Available online at www.sciencedirect.com

R

Review of Palaeobotany and Palynology 126 (2003) 103^129 www.elsevier.com/locate/revpalbo

The in situ Glyptostroboxylon forest of Hoegaarden (Belgium) at the Initial Eocene Thermal Maximum (55 Ma)

M. Fairon-Demaret a;Ã, E. Steurbaut b, F. Damblon b, C. Dupuis c, T. Smith b, P. Gerrienne a

a Universite¤ de Lie'ge, De¤partement de Ge¤ologie, Pale¤obotanique et Pale¤opalynologie, Alle¤e du 6 Aou“t, Ba“timent B18, B-4000 Lie'ge, Belgium b Institut royal des Sciences naturelles de Belgique (IRSNB), De¤partement de Pale¤ontologie, 29, rue Vautier, B-1000 Brussels, Belgium c Faculte¤ Polytechnique de Mons, Ge¤ologie Fondamentale et Applique¤e, 9, rue de Houdain, B-7000 Mons, Belgium

Received 19 June 2002; accepted 6 March 2003

Abstract

Hundreds of silicified standing stumps have been discovered within a lignitic horizon in the middle of the Tienen Formation near Hoegaarden in northeast Belgium. The anatomical features of the fossil stumps, as those of the numerous silicified secondary xylem remains collected since the last century from this area, demonstrate that they all belong to a single taxodiaceous taxon. The stumps bear characteristics shared by Taxodioxylon gypsaceum and Glyptostroboxylon tenerum, but affinities with the latter appear closer. They are attributed to Glyptostroboxylon sp. Calibration of the sedimentological, stratigraphical and organic carbon isotope data reveals that these taxodiaceous fossil trees developed in a swampy lowland environment most probably during the Initial Eocene Thermal Maximum at ca. 55 Ma. ß 2003 Elsevier B.V. All rights reserved.

Keywords: Early Eocene; fossil wood; gymnosperm; Glyptostroboxylon; taphonomy; Belgium

1. Introduction more proximal continental settings known as the Dormaal Sands, is extremely rich in remains of The Tienen Formation, occurring throughout land mammals (Smith and Smith, 1996; Smith northern Belgium and in the east of the Mons et al., 1999; Steurbaut et al., 1999; Smith, Basin (Steurbaut, 1998), has been intensively 2000). Records of land plant macro-remains studied in recent years because of its position from the Tienen Formation are relatively rare, close to the Palaeocene/Eocene boundary (Steur- and usually consist of secondary xylem fragments baut et al., 1999, 2000, in press). Its base, in the (Stockmans and Willie're, 1934; Doutrelepont et al., 1997). Current palaeobotanical information is mostly based on palynological analyses (e.g. * Corresponding author. Fax: +32-4-366-5338. Roche in Steurbaut et al., 1999, and in Steurbaut E-mail address: [email protected] et al., in press), providing a generalised, homoge- (M. Fairon-Demaret). neous picture of the vegetation. Noticeable excep-

0034-6667 / 03 / $ ^ see front matter ß 2003 Elsevier B.V. All rights reserved. doi:10.1016/S0034-6667(03)00062-9

PALBO 2534 15-8-03 Cyaan Magenta Geel Zwart 104 M. Fairon-Demaret et al. / Review of Palaeobotany and Palynology 126 (2003) 103^129

very complex and needs some more detail. Unit 4, made up of 0.5 m of leached whitish sands, locally includes quartzitic silcretes (‘quartzite d’Overlaar- lez-Tirlemont’ of Ledoux, 1910). Occasional root casts with unidenti¢able structure are observed perforating this thick but discontinuous white, massive sandstone layer with a bumpy upper sur- face. The embedding whitish sands are devoid of organic remains. Unit 5 consists of a 45-cm-thick layer of heterogeneous more or less lignitic depos- its, enclosing the stumps and showing demonstra- Fig. 1. Geographical location of the localities mentioned in tive compaction patterns. It includes in ascending the text, especially of the Goudberg Section (black star). order (Fig. 3): (1) 5.1a, a basal layer with dark lignite wrapping the bases of the trunks (Plate I); (2) 5.1b, small sandy lenses interstrati¢ed with lignitic layers towards the base, and with brown tions are the angiosperm leaf assemblage of Leval to grey clay towards the top; (3) 5.1c, grey^brown described by Marty (1907), which is in need of strati¢ed clay with tiny black pieces of fusain; revision in the light of modern concepts of foliar (4) 5.2, an intermediary clay layer with a more morphologies, and the seeds and fruits recently or less breccia-like texture, underlain by a white described from Dormaal (Fairon-Demaret and band progressively becoming grey^blue and dark- Smith, 2002). Here we report the discovery of er, and towards the top interstrati¢ed with small, an exceptional apparently monospeci¢c fossil for- millimetre-thick lenses of brown clay; (5) 5.3, an est at Goudberg^Hoegaarden, 3 km southwest of upper light grey to brown clayey layer capped by Tienen, in the Belgian province of Vlaams-Bra- 2^3 cm of dark brown clay with numerous root bant (Fig. 1). Hundreds of silici¢ed stumps are departures; and (6) 5.4, 17 cm of blackish silt. preserved in situ within a lignitic horizon (unit Unit 6 consists of an about 45-cm-thick layer of 5) in the middle of the Tienen Formation, in an brown sandy to silty mud with in the middle 10 area extending over more than one hectare. cm of greyish clayey silt with a black organic-rich base. It is overlain by unit 7, consisting of a 5-cm- thick layer of white clayey silt, locally ¢nely lami- 2. Geographical setting and lithological description nated. The succession is not always entirely preserved The stumps were exposed during excavations along the excavation front because of subsequent for the new High Speed Train railway track at local erosion. Units 6 and 7, next to the upper 17 Goudberg^Hoegaarden, extending parallel to the cm of unit 5 were missing in the eastern part of Lie'ge/Brussels E40 motorway (50‡47P27.4QN, the excavation, reducing the thickness of the Tie- 04‡54P06.1QE; altitude: 55 m; Institut Ge¤ogra- nen Formation by about 65 cm. phique National Map 32/7^8: coordinates x = 187, y = 164; Figs. 1 and 4). An 8-m-thick section has been exposed (Figs. 2 and 3). Its upper part, 3. Stratigraphy and age of the fossil forest down to the fossil-tree-bearing lignite, was seen in outcrop and the lower part in a series of 3-m-deep The stratigraphical interpretation of the di¡er- temporary trenches dug out at the railway track. ent units of the Goudberg Section is exclusively This composite pro¢le, known as the Goudberg based on lithofacies analysis, as the entire section Section, consists of nine distinct units, of which is devoid of stratigraphically diagnostic microfos- the lithological description is given in Fig. 2. The sils (no dino£agellate cysts and calcareous micro- middle part of the section, including units 4^7, is fossils; a few pollen, spores and freshwater algae

PALBO 2534 15-8-03 Cyaan Magenta Geel Zwart M. Fairon-Demaret et al. / Review of Palaeobotany and Palynology 126 (2003) 103^129 105

Fig. 2. Lithology of the Goudberg Section with position of the silici¢ed stumps; compare with Fig. 3.

PALBO 2534 15-8-03 Cyaan Magenta Geel Zwart 106 M. Fairon-Demaret et al. / Review of Palaeobotany and Palynology 126 (2003) 103^129

Fig. 3. Field picture of units 4^8 (photograph by Professor N. Vandenberghe).

PALBO 2534 15-8-03 Cyaan Magenta Geel Zwart M. Fairon-Demaret et al. / Review of Palaeobotany and Palynology 126 (2003) 103^129 107

(Botryococcus sp.) were found in the top of unit In the most complete settings of northwest Bel- 8; see Fig. 2 for location of samples). It includes gium (Knokke area), the Tienen Formation is un- identi¢cation of the lithofacies characteristics, conformably overlain by the Zoute Silt Member, trends and junctions, and relies on the lithostrati- the lowermost member of the Kortrijk Clay For- graphical classi¢cation of Steurbaut (1998), taking mation (Steurbaut, 1998; Moorkens et al., 2000). into account previous studies carried out in the The latter is part of the Ypresian stratotype. The Tienen area by Rutot (1887), Van den Broeck Zoute Silt Member, through calibration known to and Rutot (1894) and Gulinck (1948). be deposited within Biochron NP 10, posterior to The glauconitic obliquely laminated sands of the well-known Apectodinium acme, is missing in unit 1 are attributed to the Hoegaarden Sands, a the Goudberg Section. Instead, a clayey unit oc- not yet o⁄cially de¢ned term for the estuarine curs (unit 8), which on the ground of its geometry sands occurring in the Hoegaarden area (Steur- and lithofacies may belong to the Kortrijk Clay baut, study in progress). These sands are sand- Formation. The overlying unit 9, of which several wiched between the Upper Thanetian Grandglise metres are locally preserved, is incorporated in the Sands and the Tienen Formation. They are a lat- Brussel Formation (Sintubin et al., 2000). eral equivalent of the fully marine (infralittoral) The lignite of the Goudberg Section in which Bois-Gilles Sand Formation, cropping out in the the fossil stumps were found does not contain any southwest of Belgium and calibrated with the biostratigraphical marker. However, its age can middle part of Biochron NP 9 (Steurbaut, 1998), be reliably inferred from organic carbon isotope dated at 55.8 Ma (Berggren et al., 1995). analysis. The isotope values measured in the The overlying interval, ranging from unit 2 to Goudberg lignite present a trend towards more unit 7, is marked by an essentially £uviatile depo- positive values from 325.7x to about 325.0x sitional regime. Units 3 and 4 represent palaeo- PeeDee Belemnite (Magioncalda, pers. commun.). sols. The white clean sands of unit 4 are due to The same isotopic trend and values are recorded intense leaching of a soil pro¢le in a well-drained, at ¢ve stratigraphically distinct places in the Mont warm, wet environment. Units 5 and 6 represent Bernon Group of the Cap d’Ailly Section in the peat swamp environment that developed as northern France, just below the lignitic complex subsidence caused regional rising of the water ta- L1, in its lowermost part (L1a), at its top (L1c), bles, whereas unit 7 is thought to be lacustrine. within unit SP3 and within unit SP4, respectively The palaeoenvironmental characteristics of this (Magioncalda et al., 2001a,b). However, compar- essentially £uviatile interval, its heterogeneity ison with the isotope curves of the Kallo and Doel and the presence of intraformational lignite refer boreholes, 75 km northwest of the Hoegaarden to the Tienen Formation. Lignite beds are known area (Steurbaut et al., in press), suggests that the to occur in many sections of the Tienen Forma- third option is the most plausible one, and that tion (e.g. in northern Belgium in an essentially the Goudberg lignite should be correlated with lagoonal context; see Steurbaut et al., in press) lignite L1c of the Cap d’Ailly Section and with and its correlatives in northern France (the the lignitic interval L in the middle of the Tienen Mont Bernon Group; Dupuis et al., 1998; Magi- Formation at Kallo and Doel. The pollen and oncalda et al., 2001a) and in southern England spore records support this correlation. The lignitic (the Woolwich Formation; Bone, 1986; Ellison interval encountered at Kallo and Doel and those et al., 1994). In proximal settings (e.g. at Dor- from other localities in the vicinity of Hoegaarden maal) these lignites overlie sandy deposits belong- (Loksbergen, Budingen) contain similar palyno- ing to the Dormaal Sand Member (Steurbaut et morph associations, marked by the highest occur- al., 1999). This member, at the base of the Tienen rence of Subtriporopollinites magnoporatus tecto- Formation, is often rich in mammal remains, rep- psilatus, by the presence of Intratriporopollenites resenting the well-known Dormaal mammal fauna microreticulatus and I. pseudoinstrictus, and by (Steurbaut et al., 1999; Smith et al., 1999; Smith, the absence of Subtriporopollenites spissoexinus 2000). (Hauregard, 1999; Ostojski, 2001). As a conse-

PALBO 2534 15-8-03 Cyaan Magenta Geel Zwart 108 M. Fairon-Demaret et al. / Review of Palaeobotany and Palynology 126 (2003) 103^129

PALBO 2534 15-8-03 Cyaan Magenta Geel Zwart M. Fairon-Demaret et al. / Review of Palaeobotany and Palynology 126 (2003) 103^129 109 quence, these lignite levels are believed to be con- lying white sands located above a sandstone layer. temporaneous or only slightly di¡erent in age. As early as 1887, Rutot discussed the origin of the Carbon isotope shifts from 326.0x to ‘fossil forest of Overlaar’. In his opinion it repre- 325.0x are known to occur within the organic sented the remnants of an in situ forest that had Carbon Isotope Excursion (CIE) in terrestrial, la- been growing in a littoral, swampy environment. goonal, as well as marine settings (Steurbaut et Quickly a controversy arose about the ‘in situ’ al., in press; Magioncalda et al., 2001a, and un- position of the ‘fossil forest’. Stainier (1909) put published research). Estimates for CIE duration forward several observations justifying the al- vary greatly (Norris and Ro«hl, 2000), although lochthonous character of the stumps that would recent high-resolution studies point to a duration have been transported by £uvial currents before of ca. 84 000 years, ranging from 55.50 to 55.41 deposition. He particularly pointed out the ab- Ma using the age model of Bains et al. (1999) and sence of appreciable lengths of anchoring organs, from 55.00 to 54.92 Ma using the model of Bowen and the presence of big root departures only at et al. (2001, ¢g. 7). The base of the CIE has re- the base of the stumps. He also noticed a relation- cently been chosen as the criterion for the Palaeo- ship between the shape of the tree fragments and cene/Eocene boundary (Luterbacher et al., 2000). their orientation in the embedding matrix: cylin- Integration of these data indicates that the fossil drical trunks, which are the longest, were found in trees of Hoegaarden probably developed during horizontal position while the conically shaped the Initial Eocene Thermal Maximum (IETM, ones with a wide, spreading base were found formerly LPTM) about 55 Ma, when climate standing. As the centre of gravity of such conical was the warmest of the entire Cenozoic (Koch stumps is lower than their centre of ¢guration, et al., 1992; Norris and Ro«hl, 1999). According they could well have been carried upright in mud- to Godinot (2000), based on data from Besse and £ows and have consequently been deposited up- Courtillot (1991), the Hoegaarden forest was sit- right. On the other hand, Ledoux (1910) argued uated at a palaeolatitude of approximately 40‡N. that these stumps were never seen prostrate or gathered into irregular piles, one above another, as a consequence of £ood rafting and accumula- 4. Historical background tion. As the distances between adjacent stumps were similar to those observed in a present-day Silici¢ed pieces of secondary xylem have been forest, he claimed that the fossil trees of Overlaar known in the Tienen area since the middle of the were autochthonous. Since that time, members of nineteenth century (Lyell, 1852). Big stumps were both ‘schools’ maintained their positions due to encountered in the quarry of Overlaar (Fig. 1), lack of new observations (Hauregard, 1999). located at about mid-distance between Hoegaar- den and Tienen (Rutot, 1887), while extracting the ‘Landenian’ massive sandstone, and in a 5. Materials and methods road section at Wommersom 10 km to the east (Rutot, 1887). At Overlaar, the stumps were ob- The studied specimens, which have all been col- served in upright position in a bed of lignite over- lected from the same horizon in the Tienen For-

Plate I.

1^3. Goudberg Section, Hoegaarden (Belgium), earliest Eocene. In situ trunks. 1. Lateral view of a specimen still partly embedded in the sediment, showing marked de£ection of the lignite layer around the trunk base. Scale bar = 20 cm. 2. Apical view of a trunk base with well-developed buttress-like roots. Scale bar = 20 cm. 3. Lateral view of a large trunk base showing the usual 20^30‡ dip towards the east. Note the thin underlying lignite layer. Scale bar = 20 cm.

PALBO 2534 15-8-03 Cyaan Magenta Geel Zwart 110 M. Fairon-Demaret et al. / Review of Palaeobotany and Palynology 126 (2003) 103^129

2

1

4

3

56

PALBO 2534 15-8-03 Cyaan Magenta Geel Zwart M. Fairon-Demaret et al. / Review of Palaeobotany and Palynology 126 (2003) 103^129 111 mation, belong to three distinct groups. The ¢rst group is made up of 23 specimens from the Stock- mans’ collection of stumps and branches retrieved during the last century from the now disused Overlaar quarry, and preserved in the palaeobo- tanical collections of the Royal Institute of Natu- ral Sciences at Brussels. The second one includes more than thirty isolated dispersed pieces of sec- ondary xylem recently collected at and around the Goudberg Section, and more particularly along the motorway which runs parallel in places to the new railway track (Fig. 1). The tiny silici¢ed pieces obtained while macerating the lignitic ma- trix are added to this second group. The third group consists of silici¢ed secondary xylem frag- ments collected from six in situ tree bases at Goudberg. Two areas about 200 m apart in southeast di- rection along the motorway were systematically dug out up to the standing stumps at the base of unit 5 (Fig. 4). The ¢rst one, rectangular in shape (Fig. 4A,C, 1), is 70 m long and 20 m Fig. 4. (A) Position of the three areas, 1, 2 and 3, systemati- wide. Some 74 irregularly distributed stumps cally excavated up to the standing stumps. (B) Detail of the and dispersed pieces of trunk were recorded position of the 13 stumps of area 3. Abbreviations: D, direc- tion of inclination of each stump; T, angle of inclination. (about 500 trees/ha). Additional stumps were no- (C) Detail of the irregular distribution of 74 stumps (black ticed outside this area, indicating that many more dots) in area 1. are still embedded in the undisturbed surround- ings. The second area, with a semicircular bound- ary, of which about 0.15 ha was excavated (Fig. to measure their height, diameter at the base and 4A, 2), demonstrated an irregular distribution of top, direction and angle of inclination, as well as 67 stump and/or trunk remains. Nearby this sec- the spacing between individuals (Fig. 4C). ond area (Fig. 4A, 3) the embedded stumps were The stumps from Goudberg share the same carefully uncovered in an area of 7.5 m2 in order characteristics. They rest on a thin layer of lignite

Plate II. Transmitted light micrographs of thin sections of the secondary xylem Glyptostroboxylon sp. from the Tienen Forma- tion, Belgium.

1^3. Transverse sections. 4^6. Longitudinal tangential sections.

1. General view; growth rings and false rings. Specimen IRSNB 67855. U50. 2. Detail showing the shape of the tracheids. Specimen IRSNB 67680. U100. 3. General view of secondary xylem devoid of false ring. Notice the distribution of the xylem parenchyma cells. Specimen IRSNB 67590. U30. 4. General view of the vascular rays. Specimen IRSNB 67680. U85. 5. Detail of a vascular ray biseriate on one row. Specimen IRSNB 67590. U350. 6. Uniseriate rays of various heights. Notice the small bordered pits on the tangential walls of the tracheids. Specimen IRSNB 67590. U190.

PALBO 2534 15-8-03 Cyaan Magenta Geel Zwart 112 M. Fairon-Demaret et al. / Review of Palaeobotany and Palynology 126 (2003) 103^129

1 2

3 4

56 7

PALBO 2534 15-8-03 Cyaan Magenta Geel Zwart M. Fairon-Demaret et al. / Review of Palaeobotany and Palynology 126 (2003) 103^129 113 interstrati¢ed with black clay, and are surrounded ing the photomicroscope Reichert Polyvar. In ad- by a thin layer of dark and glossy lignitic clay. dition, pieces of fractured silici¢ed secondary xy- They are silici¢ed, more or less conical in shape, lem were prepared on stubs and gold-coated. truncated at the top which appears scalloped and Observation and photographs were made using crushed (Plate I, 1^3), and generally range be- a Jeol JSM-5800 scanning electron microscope. tween 60 and 100 cm in height. They stand up- Pieces of lignite were also soaked in hot water right, and most of them, when fully detached with Na2CO3 added and the dark brown solution from the clayey embedding matrix, show a 20^ obtained was sieved. No remains of diaspores 30‡ dip towards the east (Fig. 4B; Plate I, 1,3). were preserved and only naturally macerated sili- Their distal diameter usually ranges from 30 to 60 ci¢ed fragments of secondary xylem were re- cm, the biggest specimens reaching up to 80 cm. trieved. These were also studied under the SEM. The stumps are decorticated and an unknown Maceration of the lignite embedding the bases thickness of the outermost wood layers is not pre- of the tree as well as of the clayey matrix was also served. The diameter of the trees at breast height performed using standard palynological proce- (dbh; necessary for reporting stand basal area) dures (Streel, 1965). No palynomorphs have could not be valuably estimated. The base of been found in the samples of the Tienen Forma- each upright stump is enlarged with buttress-like tion, including the lignite of unit 5 (see Fig. 2 for £anges (Plate I, 1,2). No attached roots have been location). This is probably due to severe oxida- observed penetrating the underlying layers for an tion. appreciable length, and only the departure of sturdy, horizontal basal roots has occasionally been seen, spreading laterally from the enlarged 6. Mineralogy of the fossil wood base of the stumps. Several specimens are re- corded lying in-between the standing stumps. Any attempt at demineralisation of the in situ These are trunk-like, cylindrical in shape but and dispersed silici¢ed secondary xylem fragments usually are dorso-ventrally £attened, being pre- was disastrous. Microdi¡raction studies show that served over a longer length than the standing polycrystalline ¢ne-grained quartz is the main tree bases. component of the specimens, mixed with amor- The wood was studied using conventional thin phous opal (Kuczumov et al., 1999). Quartz oc- sections combined with observation of fractured curs both in cell walls and lumina, and very little, fragments under the scanning electron microscope if any, of the original organic matter is still (SEM). A transverse thin section of every speci- present. Apparently, the secondary wood pattern men was prepared, and when preservation ap- has not been lost to an appreciable extent during peared promising, tangential and radial sections the transition from the opal-like to the micro- were made. Light microscopy was performed us- quartz structure.

Plate III. Transmitted light micrographs of radial thin sections of Glyptostroboxylon sp. from the Tienen Formation, Belgium.

1. A vascular ray, two cells high with 1^4 rounded, eroded pit apertures/cross-¢eld. Notice the shape of the cross-¢elds. Specimen IRSNB 34865. U350. 2. An early wood vascular ray, four cells high; the marginal cells show four cross-¢eld pits arranged in two tiers; the median cells show two, side by side, taxodioid to glyptostroboid pits. Specimen ULg I2. U300. 3. Glyptostroboid to taxodioid early wood cross-¢eld pits. Specimen IRSNB 67590. U300. 4. Detail of the bordered pits on the horizontal walls of the tracheids. Specimen IRSNB 67590. U870. 5. Paired bordered pits. Crassulae are obvious. Specimen IRSNB 34865. U350. 6. Radial wall of a wood parenchyma cell. Specimen IRSNB 67642. U870. 7. Slightly knotted radial wall of a wood parenchyma cell. Specimen ULg I3. U870.

PALBO 2534 15-8-03 Cyaan Magenta Geel Zwart 114 M. Fairon-Demaret et al. / Review of Palaeobotany and Palynology 126 (2003) 103^129

1 2

3 4

5 6

PALBO 2534 15-8-03 Cyaan Magenta Geel Zwart M. Fairon-Demaret et al. / Review of Palaeobotany and Palynology 126 (2003) 103^129 115

7. Taxonomy

Family Cupressaceae Gray, nom. cons. Subfamily Taxodioideae Endl. ex K. Koch Genus Glyptostroboxylon Conwentz Glyptostroboxylon sp.

Fig. 5. Maximum likelihood phenogram stemming from a 8. Description cladistic analysis using the characters listed in Table 1.

The characters of all secondary xylem speci- mens studied are distributed along a continuum occur near the middle of a growth ring. The radial of variation, and despite some apparent dissimi- walls of early wood tracheids bear uniseriate to larity it was impossible to separate them into dif- rarely biseriate opposite bordered pits, 14^17 Wm ferent structural entities. They are consequently in diameter (Plate III, 1,4,5; Plate IV, 1). Crassu- interpreted as belonging to a single taxon, and lae are common (Plate III, 4,5). Bordered pit pairs described accordingly. have a well-developed torus which is scalloped The secondary xylem is homogeneous and (Plate III, 4,5). Their apertures are slightly ellip- shows no normal resin canals (Plate II, 1,3). De- tical. On the tangential walls of late wood trache- spite the high number of specimens studied, no ids slightly smaller uniseriate bordered pits, 12^15 traumatic resin ducts were observed. Growth Wm in diameter, are common (Plate II, 6). rings are clearly distinct (Plate II, 1^3), and of Axial parenchyma is di¡use (Plate II, 2,3) or very variable width. Within the same specimen, loosely grouped in tangential rows, 1 cell wide some growth rings show a gradual early^to late (Plate II, 1). In longitudinal sections the second- wood transition, whereas others show an abrupt ary xylem parenchyma cells are typically barrel transition (Plate II, 1^3). False rings may occur, shaped (Plate IV, 1). Brown to black deposits generally in the outermost part of a growth ring are frequent and usually obliterate the wall details (Plate II, 1); their number and frequency are (Plate III,7;Plate IV, 1). The horizontal walls are highly variable. Early wood tracheids of wide thin (Plate IV, 5) and smooth, slightly knotted growth rings are generally hexagonal to more or when pits are present (Plate III, 6,7). They never less rounded (Plate II, 2,3). They are more quad- appear strongly beaded. Small rounded half-bor- rangular in the early wood of narrow growth dered pits occur on their vertical walls often ar- rings (Plate II, 1), and are tangentially compressed ranged in two irregular, more or less parallel rows in late wood. Early wood tracheids have a radial (Plate IV, 5). diameter of 24^56 Wm (usually 40 Wm) and a tan- Vascular rays are homocellular (Plate II, 4^6; gential breadth between 32^44 Wm (usually 40 Plate IV, 1,2). They are mostly uniseriate, ranging Wm). As a rule the tangentially broadest tracheids from 1 to 34 cells high, although typically only up

Plate IV. Scanning electron micrographs of fractured longitudinal radial plane of Glyptostroboxylon sp. from the Tienen Forma- tion (Belgium). Specimen ULg I3.

1. General view with two vascular rays and two vertical rows of parenchyma cells. U95. 2. Detail of wide, rounded to oval, cross-¢eld pits. Notice the outline of the cross-¢elds. U490. 3. Glyptostroboid cross-¢eld pits (casts) irregularly arranged, up to ¢ve per cross-¢eld. U490. 4. Variation in shape, size and arrangement of cross-¢eld pits with a very narrow border. U490. 5. Detail of a wood parenchyma cell with small half-bordered pits. U290. 6. Detail of a vascular ray showing sparsely pitted (arrow heads) horizontal walls and occasionally, an enlargement at the junction between horizontal and vertical walls (small arrows). U875.

PALBO 2534 15-8-03 Cyaan Magenta Geel Zwart 116 M. Fairon-Demaret et al. / Review of Palaeobotany and Palynology 126 (2003) 103^129

1

2 3

4 5

PALBO 2534 15-8-03 Cyaan Magenta Geel Zwart M. Fairon-Demaret et al. / Review of Palaeobotany and Palynology 126 (2003) 103^129 117 to 2^4 cells (Plate II, 4,6); some are biseriate on rootlets less than 1 mm wide to tetrach (Plate V, one row (Plate II, 5). They occasionally contain 2,3) and exceptionally pentarch for the ‘widest’ black deposits. On tangential sections the outline ones 3.3 mm in diameter. Tiny frequently of the ray cells looks more or less like a £attened branched rootlets are seen attached to larger ellipse, the pointed, marginal cells being higher ones (Plate V, 2). In all sections epidermal cells than the median ones (Plate II, 4^6). The height lack root hairs. A mantle of hyphae surrounds of the median ray cells measures between 20 and each root (Plate V, 4,5); tiny Hartig net hyphae 28 Wm while the marginal ones reach 32^40 Wm. occur around the cortical cells, reaching the endo- Their relatively thick (1^3.4 Wm wide) horizontal dermis (Plate V, 3). These small roots with ecto- walls are smooth, and appear unpitted under the mycorrhizal association might belong to the same light microscope. The tangential walls are most taxon as the secondary wood. generally perpendicular (Plate IV, 6). Indentures are not present. At the point of junction of tan- gential with horizontal ray cell walls, a triangular 9. Identi¢cation widening is sometimes noticed (Plate III,2;Plate IV, 6, arrows). The combination of distinct growth rings, Cross-¢eld pits vary from taxodioid to glypto- smooth to sparsely pitted, horizontal and tangen- stroboid. Cupressoid pits have not been observed. tial walls of ray parenchyma, 1^30 cells high rays The pit aperture is often rounded (Plate III, 1^3; with occasionally 1^2 paired cells in the body, and Plate IV, 2^4), although wide oval pit apertures 1^6 taxodioid to glyptostroboid pits in the cross- are not rare either (Plate II,3;Plate IV, 3,4,6). ¢elds, in association with the absence of resin Their long axis is inclined at an angle of 0 to ducts and spiral thickening, indicates taxodia- about 25‡ to the horizontal wall of the ray cell. ceous secondary xylem. In the absence of other The border, if present, is always narrow. The di- evidence, these woods are notoriously di⁄cult to ameter of the cross-¢eld pits is 8^14 Wm. Their assess because of the overlapping characters (Bas- number ranges from 1 to 6 (exceptionally 7) per inger, 1981). Furthermore, there are di¡erent cross-¢eld. When more then two are present, the opinions about the diagnostic value of these char- cross-¢eld pits are usually arranged in two tiers, acters (Figueiral et al., 1999). occasionally three tiers, and are irregularly dis- Usually, determination of taxodioid fossil sec- posed (Plate IV, 3,4,6). Numerous irregularly dis- ondary xylem puts special emphasis on the cross- posed cross-¢eld pits are particularly obvious on ¢eld pits (Kra«usel, 1949). However, it has been the higher marginal cells but they also occur on shown that the type of cross-¢eld pitting is rather the median ones. variable within a single species according to the Incidentally, small roots (Plate V, 1) were ob- part of the tree considered (Bailey and Faull, served inside branch pieces, 15/10 cm wide by 1934), and only the most common type of early about 30 cm long, lying in-between the stumps. wood cross-¢eld pitting should be considered These have no secondary xylem; they vary from (Kra«usel, 1949). In addition, even in modern sec- diarch and triarch (Plate V, 4) for the smallest ondary xylem, the di¡erence between taxodioid,

Plate V. Transversal sections through Glyptostroboxylon sp. from the Tienen Formation, Belgium, with roots in the decayed pith. Specimen ULg Re¤servoir 1.

1. Transverse section through a branch, general view showing sections of small roots in the decaying pith. Re£ected polarised light micrograph of the polished surface. U3. 2. Detail of a branching rootlet. U20. 3. Detail of a tetrach root. Cortical cells up to the endodermis are enclosed in the Hartig net. U90. 4. A triarch root with a thick mantle of hyphae. The arrows point to the secondary xylem of the branch. U35. 5. Detail of the mantle of ectomycorrhizal hyphae. U200.

PALBO 2534 15-8-03 Cyaan Magenta Geel Zwart 118 Table 1 Comparison of the characteristics of extant Taxodioideae genera, Taxodioxylon gypsaceum, Glyptostroboxylon tenerum, and the Hoegaarden wood

Cunning- C Sequoia C Sequoia- C Metase- C Crypto- C Taxodium C Glypto- C gypsa- C tenerum C wood C hamia dendron quoia meria strobus ceum

Tracheids Number 1 (rarely 2), 1 scattered, 1 1 (3) 0 1^2 (3) 1 1^2^(3), (3) 2 up to quadri- 3 1^2, in long 1 1^2^(3^4), (6), 3 uni- to 1 uni- to 1 of pits (2), (3), (6) rarely 2 side seriate (3) rows (3) up to (8), 1^2^3 (9) biseriate (9) biseriate

by side (3) 4 in thick root, 103^129 (2003) 126 Palynology and Palaeobotany of Review / al. et Fairon-Demaret M. (10) Diameter of 9^11 (3) 0 16^18 (3) 1 14^17 (3) 1 20^22 1 13^14 (3) 0 12^14 (3), 8^120 13^16 (3) 1 14^17 (8) 1 11 (10); 14^20 1 14^17 1 pits (9) (9) Torus present 1 present 1 absent (1) 0 present 1 present 1 present 1 present 1 present 1 present 1 present 1 Tang. diam. 30^55 (3), 30^ 0 40^50 (3) ^80 1 30^90 (3) 1 65^85 (3), 40^ 1 30^50 (2) 0 35^90 (2), (7) 1 40^50 (3), 20^ 1 40^54^70 (8), 1 40^44^50 (9), 0 32^40^44 0 AB 5415-8-03 2534 PALBO (early wood) 60 (2) (7), 24^60 (2) 85 (4) 70 (2) 45^48^60 (9) 32^50 (10) Rays Height 1^24, 30 (2) 0 1^30 (2)^ 40+ 1 1^20+ (3) 0 1^30 (3) 0 1^30 (2); 1^6 0 up to 60 cells 1 1^18 (330) (3) 0 1^30 (8), 7^12 0 1^8^14 (9) up 0 1 up to 34 0 (7) (7), (3) (9) to 24 (10) Width partly biseriate 1 biseriate 1 uniseriate, rare 1 uniseriate, rare 1 partly biseriate 1 ? rare 1^2 paired1 rare paired 1 occas. paired 1 rare 1^3 paired1 (2) (partly or biseriate partly biseriate (rare) cells (3) cells (9) cells cells compl.) (partly or (3) compl.) (3) Ray tracheids present (1) 1 present (1), (4) 1 present (4); ? 1 present (1), (4) 1 absent (1) 0 absent (1) 0 absent (1) 0 absent (8) 0 absent (9) 0 absent 0 Cyaan (1) Hor. wall thin and pitted 1 sparsly pitted 1 sparsly pitted 1 sparsly pitted 1 thick and 0 thick and 1 thin+warts (3) 1 smooth (9) to 1 smooth (9) 0 thin and 1 pitting (4) (4) (4) smooth (3) pitted (3) pitted (6) sparsly pitted Magenta Indentures prominent in 1 absent (2), 1 shallow (3) 1 not noted (3), 1 prominent (2) 1 absent (3) 0 present (2); 1 not mentioned ? not mentioned ? absent 0 early wood (2) occasional (3) present (7) none (3) Peculiarity relatively small resin rad.+tg. walls tg. wall thin, highest rays triang. occasional cross-¢eld pits tracheids+ thickn. to the smooth (3) within widening at triang. Geel (3) medull. stone same extent (3) medull. stone taxodiaceae (2, junction (3) widening at cells (11) cells (11) 3) junction

Zwart Cross-¢eld pits Type glypto-cupresso taxodioid (3) taxodioid (3) taxodioid (3), taxo to glypto taxodioid (2) glypto (3), taxo-(glypto)- taxo to glypto taxo to glypto (5), taxo- (5), taxo- taxo-glypto- (2) taxo to glypto (cup- (9) glypto- (glypto- (cupresso- (2), (4) ressoid) (6) (cupresso- cupresso- podocarpo) (4) podocarpo) (4) podocarpo) (4) Number 2^4 (2) 0 2^5 (2); 1^6 1 1^2 and 4^6 1 1^2 (3) 0 2^4 (2) 0 2^6 (2) up 8 1 1^8 (3); 2^6 1 2^6^(5), (8); 1 1^4^8 (9), (10) 1 1 to 7 1 (3) (3) (3) (2), (4) 2^3 (9) Disposition one horizontal one horizontal one horizontal side by side or one horizontal mostly in twos 2 tiers, occas. side by side in several tiers, 2 tiers, occas. series (6) superposed 3, one and 3 series (2); 0 series (2) 0 or two (3), 1 (3), (7) 1 series (2), 1 side by side (3)0 irregularly 1 row (8), (9), 1 irregularly 1 irregularly 1 superposed in aperture often distributed (2) two tiers distributed distributed terminal cell horizontal. (3) ‘elongated (6) M. Fairon-Demaret et al. / Review of Palaeobotany and Palynology 126 (2003) 103^129 119 ;

0 half-bordered pits with wide oval aperture and narrow border, and glyptostroboid pits similar to the taxodioid ones but with a very narrow, also two side by side sparsly pitted pitted with almost invisible border (Schwarz and Weide, ? smooth to C wood C 1 small nodules 1 1962, p. 177), is not always easy to assess, as a variety of transitional forms occur within each species. Measurements of the length of the pit and width of the margo, followed by calculation tenerum also two side by side (9) smooth (10) thin and (6) thickn. (9) C 1 irregularly of the Schwarz and Weide (1962) index, plus con-

van der Burgh and Meijer, 1996 sideration of the inclination of the aperture give

;6 good clues. On the Belgian fossil secondary xylem the Schwarz and Weide index is rarely applicable, gypsa- ceum when more than 4 (8) thin, smooth (9) (6), (8) ? to pitted with 0 pitted (beaded) C 1 small nodules as the cross-¢eld pits often appear corroded and with ill-de¢ned margins when observed under the transmitted light microscope (Plate III, 1^3). Nevertheless, on the same piece of secondary xy- Glypto- strobus small nodules (1), coarse on internal+ marginal ray cells (2) occasional pits nodular (4) lem both types of cross-¢eld pitting ^ 4^7 more or C 1 (3), smooth to less superposed glyptostroboid pits (Plate III, 1,4; .

Henry and McIntyre, 1926 Plate IV, 3,4) or 1^2 side by side taxodioid ones (Plate III, 1,2) ^ are observed on early wood ray Taxodium large nodules (1) series (2) (5) ; (5) cells. Amongst the many specimens studied, both ? coarse pits (2), 1 pits (2), 1^2 C 1 thick, nodulose taxodioid and glyptostroboid cross-¢eld pits are thus present, the glyptostroboid type of pitting occurring at least as frequently as the taxodioid. Crypto- meria large nodules (1) superposed (3) 1 horizontal (2) nodular (3) We have not observed typical cupressoid pits. Ac- Bailey and Faull, 1934 ? rare coarse pits C cording to Kra«usel’s key, the Hoegaarden second-

;11 ary xylem falls between Taxodioxylon Hartig emend. Gothan and Glyptostroboxylon Conwentz. Schwarz and Weide, 1962 Metase- quoia large nodules (1) nodul. (4) According to the last ‘diagnoses’ (sic) provided C 0 smooth to nfeld, 1955

; (4) for Taxodioxylon and Glyptostroboxylon (Su«ss « and Velitzelos, 1997), the di¡erence between Scho both genera is narrow indeed. The segregation, ;10 Sequoia- dendron small nodules (1) simple pits (5) once again, rests on the early wood cross-¢eld C 0 thin with pits: they have broad apertures of more or less Greguss, 1955 elongated axis (taxodioid pitting) in Taxodioxylon

; (3) while they are ovoid in Glyptostroboxylon, all the Sequoia large nodules (1) (5) other characters listed in both ‘diagnoses’ being Gottwald, 1992 C 0 thin, uniform identical. Su«ss and Velitzelos (1997) do not dis- ;9 cuss the taxonomic value of this single feature, Peirce, 1936 which is known to be rather variable even within a single extant species (Bailey and Faull, 1934). ; (2) Cunning- hamia smooth (1), thin, pitted slightly thickn. (2) 1 smooth (3) 1 smooth (3) 1 smooth (3) 0 slightly

Huard, 1966 As both types of pitting occur in the Hoegaarden ).

;8 wood, the morphology of the cross-¢eld pits gives no clue for its identi¢cation. In taxodioid fossil (and extant) secondary xy- Continued lem, emphasis is also put on the morphology of

Gadek et al., 2000 the horizontal wall of the secondary xylem paren- Basinger, 1981 7 Table 1 ( (1) C, coding of the characters. Parenchyma Horiz. wall to nodular (3), chyma cells. In Glyptostroboxylon these walls are

PALBO 2534 15-8-03 Cyaan Magenta Geel Zwart 120 M. Fairon-Demaret et al. / Review of Palaeobotany and Palynology 126 (2003) 103^129 described as smooth, sparsely pitted (see Scho«n- T. gypsaceum. The formalisation of such a feld, 1955 for a listing of Glyptostroboxylon speci- move, however, requires ¢rst-hand knowledge of men characters) to irregularly thickened (Gott- the type-specimens plus an in-depth analysis of a wald, 1992). A similar range of variation is also variety of formerly described fragments from dif- noticed in Kra«usel’s descriptions of Taxodioxylon ferent localities and ages. This is beyond the scope gypsaceum Go«ppert, the most common European of this paper. Tertiary taxodiaceous secondary xylem, where the Meijer (2000), while describing late Cretaceous horizontal walls of the axial parenchyma are re- silici¢ed driftwood from the Aachen Formation garded as smooth to granularly thickened (Su«ss (northeast Belgium), faced a similar problem of and Velitzelos, 1997) or as frequently nodular, overlapping characteristics. Despite occurrence the nodules being small and uneasy to observe of so-called ‘Eiporen’ (sensu Kra«usel, 1949) ar- (van der Burgh and Meijer, 1996). The validity ranged in more than one horizontal row in me- of Glyptostroboxylon has even been questioned dian ray cells, he chose assignation to Taxodi- because G. tenerum (Kraus) Conwentz appears oxylon as Taxodioxylon cf. gypsaceum instead of di⁄cult to distinguish from T. gypsaceum (van Glyptostroboxylon mainly because his specimen der Burgh and Meijer, 1996, and references there- demonstrated rootwood features, and Sequoia in). Actually, when considering the variability of rootwood according to Bailey and Faull (1934) both key features, i.e. cross-¢eld pits and wood possesses similar cross-¢eld pits. We have second- parenchyma horizontal walls (Table 1), it is ary xylem from branches and trunk bases, not tempting indeed to synonymise G. tenerum and from roots. These wood fragments show a variety

Table 2 Quanti¢cation of the characters Characters Coding Tracheids Pit number 1 0 21 32 more than 3 3 Pit diameter less than 16 Wm0 more than 15 Wm1 Torus no 0 yes 1 Tangential diam. less than 61 Wm0 more than 60 Wm1 Rays Height less than 41 cells 0 more than 40 cells 1 Width uniseriate 0 biseriate 1 Tracheids no 0 yes 1 Hor. wall smooth 0 pitted 1 IØndentures no 0 yes 1 Cross-¢eld pits less than 5 0 more than 4 1 Disposition one row 0 two rows 1 Parenchyma Horizontal wall smooth 0 nodular 1 Horizontal wall thin 0 thick 1

PALBO 2534 15-8-03 Cyaan Magenta Geel Zwart M. Fairon-Demaret et al. / Review of Palaeobotany and Palynology 126 (2003) 103^129 121 of cross-¢eld features. Their cross-¢eld pits are mative. The specimens attributed to G. tenerum nevertheless more often organised in irregularly from brown coal of the Lower Rhine Embayment superposed tiers rather than side by side in a by van der Burgh (1973) appear to be di¡erent line, even in median ray cells. Accordingly, we from those of Hoegaarden. They are instead re- adopted a conservative position and decided for garded as belonging to Taxodioxylon by Su«ss and the inclusion of Hoegaarden secondary xylem in Velitzelos (1997), a divergence of opinion illustrat- Glyptostroboxylon. In the present state of knowl- ing once more the di⁄culty in distinguishing be- edge of both wood arti¢cial taxa, our decision is tween Taxodioxylon and Glyptostroboxylon.Our comforted by the following observations: (1) the specimens are more comparable to G. tenerum intertracheidal bordered pits are never triseriate, Eocene silici¢ed material from brown coal pits even on the radial walls of the widest elements, (2) near Leipzig (Germany), but on transverse sec- the latter are smaller than those of T. gypsaceum tions the German secondary xylem shows a looser (van der Burgh and Meijer, 1996, for a compar- arrangement of the tracheids with open, recognis- ison of data from di¡erent descriptions of T. gyp- able intercellular spaces (Scho«nfeld, 1955, Taf. 7, saceum), and (3) the relatively narrow width of Abb. 54). The G. tenerum phosphatised driftwood early wood tracheids and the height of ray cells described by Gottwald (1992) from the Late Eo- give a peculiar appearance to the radial sections cene of Helmstedt (Germany) is similar to the with cross-¢elds generally much less radially elon- Belgian Glyptostroboxylon, but cross-¢elds with gated than those usually illustrated for T. gypsa- single pits are apparently not present. We there- ceum. Nevertheless, the Hoegaarden wood in- fore decided not to refer the Hoegaarden second- cludes features of both Taxodioxylon and Glyp- ary xylem to G. tenerum. It is designated as Glyp- tostroboxylon, illustrating the occurrence of a Ter- tostroboxylon sp. to emphasise its unique combi- tiary taxodioid secondary xylem complex in which nation of characteristics pointing to the Glypto- segregation between arti¢cial genera is presently stroboxylon type of fossil wood genus, but with debatable. several traits, notably the horizontal wall pitting Until recently Glyptostroboxylon tenerum was of the wood parenchyma cells, of Taxodioxylon the only species referred to Glyptostroboxylon gypsaceum. (for synonymy, see Kra«usel, 1949; Su«ss and Ve- litzelos, 1997). Lately two more species have been added to the genus: G. microtracheidale Su«ss and 10. Discussion and comparison with modern Velitzelos 1997 and G. tendagurense Su«ss and taxodiaceous taxa Schultka 2001. Glyptostroboxylon tendagurense, known from the Upper Jurassic of East Africa, Recently, several clades have been identi¢ed is remarkable for its extremely narrow tracheids within taxodiaceous taxa leading to a more infor- with variable size and shape. Glyptostroboxylon mative infrafamilial classi¢cation (Gadek et al., microtracheidale, present in the Upper Oligo- 2000; Kusumi et al., 2000), Sciadopitys Siebold cene^Lower Miocene of Lesbos (Greece), di¡ers et Zucc. being transferred to the monotypic family from the Hoegaarden secondary xylem in the ar- of the Sciadopityaceae Luerss. (Farjon, 1998). rangement of its radially shortened tracheids The Taiwanioideae (Hayata) Quinn and Athro- which are disposed in irregular rows. taxidoideae Quinn have secondary xylem di¡erent Glyptostroboxylon tenerum is considered as from the Hoegaarden specimens, showing smaller widespread in the European Cenozoic (van der bordered pits on their tracheids, shorter rays Burgh, 1973, and references therein; Mai, 1995), (rarely exceeding 10 cells high in Athrotaxis D. but no recent detailed description is available. Don), and smaller cross-¢eld pits which are dis- Stockmans and Willie're (1934) recorded G. tene- tinctly cupressoid in Taiwania Hayata (Peirce, rum at Leval^Trahegnies in Belgium, a locality of 1936; Greguss, 1955). about the same age as Hoegaarden, but the de- The gross morphology of the secondary xylem scription is very short and the drawings uninfor- of monogeneric Cunninghamioideae (Siebold et

PALBO 2534 15-8-03 Cyaan Magenta Geel Zwart 122 M. Fairon-Demaret et al. / Review of Palaeobotany and Palynology 126 (2003) 103^129

Zucc.) Quinn is close to the Belgian specimens, Cryptomeria, with up to 3-seriate bordered pits especially in the size of the cells and the outline on the radial walls of its tracheids, strongly nod- of the cross-¢elds. Actually, according to Gothan ular parenchyma horizontal walls, thickened hor- (1905), Glyptostroboxylon is comparable to the izontal walls of the ray cells with well discernible wood of both the extant genera Cunninghamia indentures, is clearly di¡erent from the Hoegaar- R. Brown and Glyptostrobus Endl. Cunninghamia den wood (Table 1). rays with pointed marginal cells, higher than the The Sequoideae have heterocellular rays, median ones, as seen on tangential sections, have although these are not common. They are consid- the same appearance indeed as those of the Hoe- ered to have smooth horizontal walls in the xylem gaarden wood. However, the tracheids usually parenchyma, as opposed to the dentate ones of show only uniseriate bordered pits on the radial the Taxodioideae (e.g. Greguss, 1955). However, walls, and thus constitute an exception to the usu- disagreement is obvious on this key distinguishing al occurrence of biseriate-bordered pits, a feature feature (Table 1). We are not in a position to shared by all other taxodiaceous secondary xylem decide between these con£icting observations. (van der Burgh and Meijer, 1996; Table 1). More- Other characters are helpful. Sequoiadendron is over, Cunninghamia possesses ray tracheids (Ga- the only taxodiaceous secondary xylem without dek et al., 2000), but these are obviously di⁄cult a torus on the membrane of intertracheidal pit to observe as they are not mentioned in earlier pairs. A torus is present on the Belgian wood literature, and non-observation of ray tracheids (Plate II,4;Plate III, 4). The size of the Sequoi- on fossil taxodiaceous wood may not preclude deae tracheids is also di¡erent. Tracheid size de- their occurrence (Basinger, 1981). In Cunningha- pends on growth rate and the vertical and lateral mia, 2^4 glyptostroboid to cupressoid pits, and position on the tree of the studied branch or apparently no taxodioid ones, are arranged in trunk material, and is thus of questionable taxo- one horizontal series in the cross-¢elds but super- nomic importance. Nevertheless, the maximum posed pits are also noticed, particularly in the tangential diameter of the tracheids in the outer- terminal cells of the rays (Table 1). These di¡er- most part of a stem gives a rough indication ences between Cunninghamia and Glyptostroboxy- about stem height (Stockey et al., 2001, and refer- lon sp. wood anatomy are di⁄cult to evaluate, ences therein). The tallest known living trees pos- more so as divergence of opinion still exists par- sess early wood tracheids with the widest tangen- ticularly about the morphology of the radial walls tial diameter (up to 85 and 90 Wm for Sequoia and of the secondary xylem parenchyma cells (see Ta- Sequoiadendron; Table 1). In Glyptostroboxylon ble 1). Anyway, both present-day species, C. ko- sp. from Hoegaarden the widest measured tangen- nishii and C. lanceolata, which are very similar tial diameter reaches 44 Wm only. Even if it can- and should perhaps be treated as varieties of a not be ascertained that this dimension represents single species (Farjon, 1998), are often multi- the widest tracheids, as we know neither the age trunked, an observation never made at Hoegaar- nor the stage of maturity reached by the stumps, den where only stumps standing singly are re- Glyptostroboxylon from Hoegaarden nevertheless corded. appears to belong to smaller trees than the giant If a consensus exists on the members ^ Sequoia Sequoideae. Endlicher, Metasequoia Hu et Cheng and Se- Within the Taxodioideae, Taxodium distichum quoiadendron giganteum Buchholz ^ of the Sequoi- (L.) Rich has strongly nodular horizontal walls deae clade, on those of the Taxodioideae there is of secondary xylem parenchyma cells. It also pos- debate. According to Gadek et al. (2000), the sesses the tallest rays (up to 60 cells high) and its Taxodioideae clade includes Taxodium L.C. Rich- tracheids are much wider than in Glyptostroboxy- ard, Cryptomeria D. Don and Glyptostrobus, lon sp., with up to 4-seriate bordered pits on the while Kusumi et al. (2000) conclude that Taxodi- radial walls (Table 1). Similarity with secondary um and Glyptostrobus form a clade which is in a xylem of Glyptostrobus pensilis (Staunton ex D. sister-group relationship to Cryptomeria. Don) K. Koch is greater. Indentures have been

PALBO 2534 15-8-03 Cyaan Magenta Geel Zwart M. Fairon-Demaret et al. / Review of Palaeobotany and Palynology 126 (2003) 103^129 123 reported as regularly present (Peirce, 1936), at with a complex comprising Taxodium, Taxodi- least in the early wood (Scho«nfeld, 1955). How- oxylon, Glyptostroboxylon, and the Hoegaarden ever, according to Greguss (1955), at the point of wood. junction with horizontal walls, the tangential ray In summary, the secondary wood from Hoe- cell walls widen in the shape of a triangle. A sim- gaarden is similar in gross morphology to extant ilar triangular enlargement is occasionally noticed Cunninghamia but clearly distinct from the mod- on the Belgian Glyptostroboxylon sp. Glyptostro- ern genus when considering anatomical details. bus pensilis shows pitting on the horizontal walls Several features (more particularly the variability of ray parenchyma cells, a character which is in the cross-¢eld pit type) are shared with extant more dubious on Glyptostroboxylon sp. Owing Sequoia wood, but Belgian Glyptostroboxylon sp. to the relative tangential diameter and height of appears most similar, although not identical, to the ray cells, early wood cross-¢elds are similar in living Glyptostrobus secondary wood. outline in both fossil and extant woods. Bordered The taxodiaceous conifers have a very long fos- pits on the radial walls of early wood tracheids sil history, originating during the Triassic (Yao et are of similar diameter to the lower range of taxo- al., 1997) and being well established by Jurassic diaceous secondary xylem pit dimension (Table time (Basinger, 1981; Stewart and Rothwell, 1). The transverse walls of the vertical wood pa- 1993). Evidence for Cunninghamia-type fossils oc- renchyma cells of G. pensilis are, once more, var- curs as early as the Middle Jurassic with several iously described as simply pitted or with incon- genera of permineralised seed cones, some wood spicuous thickenings or as distinctively nodular pieces and compressed vegetative and fertile re- but with small nodules (Table 1). Anyway, the mains (Yao et al., 1998, and references therein). di¡erence between Glyptostroboxylon sp. from The earliest fossil identi¢ed as Cunninghamia Hoegaarden and extant G. pensilis wood is nar- dates back to the Hauterivian^Barremian (middle row, the most obvious di¡erence being the usually Early Cretaceous) of Inner Mongolia (Kester, higher number of pits/cross-¢eld and their nar- 2000) but fossil cones most similar to those of rower diameter in the modern species. The impor- Cunninghamia are known to occur in the Lower tance of these discrepancies in relation to preser- Cretaceous beds of California (Miller, 1974). On vation bias, nature of environmental signature, the basis of parsimony analysis of nucleotide se- physiology and development of the source trees quence data from the plastid genes matK and is presently impossible to assess. rbcL, together with non-molecular data consider- The a⁄nities of the Hoegaarden wood to some ations (Gadek et al., 2000) as well as of nucleotide taxa with roughly comparable secondary xylem sequences from three additional chloroplasts (Table 1) were also estimated through a cladistic genes (Kusumi et al., 2000), Cunninghamia was analysis. The analysis was based on 10 taxa and the ¢rst indeed to separate within the taxodia- 13 characters, listed in Table 1. Some characters ceous lineage. The order of divergence of both have been arbitrarily coded such as the tracheid sequoioid and taxodioid clades, although re- tangential diameter, coded 0 for diameters under solved, receives less support, but apparently they 60 Wm and 1 for larger diameters (see coding for both diverged after separation of Cunninghamia, each character, columns marked C in Tables 1 Taiwania and Athrotaxis (Gadek et al., 2000; and 2). The Branch-and-Bound routine of Kusumi et al., 2000). A glyptostroboid type PAUP (version 3.1.1; Swo¡ord, 1991) generated of wood is already recognised by the Upper one single tree of 21 steps, with consistency index Jurassic in East Africa (Su«ss and Schultka, of 0.667. This phenogram (Fig. 5) con¢rms our 2001). Taxodioxylon gypsaceum is present in the more intuitive analysis, as the Hoegaarden wood Cretaceous (Meijer, 2000). Occurrence of second- appears to share the closest similarities with Glyp- ary xylem, the overlapping characteristics of tostroboxylon, and to a lesser extent with Taxodi- which appear to be shared by both Taxodioxylon um and Taxodioxylon. Furthermore, the analysis and Glyptostroboxylon in the very early Eocene places Glyptostrobus in a sister-group relationship once more points to the structural unity of this

PALBO 2534 15-8-03 Cyaan Magenta Geel Zwart 124 M. Fairon-Demaret et al. / Review of Palaeobotany and Palynology 126 (2003) 103^129 taxodioid type of wood, while seeds belonging to the organic molecules of the dead wood tissues three modern genera, Glyptostrobus, Sequoia and (Martin, 1999). Taxodium, are already recognised in Middle Euro- pean Cenomanian strata (Knobloch and Mai, 1986). 12. Palaeoenvironmental considerations

At Hoegaarden the bases of the stumps are 11. Taphonomic considerations embedded in a lignite layer (unit 5; Figs. 2 and 3). The Hoegaarden trees were lignite builders Examples of stumps transported in upright po- consistently colonising lowland habitats and living sition in mud£ows (e.g. in those generated by the in a swampy but nevertheless irregularly water Mount Saint Helen’s eruption; Karowe and Jef- stressed environment. Water stresses, consequence ferson, 1987) are well known. As is the case for either of low or high water levels, caused the de- the Hoegaarden stumps, they are less than 2 m velopment of false growth rings in addition to high and possess a wide base with no or very few regular, seasonally induced ones. roots remaining. A matrix di¡erent from the sur- Present-day Taxodioideae are often found in rounding sediment is often noticed in their root- swampy environments, particularly both decidu- balls, a character by which they di¡er from the ous swamp cypresses, Glyptostrobus pensilis and Hoegaarden stumps (Chapman, 1994, and refer- Taxodium distichium. These peat builders share ences therein). At Hoegaarden the stumps are 1^3 similar ecological requirements. One of the re- m apart, and, as already noticed in the nearby maining populations of the globally threatened Overlaar area, distributed in a similar way as in G. pensilis, with more than 200 individuals, is to some modern virgin conifer forests. Clearly, the be found in a swampy area, in the Da Lak prov- density of the stumps is a good argument for their ince at about 500 m altitude in the central high- in situ position. The large geographical extent of lands of Vietnam (Source book of Existing and the lignitic layer on which the stumps are to be Proposed Protected Areas in Vietnam, 2001). found precludes the hypothesis of small rafts of Glyptostrobus pensilis is scattered also in southern forest £oor with standing trees having been trans- China and occurs to as far as 13‡N in Vietnam, ported several times (Karowe and Je¡erson, attesting to its wide amplitude of ecological toler- 1987). In addition, occurrence of roots reaching ance (Li, 1953). It thrives in damp places usually the underlying sandstone reinforces the argument. at low elevation, on river banks and next to in- No roots are preserved between the stump bases undated rice ¢elds. In the eastern US Taxodium and the massive sandstone in which undetermin- distichum is widespread in swamps and on water- able root casts only rarely are observed. The al- logged lakeshores where it usually occurs in pure teration of wood is greatly in£uenced by the em- stands but with sparse understory angiosperm bedding sediment and its permeability (Weibel, trees on drier sites. Such a Taxodium consociation 1996), and all the original organic content includ- could provide a likely modern analogue for the ing roots have been leached out of the permeable Hoegaarden fossil forest in which the spacing of white sands, a process most probably resulting the taxodiaceous stumps is similar as in some from variations in the water table level and in modern intact swamp forests. its physical and chemical characteristics. As a On the other hand, extant Sequoia sempervirens consequence also of considerable variations in (D. Don) Endl is often assumed to be the nearest the water table levels, accumulated dead organic living relative to Taxodioxylon gypsaceum (van material in the peat decayed while the stumps, der Burgh and Meijer, 1996, and references there- sitting on poorly permeable lignitic clay, were per- in), which also shares characteristics with the mineralised by silica-rich water percolating Hoegaarden Glyptostroboxylon sp. Such an as- through the overlying sandy deposits, silica pre- sumption is questionable, independent from the cipitation during petrifaction being templated by di⁄culties raised by the variability of this taxodia-

PALBO 2534 15-8-03 Cyaan Magenta Geel Zwart M. Fairon-Demaret et al. / Review of Palaeobotany and Palynology 126 (2003) 103^129 125 ceous wood. The coast redwoods which include the Mons Basin yields a diversi¢ed leaf assem- the tallest known trees are now restricted to the blage with a paratropical signature according to foggy coastal belt of northern California. They Marty (1907). In addition, numerous charred sec- are not peat builders, as opposed to Taxodioxylon ondary xylem remains have been recently col- gypsaceum which is commonly found in European lected. Apart from angiosperm secondary xylem Tertiary lignite. A hypothetical change in ecolog- remains, several pieces of Glyptostroboxylon sp. ical requirements of S. sempervirens (Jurasky, identical to the Hoegaarden taxon have been 1936, in Mai, 1995) through time does not pro- identi¢ed. The embedding sediment yields a di- vide an answer to the disagreement. Obviously verse palyno£ora (Petricevic, 2000) with, amongst within the fossil taxodioid complex of secondary other taxa, many Inarperturopollenites hiatus (Po- wood, anatomical information is on itself insu⁄- tonie¤) Thompson et P£ug, the mother plant of cient for deduction of precise taxonomic a⁄nities which is Taxodium or/and Glyptostrobus. Hup- with a modern species. This is particularly true for paye, located along the Namur^Tienen railway the Hoegaarden wood. track about 16 km from Tienen, is another fossil locality in the Tienen Formation. Its position within the Formation is not well constrained, 13. Other macrofossil remains from the Tienen but its age appears similar to Hoegaarden. The Formation plant remains of Huppaye studied by Gilkinet (1925) are preserved in a very hard whitish mi- Nearby coeval fossil localities may provide crite. The assemblage is diverse, yielding a variety helpful additional macrofossil remains to recon- of fern pinnules with a majority of Lygodium re- struct the plant landscape, as more than 30 fossil mains, several types of eudicot and palm leaves, localities are known from the Tienen Formation well preserved internal and external moulds of in strata encompassing the Palaeocene/Eocene Ericaceae capsules and many gymnosperm re- transition in Belgium. Yet, most of them, with mains. Taxodiaceous twig fragments and cones the exception of Dormaal, Trieu de Leval and called ‘Athrotaxis (Sequoia) couttsiae’byGilkinet Hoegaarden, are known only from small outcrops (1925) are especially numerous; they occur as 3-D or boreholes. The Dormaal Sand Member is fa- empty casts without any organic matter pre- mous for the richness and diversity of the verte- served. This association of remains trapped in brate assemblage it yields. It is located at the base the sandy sediment illustrates a rich and diverse of the Tienen Formation (Steurbaut et al., 1999), £ora with a wet, warm signature. and is slightly older than the Hoegaarden lignitic Palynological remains, gymnosperm leaf litter bed. Silici¢ed wood of Populoxylon Ma«del^Ange- and roots have been destroyed at Hoegaarden liewa (Doutrelepont et al., 1997) plus angiosperm by oxidative taphonomic processes and diagene- fruits and seeds are present at Dormaal, but no sis. It can be argued that the same might explain gymnosperm remains are recorded. The Dormaal the absence of angiosperm remains. Of course plant assemblage is characterised by the abun- gymnospermous secondary xylem is more resis- dance of £eshy fruits, drupes and berries pro- tant to decay than angiospermous wood (Lu«cke duced by climbing plants, especially woody lianas et al., 1999; Figueiral and Mosbrugger, 2000). (Fairon-Demaret and Smith, 2002) that are Lignin of the latter is typically degraded into known to play an important role in forest types water-soluble products and hence is rapidly de- in a warm moist climate (Morley, 2000). Accord- stroyed, whereas the gymnosperm lignin decays ing to palynological analyses of the Dormaal into water-insoluble products (Hatcher and Clif- Sands, the assemblage that also yields a variety ford, 1997; Kim and Singh, 2000). However, we of fern spores is dominated by Juglandaceae, think that the non-occurrence of angiosperm re- and includes Myricaceae, Restionaceae, Pinaceae, mains at Hoegaarden is not to be attributed to and two taxa of Normapolles (Steurbaut et al., taphonomic bias. The monospeci¢c character of 1999). The correlative Trieu de Leval locality in the Hoegaarden in situ forest is linked to the spec-

PALBO 2534 15-8-03 Cyaan Magenta Geel Zwart 126 M. Fairon-Demaret et al. / Review of Palaeobotany and Palynology 126 (2003) 103^129 i¢city of its swampy coastal alluvial £oodplain LPTM) at about 55 Ma, when climate was the environment as deduced by sedimentological data. warmest of the entire Cenozoic. In another Glyptostroboxylon sp. locality de- scribed in younger, Upper Eocene, sediments on the Isle of Wight no other plant macrofossils oc- Acknowledgements cur with the ligniti¢ed and occasionally heavily pyritised stumps. They also are thought to have All the team members are very grateful to Dr. grown as monospeci¢c stands in a waterlogged Piet Laga of the Belgium Geological Survey for habitat, occupying swampy areas within the veg- his generous sharing of information and to Hugo etation of a coastal alluvial £oodplain (Fowler et De Potter of the IRSNB for his active help in the al., 1973). ¢eld. We also thank Mr. M. Dejean, secre¤taire du Cercle ge¤ologique du Hainaut, for his generous loan of several specimens to Professor C. Dupuis, 14. Conclusions and Professor N. Vandenberghe for providing the original picture of the Goudberg Section. Special The fossil forest deposit of Goudberg^Overlaar, thanks are due to Mr. J. Kerkhof and Mr. H. at Hoegaarden, has been known since the middle Mestdagh (Vlaamse Landmaatschappij) and Mr. of the nineteenth century. For the ¢rst time an C. Van Du¡el (TUC rail society) for logistic help anatomical analysis of the silici¢ed stumps and in the ¢eld. We also thank Dr. Catherine Prive¤- trunk fragments allows their attribution to a sin- Gill for her advice in determining the fossil sec- gle taxon. The anatomical structure of the second- ondary xylem, Dr. Philippe Steemans for his help ary wood specimens shows characteristics shared in preparing the manuscript, Mr. Stefaan Van Si- by Taxodioxylon gypsaceum and Glyptostroboxy- maeys for additional information on the palyno- lon tenerum, but a⁄nities with the latter are clos- morph content of some samples, and Mrs. Mar- er. We chose the conservative attribution Glypto- cella Giraldo-Martin and Mr. Fernand Noebert stroboxylon sp. for their technical support during the preparation The long lasting controversy about the autoch- of the palynological samples and thin sections. thonous or allochthonous origin of the stumps is Dr. Chris Berry kindly accepted to correct the resolved, favouring the in situ character of the English text. We would like to thank also Dr. fossil forest. Such a conclusion is based on the J.F. Basinger and Dr. I. Figueiral for their helpful upright position of the great majority of the reviews of the manuscript. This work has bene- stumps, their distribution in the ¢eld, and the ¢ted from ¢nancial support by Grant FRFC-IC embedding of the stump bases within a single lig- 2.4540.99 of the Belgian National Fund of Scien- nitic layer, implying a continuum in the fossilifer- ti¢c Research. P. Gerrienne is an FNRSResearch ous deposit. Thus, the fossil deposit corresponds Associate. to remains of a natural forest rather than to a rafted secondary accumulation of stumps. This apparently monospeci¢c population of taxodiaceous gymnosperms is suggestive of a References swamp with oscillating water table levels not dis- Bailey, I.W., Faull, A.F., 1934. Structural variability in the similar in appearance to a present-day Bald Cy- Redwood, Sequoia sempervirens, and its signi¢cance in the press dominated swamp. Such an understanding identi¢cation of fossil woods. J. Arnold Arbor. 15, 233^ of the palaeoenvironment of the Hoegaarden fos- 254. sil forest is in agreement with sedimentological Bains, S., Cor¢eld, R.M., Norris, R.D., 1999. Mechanisms of and stratigraphical data demonstrating that the climate warming at the end of the Paleocene. Science 285, 724^727. trees grew in £uctuating £uvio^lacustrine settings. Basinger, J.F., 1981. The vegetative body of Metasequoia mil- The Hoegaarden taxodiaceous swamp forest most leri from the Middle Eocene of southern British Columbia. probably developed during the IETM (formerly Can. J. Bot. 59, 2379^2410.

PALBO 2534 15-8-03 Cyaan Magenta Geel Zwart M. Fairon-Demaret et al. / Review of Palaeobotany and Palynology 126 (2003) 103^129 127

Berggren, W.A., Kent, D.V., Swisher, C.C. III, Aubry, M.-P., Gilkinet, A., 1925. Flore fossile du Lande¤nien de Huppaye. 1995. A revised Cenozoic geochronology and chronostratig- Me¤m. Soc. ge¤ol. Belg., vol. 4, pp. 5^28. raphy. In: Berggren, W.A., et al. (Eds.), Geochronology, Godinot, M., 2000. Primate diversity during the Eocene in Time Scales and Global Stratigraphic Correlation. SEPM Europe and North America and its climatic implications. Special Publications 54, pp. 129^212. In: Schmitz, B., et al. (Eds.), Early Paleogene Warm Cli- Besse, J., Courtillot, V., 1991. Revised and synthetic apparent mates and Biosphere Dynamics. GFF 122, pp. 60^61. polar wander paths of the African, Eurasian, North Amer- Gothan, W., 1905. Zur Anatomie lebender und fossiler Gym- ican and Indian plates, and true polar wander since 200 Ma. nospermen-Ho«lzer. Abh. preuss. geol. Landesanst. 44, 1^ J. Geophys. Res. 96, 4029^4050. 108. Bone, D.A., 1986. The stratigraphy of the Reading Beds (Pa- Gottwald, H., 1992. Ho«lzer aus marinen Sanden des oberen laeocene), at Felpham, West Sussex. Tert. Res. 8, 17^32. Eoza«n von Helmstedt (Niedersachsen). Palaeontographica B Bowen, G.J., Koch, P.L., Gingerich, P.D., Norris, R.D., 225, 27^103. Bains, S., Cor¢eld, R.M., 2001. Re¢ned isotope stratigraphy Greguss, P., 1955. Identi¢cation of living Gymnosperms on the across the continental Paleocene^Eocene boundary on Pole- basis of xylotomy. Akade¤miai Kiado¤, Budapest. cat Bench in the Northern Bighorn Basin. In: Gingerich, Gulinck, M., 1948. Sur des phe¤nome'nes de glissement sous- P.D. (Ed.), Paleocene^Eocene Stratigraphy and Biotic aquatique et quelques structures particulie'res dans les sables Change in the Bighorn and Clarks Fork Basins, Wyoming. lande¤niens. Bull. Soc. belg. Ge¤ol. Pale¤ontol. Hydrol. 57 (1), Papers on Paleontology 33, pp. 73^88. 12^30. Chapman, J.L., 1994. Distinguishing internal developmental Hatcher, P.G., Cli¡ord, D.G., 1997. The organic geochemistry characteristics from external palaeoenvironmental e¡ects in of coal: From plant material to coal. Organ. Geochem. 5/6, fossil wood. Rev. Palaeobot. Palynol. 81, 19^32. 251^274. Doutrelepont, H., Smith, T., Damblon, F., Smith, R., Beeck- Hauregard, F., 1999. La Transition Pale¤oce'ne^Eoce'ne dans la man, H., 1997. Un bois silici¢e¤ de peuplier de la transition re¤gion de Tirlemont (Tienen): Contribution a' la reconstitu- Pale¤oce'ne-Eoce'ne de Dormaal, Belgique. Bull. Inst. r. Sci. tion des pale¤onenvironnements continentaux. M.Sc. Thesis, nat. Belg. Sci. Terre 67, 183^188. Universite¤ de Lie'ge, 59 pp. Dupuis, C., Steurbaut, E., De Coninck, J., Riveline, J., 1998. Henry, A., McIntyre, M., 1926. The swamp cypresses, Glyp- The Western Argiles a' lignite facies. Cap-d’Ailly sections. tostrobus of China and Taxodium of America, with notes on In: Thiry, M., Dupuis, C. (Eds.), The Palaeocene/Eocene allied genera. Proc. R. Irish Acad. 37, B, 90^124. boundary in Paris Basin: The Sparnacian deposits. Field Huard, J., 1966. Etude anatomique des bois de conife'res des Trip Guide, Ecole des Mines de Paris, Me¤m. Sci. Terre 34 couches a' lignite ne¤oge'nes des Landes. Me¤m. Soc. ge¤ol. Fr. (9), pp. 60^71. (nouv. se¤r.) 105, 85 pp. Ellison, R.A., Knox, R.W.O’B., Jolley, D.W., King, C., 1994. Karowe, A.L., Je¡erson, T.H., 1987. Burial of trees by erup- A revision of the lithostratigraphical classi¢cation of the tion of Mount St. Helens, Washington: Implications for the early Palaeogene strata of the London Basin and East An- interpretation of fossil forests. Geol. Mag. 124, 191^204. glia. Proc. Geol. Assoc. 105, 187^197. Kester, P.R., 2000. Tracking the radiation and regional extinc- Fairon-Demaret, M., Smith, T., 2002. Fruits and seeds from tions of the genus Cunninghamia (Taxodiaceae) (abstract). the Tienen Formation at Dormaal, Paleocene^Eocene tran- Am. J. Bot. 87, 81. sition in eastern Belgium. Rev. Palaeobot. Palynol. 122, 47^ Kim, Y.S., Singh, A.P., 2000. Micromorphological character- 62. istics of wood biodegradation in wet environments: A re- Farjon, A., 1998. World checklist and bibliography of Coni- view. IAWA J. 21, 135^155. fers. The Royal Botanical Gardens, Kew. Knobloch, E., Mai, D.H., 1986. Monographie der Fruchte und Figueiral, I., Mosbrugger, V., 2000. A review of charcoal anal- Samen in der Kreide von Mitteleuropa. Rozpr. Ustred. Ust. ysis as a tool for assessing Quaternary and Tertiary environ- Geol. Praha 47, 1^219. ments: Achievements and limits. Palaeogeogr. Palaeoclima- Koch, P.L., Zachos, J.C., Gingerich, P.D., 1992. Correlation tol. Palaeoecol. 164, 397^407. between isotope records in marine and continental carbon Figueiral, I., Mosbrugger, V., Rowe, N.P., Ashraf, A.R., reservoirs near the Palaeocene/Eocene boubdary. Nature Utesher, T., Jones, T.P., 1999. The Miocene peat-forming 358, 319^322. vegetation of northwestern Germany: An analysis of wood Kra«usel, R., 1949. Die fossile Koniferenho«lzer, II Teil. Kriti- remains and comparision with previous palynological inter- sche Untersuchungen zur diagnostik lebender und fossiler pretations. Rev. Paleobot. Palynol. 104, 239^266. Koniferenho«lzer. Palaeontographica B 89, 83^203. Fowler, K., Edwards, N., Brett, D.W., 1973. In situ coniferous Kuczumov, A., Vekemans, B., Schalm, O., Dorrine¤, W., Che- (Taxodiaceous) tree remains in the Upper Eocene of south- vallier, P., Dillmann, P., Ro, C.-U., Janssens, K., Van ern England. Palaeontology 16, 205^217. Grieken, R., 1999. Analyses of petri¢ed wood by electron, Gadek, P.A., Alpers, D.L., Heslewood, M.A., Quinn, C.J., X-ray and optical microprobes. J. Anal. At. Spectrom. 14, 2000. Relationships within Cupressaceae sensu lato: A com- 435^446. bined morphological and molecular approach. Am. J. Bot. Kusumi, J., Tsumura, Y., Yoshimaru, H., Tachida, H., 2000. 87, 1044^1057. Phylogenetic relationships in Taxodiaceae and Cupressaceae

PALBO 2534 15-8-03 Cyaan Magenta Geel Zwart 128 M. Fairon-Demaret et al. / Review of Palaeobotany and Palynology 126 (2003) 103^129

sensu stricto based on matK gene, chlL gene, tmL^tmF IGS ogy for the Palaeocene/Eocene transition. In: Schmitz, B., et region, and tmL intron sequences. Am. J. Bot. 87, 1480^ al. (Eds.), Early Paleogene Warm Climates and Biosphere 1488. Dynamics. GFF 122, pp. 117^118. Ledoux, A., 1910. Sur une fore“t fossile du Lande¤nien supe¤rieur Ostojski, D., 2001. Etude palynologique de la transition Pale¤o- a' Overlaer lez-Tirlemont. Ann. Soc. ge¤ol. Belg. 37, M39^ ce'ne^Eoce'ne dans les de¤po“ts continentaux de Morialme¤ et M45. de Lincent: Contribution a' la reconstitution des milieux Li, H.-L., 1953. Present distribution and habitats of the Coni- continentaux et comparaison avec les de¤po“ts lagunaires et fers and Taxads. Evolution, pp. 245^261. laguno-marins du sondage de Kallo. M.Sc. Thesis, Univer- Lu«cke, A., Helle, G., Schleser, G.H., Figueiral, I., Mosbrug- site¤ de Lie'ge, 43 pp. ger, V., Jones, T.P., Rowe, N.P., 1999. Environmental his- Peirce, A.S., 1936. Anatomical interrelationships of the Taxo- tory of the German Lower Rhine Embayment during the diaceae. Trop. Woods 46, 1^15. Middle Miocene as re£ected by carbon isotopes in brown Petricevic, D., 2000. Etude des micro- et macrofossiles ve¤ge¤- coal. Palaeogeogr. Palaeoclimatol. Palaeoecol. 154, 339^352. taux de la Transition Pale¤oce'ne^Eoce'ne (Tertiaire) de Leval Luterbacher, H.P., Hardenbol, J., Schmitz, B., 2000. Decision (Bassin de Mons, Belgique). M.Sc. Thesis, Universite¤ de of the voting members of the International Subcommission Lie'ge, 53 pp. on Paleogene Stratigraphy on the criterion for the recogni- Rutot, A., 1887. Course ge¤ologique du 28 aou“t 1887 d’Esemael tion of the Paleocene/Eocene boundary. Newslett. Int. Sub- a' Tirlemont par Grossoncourt, Autgaerden et Hoegaerden. comm. Paleogene Stratigr. 9, p. 13. Bull. Soc. belg. Ge¤ol. 1 (Proce's-verbal), pp. 171^177. Lyell, C., 1852. On the Tertiary strata of Belgium and French Scho«nfeld, G., 1955. Die Kieselho«lzer aus der Braunkohle von Flanders, Part II. The Lower Tertiary of Belgium. Quart. J. Bo«hlen bei Leipzig. Palaeontographica B 99, 1^83. Geol. Soc. Lond. 8, 277^370. Schwarz, O., Weide, E., 1962. Systematische Revision der Gat- Magioncalda, R., Dupuis, C., Blamart, D., Fairon-Demaret, tung Sequoia Endl. Feddes Repert. 66, 159^192. M., Perreau, M., Renard, M., Riveline, J., Roche, M., Kep- Sintubin, M., Laga, P., Vandenberghe, N., Kenis, I., Dusar, pens, E., 2001a. L’excursion isotopique du carbone organi- M., 2000. Deformation features in Paleogene sands in the que (N13Corg) dans les pale¤oenvironnements continentaux de Hoegaarden area (Belgium). Geol. Belg. 3, 257^269. l’intervalle Pale¤oce'ne/Eoce'ne de Varengeville (Haute Nor- Smith, T., 2000. Mammals from the Paleocene^Eocene transi- mandie). Bull. Soc. ge¤ol. Fr. 172, 349^358. tion in Belgium (Tienen Formation, MP7): Palaeobiogeo- Magioncalda, R., Dupuis, C., Steurbaut, E., Van Simaeys, S., graphical and biostratigraphical implications. GFF 122, De Coninck, J. 2001b. The Palaeocene/Eocene C.I.E. in con- 148^149. tinental organic carbon in the Paris Basin (Haute-Norman- Smith, T., Smith, R., 1996. Synthe'se des donne¤es actuelles sur die). Climate and Biota of the Early Paleogene. Abstracts les verte¤bre¤s de la transition Pale¤oce'ne^Eoce'ne de Dormaal International Meeting, July 3^8, 2001, Northwest College, (Belgique). Bull. Soc. belg. Ge¤ol. 104, 119^131. Powell, WY, p. 61. Smith, R., Smith, T., Steurbaut, E., 1999. Les e¤lasmobranches Mai, D., 1995. Tertia«re Vegetationsgeschichte Europas. Gus- de la transition Pale¤oce'ne^Eoce'ne de Dormaal (Belgique): tav Fisher, Jena. Implications biostratigraphiques et pale¤oge¤ographiques. Martin, R.E., 1999. Taphonomy ^ A Process Approach. Cam- Bull. Soc. ge¤ol. Fr. 170, 327^334. bridge Paleobiology Series 4, Cambridge University Press, Source book of Existing and Proposed Protected Areas in Cambridge. Vietnam,2001.http://www.wing-wbsj.or.jp/Vvietnam/source Marty, P., 1907. Etudes sur les ve¤ge¤taux fossiles du Trieu de _book/index.htm. Leval (Hainaut). Me¤m. Mus. r. Hist. nat. Belg. 5, 1^52. Stainier, X., 1909. Un gisement de troncs d’arbres debouts Meijer, J.J.F., 2000. Fossil woods from the Late Cretaceous dans le Lande¤nien supe¤rieur. Bull. Soc. belg. Ge¤ol. 23, Aachen Formation. Rev. Palaeobot. Palynol. 112, 297^336. 270^280. Miller, C.N., 1974. Petri¢ed cones and needle-bearing twigs of Steurbaut, E., 1998. High resolution holostratigraphy of Mid- a new taxodiaceous conifer from the Early Cretaceous of dle Paleocene to Early Eocene strata in Belgium and adja- California. Am. J. Bot. 62, 706^713. cent area. Palaeontographica A 247, 91^156. Moorkens, T., Steurbaut, E., Jutson, D., Dupuis, C., 2000. Steurbaut, E., De Coninck, J., Dupuis, C., King, C., 2000. The Knokke borehole of northwestern Belgium re-analysed: Dino£agellate cyst events and depositional history of the New data on the Paleocene/Eocene transitional strata in the Paleocene/Eocene boundary interval in the southern North southern North Sea Basin. In: Schmitz, B., et al. (Eds.), Sea Basin. GFF 122, 154^157. Early Paleogene Warm Climates and Biosphere Dynamics. Steurbaut, E., De Coninck, J., Roche, E., Smith, T., 1999. The GFF 122, pp. 111^114. Dormaal Sands and the Palaeocene/Eocene boundary in Bel- Morley, R.J., 2000. Origin and Evolution of Tropical Rain gium. Bull. Soc. ge¤ol. Fr. 170, 217^227. Forests. Wiley, Chichester, 362 pp. Steurbaut, E., Magioncalda, R., Dupuis, C., Van Simaeys, S., Norris, R.D., Ro«hl, U., 1999. Carbon cycling and chronology Roche, E., Roche, M., in press. Palynology, paleoenviron- of climate warming during the Palaeocene/Eocene transition. ments and organic carbon isotope evolution in lagoonal Pa- Nature 401, 775^778. leocene/Eocene boundary settings in North Belgium. In: Norris, R.D., Ro«hl, U., 2000. Astronomically-tuned chronol- Wing, S.L., et al. (Eds.), Causes and Consequences of Glob-

PALBO 2534 15-8-03 Cyaan Magenta Geel Zwart M. Fairon-Demaret et al. / Review of Palaeobotany and Palynology 126 (2003) 103^129 129

ally Warm Climates in the Early Paleogene. Geol. Soc. Am. Swo¡ord, D.L., 1991. PAUP: Phylogenetic Analysis Using Spec. Pap. 369. Parsimony. 3.1.1. Natural History Survey, Champaign, IL, Stewart, W.N., Rothwell, G.W., 1993. Paleobotany and the pp. 1^263. Evolution of Plants, 2nd ed. Cambridge University Press, Van den Broeck, E., Rutot, A., 1894. Carte Ge¤ologique de la Cambridge. Belgique a' 1/40.000, Meldert^Tirlemont 104, Institut carto- Stockey, R.A., Rothwell, G.W., Falder, A.B., 2001. Diversity graphique militaire. among taxodioid conifers: Metasequoia foxii sp. nov. from van der Burgh, J., 1973. Ho«lzer der niederrheinischen Braun- the Paleocene of Central Alberta, Canada. Int. J. Plant Sci. kohlenformation, 2. Ho«lzer der Braunkohlengruben ‘Maria 162, 221^234. Theresa’ zu Herzogenrath, ‘Zukunft West’ zu Eschweiler Stockmans, F., Willie're, Y., 1934. Notes sur des bois fossiles und ‘Victor’ (Zu«lpich Mitte) zu Zu«lpich. Nebst einer system- re¤colte¤s en Belgique. II. Pinuxylon pinastroides Kraus sp. III. atisch-anatomischen Bearbeitung der Gattung Pinus L. Rev. Palmoxylon bacillare Brongn. sp. IV. Glyptostroboxylon Palaeobot. Palynol. 15, 73^275. tenerum Kraus sp. Bull. Mus. r. Hist. nat. Belg. 10, 1^11. van der Burgh, J., Meijer, J.J.F., 1996. Taxodioxylon gypsa- Streel, M., 1965. Techniques de pre¤paration des roches de¤tri- ceum and its botanical a⁄nities. Curr. Sci. 75, 373^378. tiques en vue de l’analyse palynologique quantitative. Ann. Weibel, R., 1996. Petri¢ed wood from an unconsolidated sedi- Soc. ge¤ol. Belg. 88, B107^B117. ment, Voervadsbro, Denmark. Sediment. Geol. 101, 31^41. Su«ss, H., Schultka, S., 2001. First record of Glyptostroboxylon Yao, X., Taylor, T.N., Taylor, E.D., 1997. A taxodiaceous from the Upper Jurassic of Tendaguru, Tanzania. Bot. J. seed cone from the Triassic of Antarctica. Am. J. Bot. 84, Linnean Soc. 135, 421^429. 343^354. Su«ss, H., Velitzelos, E., 1997. Fossile Ho«lzer der Familie Taxo- Yao, X., Zhou, Z., Zhang, B., 1998. Reconstruction of the diaceae aus tertia«ren Schichten des Versteinerten Waldes von Jurassic conifer Sewardiodendron laxum (Taxodiaceae). Lesbos, Griechenland. Feddes Repert. 108, 1^30. Am. J. Bot. 85, 1289^1300.

PALBO 2534 15-8-03 Cyaan Magenta Geel Zwart