowers, and the tepal apices with conspicuous perforations. However, the distinctly bilobed nature of the flower-bearing inflorescence units of Mauldinia was not observed in taxon A. Further, in taxon A flowers are borne at the same height, whereas in Mauldinia proximal flowers are borne more basally on the bilobed inflorescence units than distal flowers. Mauldinia, which was originally described from the Cenomanian of the Potomac Group, Maryland, U.S.A. (Drinnan et al., 1990), is a distinct lauraceous element in the Cenomanian floras of the Northern Hemisphere. Mauldinia has been recovered from other localities in North America, Europe and Asia as well (Eklund & Kvacˇek, 1998; Frumin, Eklund & Friis, unpublished work; Herendeen et al., 1999). The fossil plant described as Prisca reynoldsii Retallack & Dilcher (1981) shows close similarity to Mauldinia in many respects, and the two taxa may in fact be congeneric. However, the material on which the reconstruction and interpretation of Prisca is based consists mainly of impression fossils and incompletely preserved compressions, and until more well preserved material is available the two genera are better kept separate. Flowers of Mauldinia are closely similar to flowers of extant Lauraceae, showing the unique combination of a trimerous flower organization with

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six tepals in two whorls, nine fertile stamens in three whorls, an inner fourth whorl of staminodes, paired glandular appendages adnate to the filaments of the third staminal whorl, and a unilocular uniovulate ovary. Anthers are disporangiate and dehisce introrsely in the first two staminal whorls and extrorsely in the third staminal whorl. The inflorescence structure of Mauldinia is, however, complicated and not found among extant Lauraceae. In Mauldinia, bilobed lateral inflorescence units are spirally arranged along elongated inflorescence axes. Each lateral inflorescence unit bears (three-)five-seven(-nine) sessile flowers, and appears to be derived from a dichasial-monochasial branching system through condensation of internodes and fusion of branches at an early ontogenetic stage (see Eklund & Kvacˇek, 1998). The resulting flower-bearing structure is apparently composed of closely spaced and distichously arranged small leaf-like scales. Because a similar inflorescence structure was not observed in taxon A, it is not assigned to Mauldinia. Taxon A from Neuse River is comparable to the Late Oligocene flower described as Lindera rottensis (Weyland, 1938) in the 3-flowered inflorescence units and disporangiate anthers. However, while flowers are completely sessile in the former species they are distinctly pedicellate in the latter. The two fossil species further differ in the unisexual (L. rottensis) and bisexual flowers (taxon A). Lindera rottensis was described based on compressed flowers from the Late Oligocene of Germany (Weyland, 1938). The flowers are unisexual, and only male flowers were observed. An inflorescence fragment with three flowers shows that flowers are pedicellate and attached at the same node, forming a loose umbel. The perianth consists of six equal tepals with dense ethereal oil cells. The androecium consists of six stamens with disporangiate and valvate anthers. Six staminal glands were observed around the filament bases; probably they are paired and associated with three of the filaments. The combination of unisexual flowers with six disporangiate stamens is unusual within Lauraceae. In the unisexual genus Iteadaphne Blume, which is sometimes included in Lindera Thunb., male flowers have 6–9 stamens, but this genus differ from the fossil in having inflorescence units with a single flower. In Lindera flowers have 9–15 fertile stamens, and are arranged in 3–15 flowered pseudo-umbels (Rohwer, 1993). Although it is difficult to judge without studying the material personally, Weyland (1938) seem to be correct in comparing the fossil to Lindera. Lauralean/lauraceous flowers without preserved anthers Four fossil flowers with lauraceous (or lauralean) features, but lacking attached anthers have been reported (Table 2; Heer, 1856; Crane et al., 1994; Herendeen et al., 1994). Because the classification of the Lauraceae followed here is based mainly on inflorescence type, presence/absence of involucre of bracts subtending inflorescence units, and the direction of anthers of the third whorl (Rohwer, 1993), it is extremely difficult to establish the affinities of these fossils. Flowers of the most well preserved species, Perseanthus crossmanensis Herendeen et al. (1994), have a ‘complete’ flower organization, but although the anthers are wanting, spinulose pollen grains were observed on the carpel and filament bases. The pollen grains may, provided that they actually belong to the flower, give some indications about the affinity of Perseanthus, but since spinulate pollen occurs both in taxa with tetrasporangiate and disporangiate anthers (van der Merwe et al., 1990), this species is discussed with the other fossils lacking anthers. The Neuse River flowers differ from the two Early Cretaceous lauralean flower

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fragments reported by Crane et al. (1994) in the morphology of the glandular head of the staminal appendages and the attachment of their stalks. In the Early Cretaceous flower fragments, the stalks of the staminal appendages are fused to the floral cup, while in the younger Neuse River flowers, the staminal appendages are adnate to the filaments. The lauralean flower fragments were recovered from the Early Cretaceous Puddledock locality of the Potomac Group, U.S.A. (Crane et al., 1994). One of the fragments shows remnants of three tepals with filaments and staminal appendages attached, similar to members of the Atherospermataceae, Hernandiaceae, Lauraceae, and Monimiaceae, but the lack of anthers and gynoecial characters prevents a more detailed comparison with these extant taxa. It is, however, interesting to note that trimerous flowers with staminal appendages were present in the Early Cretaceous. Neusenia is similar to the Late Cretaceous flower Perseanthus crossmanensis (Herendeen et al., 1994) in the ‘complete’ flower organization, but differs in perianth structure and pollen morphology. This flower organization is very common within the family, and cannot provide much evidence of the degree of closeness. Perseanthus crossmanensis was described based on dispersed flowers from the Late Cretaceous (Turonian) of North America (Herendeen et al., 1994). Flowers are bisexual, trimerous and incompletely preserved at the base. The perianth consists of six tepals arranged in two whorls of three; outer tepals are shorter than inner tepals. Tepals are basally fused for about 0.2 mm, forming a short hypanthium. Abaxial surface of tepals has dense trichomes; adaxial surface is glabrous. Androecium consists of nine stamens in three whorls of three, and an inner whorl of three smaller staminodes. Anthers are wanting. Filaments of third whorl have staminal appendages attached near the base. The gynoecium consists of a single superior and unilocular carpel with a single ovule. The carpel surface is densely covered with simple trichomes. Inaperturate, spheroidal pollen grains with a spinulate surface ornamentation were found among the trichomes on the carpel and filament bases. Similar pollen grains occur in some extant lauraceaeous taxa, but it cannot, however, be completely excluded that the fossil grains do not belong to the Perseanthus flower. Herendeen et al. (1994) compared P. crossmanensis with flowers of extant Lauraceae and found closest similarity to Persea, Alseodaphne, Caryodaphnopsis, and Dehaasia, all of which belong to the tribe Perseeae. Herendeen et al. (1994) concluded that while pollen structure indicates a close relationship of Perseanthus with Caryodaphnopsis, perianth structure differs between these genera, and except for pollen structure Perseanthus shows closest similarity to Persea. Herendeen et al. (1994) did not demonstrate unequivocally that Perseantus belongs to tribe Perseeae. Flowers of Perseanthus agree with flowers of the isolated genus Mauldinia, for example, in all characters except the distribution of trichomes on tepals and pollen morphology (unknown in Mauldinia). Therefore, additional information on Perseanthus (e.g. on inflorescence structure, anthers etc.) is needed until reliable systematic affinities can be established. Neusenia shows some similarity to the Late Tertiary flower described as Cinnamomum polymorphum (A. Braun) Heer (1856) in the perianth consisting of six equal tepals. However, this feature is widespread within the family and no other characters indicate a close relationship between the two fossil species. Cinnamomum polymorphum was described based on compressed flowers from the Early to Late Miocene of Switzerland and Germany (Heer, 1856). The material includes open, isolated flowers and branches with racemose inflorescences in bud stage and attached leaves. Open flowers are about 7–8 mm in diameter and have six tepals in two whorls. According

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to the illustrations the androecium consists of six stamens, and the gynoecium of a single carpel. Although both leaf morphology and general features of flowers seem to be in accordance with a lauraceous affinity of the fossil taxon, the description and illustration provided by Heer (1856) include too few details for making comparisons with extant genera. Are disporangiate or tetrasporangiate anthers the plesiomorphic condition in Lauraceae? Based on the occurrence of tetrasporangiate anthers in most taxa with a ‘complete’ flower organization (i.e. two perianth whorls with three tepals each, four androecial whorls with nine fertile stamens in three whorls of three and one whorl with three staminodes, and one central carpel), Rohwer (1993) suggested that the presence of tetrasporangiate anthers was the plesiomorphic condition in the Lauraceae. Later he discussed the possibility that disporangiate anthers could be the plesiomorphic state in the family (Rohwer, 1994). He based this discussion on the observation that all close outgroups with valvate dehiscence have disporangiate anthers (i.e. Atherospermataceae, Siparunaceae, Gomortegaceae, Hernandiaceae), and that the Cenomanian Mauldinia has disporangiate anthers. New fossil material, however, indicates that lauralean plants with tetrasporangiate valvate anthers were established in the Early Cretaceous (early-mid Albian?) before the appearance of Mauldinia in the Cenomanian (see Crane et al., 1994). The Early Cretaceous tetrasporangiate anther differs from extant species of Lauraceae in having the sporangia arranged in two lateral pairs which may indicate a derivation of the lauraceous anthers from ‘ordinary’ dithecate, tetrasporangiate anthers with slit-like dehiscence. A recent phylogenetic analysis of Laurales based on morphological and molecular data shows that Lauraceae are sister to Monimiaceae (Renner, in press; Fig. 45). Monimiaceae have tetrasporangiate anthers that dehisce through longitudinal slits; the stomium may bifurcate at both ends resulting in a saloon door-like opening of the theca (Endress & Hufford, 1989). Renner’s phylogenetic analysis further indicates that Calycanthaceae are the first family branch of Laurales (Fig. 45). Calycanthaceae have tetrasporangiate anthers dehiscing through longitudinal slits and since this feature occurs also in other magnoliids outside the Laurales it appears to be the plesiomorphic state in the order. Based on these results it is suggested here that an early event in the lineage leading to the Lauraceae–Monimiaceae– Hernandiaceae– Atherospermataceae–Gomortegaceae–Siparunaceae clade involved a change from slit-like to valvate dehiscence, resulting in the exposure of the two pollen sacs of each theca by the opening of a single apically hinged valve (Fig. 46 a–b1). Such tetrasporangiate bivalvate anthers occur in the extant lauraceous species Brassiodendron fragrans C.K. Allen and in several species of Endiandra R.Br. (Rohwer, 1994). In these species the valves sometimes show a median longitudinal furrow that may represent a former stomium (Rohwer, 1994). In the hypothesis described here fusion of the two pollen sacs of each theca by reduction of the septa resulted in disporangiate anthers opening by two apically hinged valves (Fig. 46 b1–b3). The anthers of the Hernandiaceae, Atherospermataceae, and Gomortegaceae, and perhaps some lauraceous taxa are here interpreted as having evolved in this way (Fig. 45). It may be pointed out here, that in the Hernandiaceae, in addition to the taxa with disporangiate anthers opening by two apically hinged valves (i.e. Gyrocarpus Jacq. Hazomalania Capuron, Sparattanthelium C. Mart.), most species of Hernandia L. and all

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Figure 45. Phylogenetic relationships within Laurales with hypothesized anther evolution; the tree is redrawn from S. Renner (in press) and represents the strict consensus of four most parsimonious trees resulting from an analysis including 27 taxa and sequences from six plastid genome regions (rbcL, rpl16, trnT-trnL, trnL-trnF, atpB-rbcL, and psbA-trnH). (Ε) Apomorphies without reversals; (Φ) apomorphies that reverse; (||) parallelisms; (×) reversals; letters and numbers as in Fig. 46)

species of Illigera Blume have theca that open by lateral valves that are attached on the dorsal side of the anther (Endress & Hufford, 1989; S. Renner, in press; Fig. 46 b4). Anthers of Siparunaceae, which have two pollen sacs that are exposed by the opening of a common valve, may have originated from a tetrasporangiate 2-valvate anther through reduction of one theca (Figs 45, 46, b1–b2). Reversal of dehiscence mode back to longitudinal slits would result in the tetrasporangiate anthers of the

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Figure 46. Hypothetical derivation of the different anther types in Laurales from a dithecate tetrasporangiate anther dehiscing through longitudinal slits. (a) Dithecate, tetrasporangiate anther with slitlike dehiscence; (b1) dithecate, tetrasporangiate anther dehiscing through two apically hinged valves (e.g. Brassiodendron fragrans, several species of Endiandra); (b2) disporangiate anther dehiscing through a single apically hinged valve (Siparunaceae); (b3) disporangiate anther dehiscing through two apically hinged valves; (b4) disporangiate anther dehiscing through two lateral, dorsally attached valves (e.g. Hernandia, Illigera); (c) tetrasporangiate anther dehiscing through four apically hinged valves (e.g. Eusideroxylon and Nectandra); (d) tetrasporangiate anther with two larger lateral and two smaller median sporangia that dehisce through four apically hinged valves (e.g. Neusenia tetrasporangiata); (e1) tetrasporangiate anther with sporangia arranged in two pairs above each other, dehiscing through four apically hinged valves (e.g. Cinnamomum and Ocotea); (e2) disporangiate anther dehiscing through two apically hinged valves (e.g. Cryptocarya and Laurus). Reversal of dehiscence mode from b2 (apically hinged valves) to b1 (longitudinal slit) would result in a monimiaceous anther.

Monimiaceae (Figs 45, 46 b1–a). In the Lauraceae anthers with four separate pollen sacs probably evolved from tetrasporangiate anthers with bivalvate dehiscence as the septa separating the pollen sacs became stronger (Rohwer, 1994). This event must have co-occurred with division of each valve into two, resulting in anthers with four equal and collateral pollens sacs (Fig. 46 b1–c). Such anthers occur, for example, in extant Eusideroxylon and Nectandra (both Lauraceae). Reduction in size of the two median pollen sacs would have resulted in an anther similar to that in Neusenia tetrasporangiata (Fig. 46 c–d). Finally, while spatial separation of the two median pollen sacs to a more distal position (Fig. 46 d–e1) would have resulted in anthers similar to those found in, for example, Cinnamomum and Ocotea of Lauraceae, reduction of the two median pollen sacs (Fig. 46 d–e2) would have resulted in disporangiate 2-valvate anthers similar to those found in, for example, lauraceous

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Cryptocarya and Laurus (Figs 45, 46 d–e1, e2). The hypothesis suggested above may be confirmed or rejected by future results from phylogenetic investigations and palaeobotanical work.

CONCLUSIONS

The Late Cretaceous flowers described here include both a tetrasporangiate (Neusenia tetrasporangiata; Figs 1–20) and a disporangiate (taxon A; Figs 21–37) form. Both types were established very early in the history of the family with the Cenomanian genus Mauldinia being the earliest fossil form with disporangiate anthers (Drinnan et al., 1990; Eklund & Kvacˇek, 1998). The tetrasporangiate state, which may be plesiomorphic in the family (see above) is, however, known from older strata (Early-Middle Albian; Crane et al., 1994). The lauraceous fossils described in this work show combinations of features that are known in extant taxa (e.g. flower organization of Neusenia, valvate dehiscence in Neusenia and taxon A, staminal appendages in Neusenia and taxon B) and features that are unique in the family (e.g. inflorescence structure in taxon A). Future fossil findings may, together with more detailed studies of extant taxa, reveal additional character combinations that can facilitate the understanding of the relationships and evolution within the Lauraceae. In the light of the difficulties at present in resolving the family’s phylogeny based on morphology and genetics ( J. Rohwer, pers. comm.) such palaeobotanical work and detailed morphological studies of extant taxa may turn out to be utterly important for reaching further progress.

ACKNOWLEDGEMENTS

I am grateful to E.M. Friis (Stockholm) and F.M. Hueber (Washington D.C.) for providing access to the fossil material; E.M. Friis is also thanked for valuable discussions and support during the progress of the work, and for reading the manuscript several times. K. Bremer (Uppsala), J.G. Rohwer (Mainz), and S.S. Renner (St. Louis) are thanked for helpful comments on the manuscript, A. Anderberg (S-herbarium, Stockholm) for providing access to herbarium material, N. Laurent (Stockholm) for helpful discussions, J. Scho¨nenberger (Stockholm) for introducing me to Photoshop work, and Y. Arremo (Stockholm) for help with preparations for SEM. Finally, K. Khullar (Stockholm) is thanked for help with practical matters. Support from the Hierta-Retzius Stipendiefond and the Swedish Natural Science Research Council (NFR) is gratefully acknowledged.

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