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American Journal of 99(4): 708–720. 2012.

T HE CONE E ATHIESTROBUS GEN. NOV.: F OSSIL EVIDENCE FOR A ORIGIN OF 1

G AR W . R OTHWELL 2,3,6 , G ENE M APES 2 , R UTH A . S TOCKEY 3,4 AND J ASON H ILTON 5

2 Department of Environmental and Biology, Ohio University, Athens, Ohio 45701 USA; 3 Department of Botany and , Oregon State University, Corvallis, Oregon 97331 USA; 4 Department of Biological Sciences, University of Alberta, Edmonton, AB, T6G 2E9, Canada; and 5 School of Geography, Earth and Environmental Sciences, University of Birmingham, Edgbaston, Birmingham, B15 2TT, UK

• Premise of the study: Pinaceae and nonpinoid are sister groups within the clade as inferred from molecular systematic comparisons of living species and therefore should have comparable geological ages. However, the record for the nonpinoid lineage of extant conifer families is , nearly 100 million years older than the oldest widely accepted Lower record for Pinaceae. An anatomically preserved fossil conifer seed cone described here extends the strati- graphic range of Pinaceae nearly 30 million years, thus reducing the apparent discrepancy between evidence from the fossil record and inferences from systematic studies of living species. • Methods: Material was prepared as serial thin sections by the acetate peel technique, mounted on microscope slides, and viewed and photographed using transmitted light. • Key results: A large cylindrical cone consisting of bract-scale complexes that diverge from the cone axis in a helical phyllotaxis has bracts and scales that separate from each other in the midregion and are of equal length and of nearly equal width. The cone has two inverted and winged that are attached to the adaxial surface of each cone scale and, thus, represents an early member of the Pinaceae. • Conclusions: Eathiestrobus mackenziei gen. et sp. nov. extends the fossil record for well-documented members of the Pinaceae from the Lower Cretaceous to the Kimmeridgian Stage of the Upper Jurassic. This species also clarifi es the set of char- acters that are diagnostic for seed cones of Pinaceae and reveals possible plesiomorphic characters for seed cones of the family.

Key words: Coniferales; Eathiestrobus ; fossil; Jurassic; Pinaceae; seed plant phylogeny.

Conifers are among the most diverse and economically im- group families ( Quinn et al., 2002 ; Rai et al., 2008 ), but a fossil portant of all seed . The clade is represented by a rich record has not been well established for Pinaceae before the fossil record that extends back over 300 million years to the Cretaceous, which is long after diversifi cation of most other Period ( Rothwell et al., 1997 ; Taylor et al., modern conifer families (e.g., , Escapa, 2009; 2009 ) and contributes a major proportion of the biomass for , Stockey et al., 2005; , Townrow, and Tertiary coals worldwide. The overall pattern of 1967). Moreover, primitive extend back to the conifer phylogeny is currently the subject of intense interest Pennsylvanian Period ( Rothwell et al., 1997 , 2005 ), revealing and study, with several interrelated approaches each contribut- that Pinaceae is not basal within the conifer clade as a whole. ing to a growing understanding of relationships among extinct This stratigraphic distribution of conifer species emphasizes and living families (e.g., Gadek et al., 2000; Quinn et al., 2002; that paleontological evidence is vital for resolving the overall Rothwell et al., 2005, 2011; Rai et al., 2008; Mathews, 2009; pattern of conifer phylogeny. Groth et al., 2011 ; Escapa et al., 2012 ). In this study, we describe Eathiestrobus mackenziei gen. Molecular phylogenetic studies of living conifers have con- et sp. nov. as the oldest conclusive fossil evidence for the family cluded that Pinaceae forms the sister group to all other crown Pinaceae. This is the third (i.e., Rothwell et al., 2011; Escapa et al., 2012 ) in a series of several studies to characterize anatomically

1 preserved conifer seed cones collected from Jurassic and Manuscript received 19 December 2011; revision accepted 8 February 2012. Cretaceous deposits in eastern and western Scotland, Patagonia The authors thank Andrew R. Rees (University of Birmingham) for collecting assistance and Lyall Anderson (formerly National Museums of (), North America, and Japan. The purpose of this and Scotland, Edinburgh) and Jeff Liston (formerly Hunterian Museum, related investigations is to elucidate the features of previously Glasgow) for access to specimens and literature related to this investigation. described fossil conifer seed cones and to characterize several Dr. Ignacio Escapa, Museo Feruglio, Trelew, Argentina provided valuable new extinct species that provide information about the evolu- discussions of extinct conifer structure and systematics. The drawings in tion of crown group morphologies and anatomy. Additional Figs. 19 and 20 were rendered by Danette Pratt, Ohio University. This goals of the research are to reveal the existence of novel combi- study was supported in part by the National Science Foundation, USA nations of characters in extinct species and to clarify the earliest (NSF Grant No. EF-0629819 to G.W.R., G.M., and R.A.S.), National evidence of species that conform to modern conifer families. Science and Engineering Research Council of Canada (NSERC Grant The cumulative goal of these studies is to employ these new A-6908 to R.A.S.), and the Natural Environment Research Council, UK (NERC Grant NE/E004369/1 to J.H.). data to test current hypotheses of conifer systematics that are 6 Author for correspondence (e-mail: [email protected]) , phone: 740- based on living species only and to clarify the overall pattern of 593-1129 conifer phylogeny. With this study, we extend the fossil record of well-documented Pinaceae into the Jurassic and reveal char- doi:10.3732/ajb.1100595 acters that may be plesiomorphic within the family.

American Journal of Botany 99(4): 708–720, 2012; http://www.amjbot.org/ © 2012 Botanical Society of America 708 April 2012] ROTHWELL ET AL. — JURASSIC PINACEOUS SEED 709

MATERIALS AND METHODS Collecting locality— Coastal exposures at Eathie on the Black Isle, NE Scotland ( Riding, 2005 ; Rothwell et al., 2011 ). The holotype of Eathiestrobus mackenziei consists of an incomplete seed cone preserved by cellular permineralization within a carbonate marine concre- Stratigraphic position and age— Kimmeridge Clay Formation, tion that is split open exposing slightly more than half of the specimen in longi- Lower Kimmeridgian Stage, Upper Jurassic ( Riding, 2005 ; tudinal view ( Fig. 1 ). The cone was labeled as Pityostrobus sp. at the Hunterian Rothwell et al., 2011 ). Museum, Glasgow, Scotland, UK, and bears collection number Pb 483. We photographed the specimen, made casts of the nodule to preserve the originally exposed features of the cone, and then cut the cone transversely into four seg- Etymology— The specifi c epithet mackenziei honors Mr. W. ments. Serial sections were made from all transverse surfaces of the cone seg- Mackenzie, Procurator Fiscal, County Buildings, Dingwall, ments using the cellulose acetate peel technique (Joy et al., 1956). One segment Scotland, who collected the specimen and donated it to the was subsequently recut and peeled for longitudinal sections. Hunterian Museum in 1896. Peels for microscopic examination and image capture were mounted on mi- croscope slides with Eukitt (O. Kindler GmbH, Freiburg, Germany). Images were captured with Microlumina ( Systems, Bedford, Massachusetts, USA) and Photophase (Phase One A/S, Frederiksberg, Denmark) digital scan- RESULTS ning cameras and processed with Adobe Photoshop (San Jose, California, USA). Specimens, specimen casts, peels, and microscope slides are housed at General features — The cone was exposed in longitudinal the Hunterian Museum, Glasgow, Scotland, UK. view showing numerous imbricating bract-scale complexes di- verging from an axis at 40– 50 ° (Fig. 1), tapering, and terminat- ing as thin tips (Figs. 1– 4 ). The specimen is cylindrical (Figs. 1, SYSTEMATICS 20a ), measuring 8 cm long and 3.3 cm wide, with a broad axis ca. 1 cm wide ( Figs. 1 – 3 ). Although the cone tapers toward — Coniferales both ends, it is missing the apex and base ( Fig. 1 ). Histological preservation is uneven across the cone, requiring that the best- Family — Pinaceae Lindley preserved areas from different sections be integrated to inter- pret fi ne details of structure. Cross sections show that slightly — Eathiestrobus Rothwell, Mapes, Stockey et Hilton more than half of the cone is present (Fig. 2). There is a paren- gen. nov. chymatous pith surrounded by a large number of small cauline bundles and diverging traces ( Figs. 2, 5 ). Bracts are fused to the Generic diagnosis — Cylindrical conifer seed cones with nu- scales basally, separating at the midregion from the margin in- merous, helically arranged bracts and axillary ovuliferous ward (Figs. 6, 9, 12, 19). Two, winged seeds are attached to the scales; bracts and scales fused to midregion, both thinning dis- adaxial surface near the midlevel of the ovuliferous scale, and tally and marginally and of nearly equivalent length, width, and in the region of bract-scale separation ( Figs. 2, 3, 6 – 11, 19, 20C ). thickness. Cone axis with little ; prominent pith sur- Individual seeds are inverted and attached at their base (Figs. 7, rounded by small cauline bundles; bract trace diverging as 8, 11, 19, 20C ). terete bundle, subtending two small traces to ovuliferous scale; cortex parenchymatous with numerous canals. Bract and Cone axis — The cone axis has a prominent parenchymatous scale separation lateral; seeds, two, inverted, asymmetrical, at- pith that is 3.2 – 3.7 mm in diameter, consisting primarily of dis- tached to adaxial surface of ovuliferous scale in region of bract- torted and broken cells with dark thin walls and light-colored ovuliferous scale separation. Interseminal ridge small. Seed lumens (Figs. 2, 5, 6). A smaller number of cells have dark am- attached basally, wing consisting of scale , extending ba- ber contents. In cross sections, a few cells at the periphery of the sally and to side of seed facing periphery of scale. pith appear less distorted and have thicker walls (Fig. 13, at ar- row), revealing the occurrence of sclereids in the region. The Etymology — Referring to the collecting locality near Eathie, stele consists of numerous small cauline bundles and traces, Scotland, and “ strobus ” for cone. with almost no secondary xylem development (Figs. 2, 5, 6, 13). The pattern of trace divergence is helical. Each bract-scale com- Type species — Eathiestrobus mackenziei Rothwell, Stockey, plex is vascularized by a single bract trace (Fig. 13, 14) and two Mapes et Hilton sp. nov.; Figs. 1 – 18 . small ovuliferous scale traces ( Figs. 15, 16 , at arrows). Cauline bundles measure up to 270 µ m in diameter and consist of tra- Specifi c diagnosis — Cone > 8 cm long and 3.3 cm wide, with cheids that have either scalariform thickenings or uniseriate, axis ca. 1 cm wide. Pith parenchymatous. Bracts and scales di- circular bordered pits (Fig. 17). Most tracheids are randomly verging at angle of 40 – 50° , each ca. 2.8 cm long, becoming wider arranged, but the occurrence of a few radially aligned tracheids and thinner distally. Ovuliferous scales up to 10 mm wide; bracts (Fig. 13) suggests that there has been a small amount of second- up to 8 mm wide; both terminating in rounded, papery thin api- ary growth. Protoxylem tracheids have not been identifi ed. ces. Bracts with one terete and both abaxial and The cortex is differentiated into an inner zone of light-col- adaxial sclerenchyma; ovuliferous scales with two terete vascular ored cells and an outer zone of dark cells (Figs. 2, 6, 12), all of bundles and abaxial sclerenchyma. Small resin canals in cortex which are thin-walled parenchyma. Numerous resin canals oc- of cone axis continue distally as single row at center of bract and cur throughout the cortex ( Fig. 12 ), extending into both the single row at center of ovuliferous scale. Seed body ca. 4.6 mm bracts and scales (Fig. 4). Individual cortical resin canals are ca. long, 2.8 mm wide, excluding basal and lateral wing. 0.25 mm in diameter, dilating slightly at branching to ca. 0.4 mm in diameter ( Fig. 12 , at arrows). Holotype hic designatus— Permineralized slabs, peels, and slides of specimen No. Pb 483, housed in the Hunterian Mu- Bract-scale complexes — Bracts and scales are each ca. 2.8 cm seum, Glasgow, Scotland ( Figs. 1 – 18 ). long, becoming wider and thinner distally ( Figs. 1 – 4 ). Both 710 AMERICAN JOURNAL OF BOTANY [Vol. 99

Figs. 1 – 5. Eathiestrobus mackenziei Rothwell, Mapes, Stockey, et Hilton gen. et sp. nov. All fi gs. of holotype (Pb 483). 1. Split surface of nodule showing cone interior in longitudinal view. Horizontal line indicates extent of broad cone axis with parenchymatous pith (p) at center. Note positions of seeds (s). × 2. Scale bar = 1 cm. 2. Cross section at cone midregion showing general features. Note ring of small xylem bundles surrounding shrunken parenchymatous pith (p), broad cortex of axis, and diverging bract-scale complexes; each ovuliferous scale bears two seeds (at arrowheads). C Top #47 × 4. Scale bar = 1 cm. 3. Radial section of cone showing general features. Note broad axis (a), angle of divergence of bract-scale complexes, thin distal tips of bracts and ovuliferous scales, and position of attachment of inverted seed (s). C2 Side #48 × 4. Scale bar = 1 cm. 4. Cross section of cone showing ovulifer- ous scales (os) and subtending bracts (b) at several levels. Most proximal bract-scale complex (at bottom) is sectioned distal to attachment of seed (s) and separation of bract from scale. Note keel of bract at that level, and resin canals (r) in both bracts and ovuliferous scales. B Bot #69 ×12.5. Scale bar = 2 mm. 5. Cross section of cone axis showing parenchymatous pith (p) surrounded by cauline bundles of the stele, and diverging traces, several of which are identi- fi ed by arrowheads. Note incompletely preserved parenchymatous cortex at top. C Top #77 × 15. Scale bar = 2 mm. April 2012] ROTHWELL ET AL. — JURASSIC PINACEOUS SEED 711

Figs. 6 – 10. Eathiestrobus mackenziei Rothwell, Mapes, Stockey et Hilton gen. et sp. nov. All fi gs. of holotype (Pb 483). 6. Cross section of cone show- ing diverging bract-scale complexes (at arrowheads), and more distal bract-scale complexes with pairs of attached seeds (s). Note pith (p) of cone axis with minimal wood, at bottom. C Top #32 × 7. Scale bar = 5 mm. 7. Bract-scale complex in longitudinal view with attached seed (s). Position of seed attachment identifi ed by arrowhead. Note resin canal (r) in longitudinal section, distal to seed attachment. C2 Side #37 ×15. Scale bar = 2 mm. 8. Longitudinal section of cone showing attachment of seed (s). Note position of seed wing (w) and ovuliferous scale (os). Bract (b) and scale fused proximal to seed attachment.

C 2 Side #48 ×15. Scale bar = 2 mm. 9. Cross section of bract-scale complex with two seeds (s). Note bract (b) and ovuliferous scale (os) separated at mar- gins, but still fused at center (arrowhead) at this level. C Top #32 × 14. Scale bar = 2 mm. 10. Cross section near base of broken seed showing sclerotesta (sc) and wing (w). Wing and ovuliferous scale (os) were originally attached, but are broken apart in this view. B Bot #17 × 15. Scale bar = 2 mm. 712 AMERICAN JOURNAL OF BOTANY [Vol. 99

Figs. 11 – 18. Eathiestrobus mackenziei Rothwell, Mapes, Stockey et Hilton gen. et sp. nov. All fi gs. of holotype (Pb 483). 11. Longitudinal section of attached seed with apex at left, showing histology of seed wing (w), integument (sa, sarcotesta; sc, sclerotesta) and nucellus (n). Note seed attached to ovuliferous scale (os) only at chalaza. m, micropyle. C2 Side #46 × 33. Scale bar = 1 mm. 12. Cross section at level where bract-scale complex is beginning to diverge. Note bract (b) has begun to separate from ovuliferous scale (os) at lateral margins. Cortex with which ovuliferous scale is still continuous (at bottom) displays numerous resin canals (r). Some resin canals show septation below level of division (at arrows). Note also well-developed row of resin canals at margin of cortical parenchyma and marginal (abaxial) zone of cells with incompletely preserved walls and distinctly dark contents in ovuliferous scale. B Bot #19 × 22. Scale bar = 1 mm. 13. Cross section at margin of stele in cone axis showing cauline bundles (cb) and one bract trace (bt) distal to level of divergence. Radial alignment of tracheids in bract trace suggests scanty development of secondary xylem. Note a small number of cells near pe- riphery of pith are thick walled (at arrow). C2 Top #42 × 78. Scale bar = 250 µ m. 14. Cross section of bract distal to divergence from ovuliferous scale showing bract trace (bt), resin canals (r), and sclerenchyma toward both abaxial and adaxial margins. Arrow identifi es papillate abaxial . B Bot #49 × 80. Scale bar = 250 µ m. 15. Enlargement of bract-scale complex comparable to area at upper right of Fig. 12 , showing bract (b) and ovuliferous scale (os) at level where margins have separated (at right) but are still connected at center of complex (at left). Arrows identify pair of ovuliferous scale traces. C Top #77 × 32. Scale bar = 1 mm. 16. Pair of ovuliferous scale traces (arrows) in cortex of cone axis, proximal to level of traces in Fig. 15 . C Top #42 × 90. Scale bar = 250 µ m. 17. Longitudinal section of cone axis showing tracheids of cauline bundle with incompletely preserved scalariform thickenings and bordered pits. C 2 Side #17 ×225. Scale bar = 100 µ m. 18. Enlargement of ovuliferous scale trace at right in Fig. 15 showing scalariform thickenings of tracheid walls. C2 Top #77 × 280. Scale bar = 100 µ m. April 2012] ROTHWELL ET AL. — JURASSIC PINACEOUS SEED 713

Fig. 19. Eathiestrobus mackenziei Rothwell, Mapes, Stockey et Hil- ton gen. et sp. nov. Diagrammatic reconstruction of bract/ovuliferous scale in midlongitudinal section, showing degree of fusion of bract to ovulifer- ous scale and attachment of inverted winged seed. broaden toward the midregion of the complex, with ovuliferous scales becoming slightly wider (10 mm) than bracts (8 mm) before both taper gently and terminate in rounded apices ( Fig. 20C ) that are papery thin ( Figs. 4, 9, 19 ). In the midregion, the bract dis- plays a small keel ( Figs. 4, 20C ) and a papillate abaxial epider- mis ( Fig. 14 , at arrow). Internally, the bract consists of abaxial and adaxial hypodermal sclerenchyma with parenchyma in the central region ( Figs. 4, 9, 14 ). The bract trace is terete ( Fig. 14 ) and measures ca. 100 µ m in diameter. Bract-scale complexes originate as radial expansions of the Fig. 20. Eathiestrobus mackenziei Rothwell, Mapes, Stockey et Hil- cone axis ( Figs. 2, 12 ). Each bract-scale complex separates ton gen. et sp. nov. Reconstructions of (A) cone and bract/ovuliferous scale from the cortex beginning from the margins and progressing complex in (B) abaxial and (C) adaxial views. toward the center ( Fig. 12 ). The bract begins to separate from the scale in the same region ( Fig. 4 ), but the separation is not complete ( Fig. 9 , at arrowhead) until somewhat distal to the ( Fig. 12 ). Distal to the level of separation, ovuliferous scale tis- level of seed attachment. Separation begins at the margins and sues are less completely preserved, but the tissue zones and the progresses distally toward the center of the bract-scale complex row of resin canals can still be identifi ed ( Figs. 4, 9 ). Vascular- ( Figs. 4, 9, 12 ). ization of the ovuliferous scale is by two terete bundles ( Fig. 16 , Near the base of the complex, the bract is easily distinguished at arrows) that separate from the stele of the cone axis immedi- from the scale by lighter-colored parenchymatous cells ( Fig. 12 ). ately distal to divergence of the bract trace. The two xylem At this level, the bract consists of relatively uniform paren- bundles extend distally to the level of seed attachment within chyma tissue in which resin canals are diffi cult to identify. In lacunae that probably represent the position of phloem and as- somewhat more distal sections, a single row of resin canals be- sociated parenchyma cells that are not preserved ( Fig. 15 ). In comes apparent within the parenchymatous . more distal sections, only the lacunae can be identifi ed. Scale Resin canals are located slightly closer to the abaxial surface traces range 70– 120 µ m in diameter and consist of tracheids than to the adaxial surface of the bract ( Figs. 4, 9, 14 ). with scalariform thickenings ( Fig. 18 ). Proximal to the level of bract-scale separation, the ovulifer- ous scale displays an abaxial sclerotic zone and an incompletely Seeds — Two inverted seeds are attached to the adaxial sur- preserved parenchymatous adaxial zone (Fig. 12). A single row face of the scale in the midregion (Figs. 2, 6, 9) and are sepa- of prominent resin canals occurs at the juncture of the zones rated by a small amount of interseminal tissue ( Figs. 2, 6, 9 ). 714 AMERICAN JOURNAL OF BOTANY [Vol. 99

T ABLE 1. Systematically informative seed cone characters of fossil and living conifers. Characters for Eathiestrobus mackenziei and concordant characters of other taxa are in boldface.

Bract vs. ovuliferous Characters Taxon Age Family Cone Shape Size (cm) Bract/scale Fusion scale trace length

Telemachus/ Triassic Voltziaceae ovoid or ellipsoidal 3.0-3.4 × 1.2- 1.4 except at tipequal Parasciadopitys

Eathiestrobus Jurassic Pinaceae cylindrical 8 × 3.3 ½ fused equal mackenziei

Hughmillerites Jurassic Cupressaceae ovoid or ellipsoidal 3.0-4.3 × 2.2- 3.6 except at tip longer than scale juddii

Pararaucaria Jurassic ovoid, conical or 5.1 × 3.0 unfused or at base onlyequal ? patagonica cylindrical Pinus Cretaceous Pinaceae ovoid or ellipsoidal 4.5 × 3.0 unfused or at base only shorter than scale belgica

Pityostrobus Cretaceous Pinaceae cylindrical 6.5 × 3.3 unfused or at base only shorter than scale californiensis

Cunninghamiostrobus Cretaceous Cupressaceaecylindrical 6.5+ × 2.5 throughout longer than scale yubariensis

Sciadopitys Cretaceous Sciadopityaceaecylindrical 5.9 × 4.5 2/3 fusedequal yezo-koshizakae

Sciadopityostrobus kerae Cretaceous Sciadopityaceaecylindrical 3 × 2.4 3/4 fused shorter than scale

Picea chihuahuana Extant Pinaceae cylindrical 10.0- 17.0 × 4.0-5.0 1/2-2/3 fused shorter than scale

Pseudolarix amabilis Extant Pinaceae ellipsoidal 4.0-8.0 × 8.8- 5.5 1/2 fused shorter than scale

Sciadopitys verticillata Extant Sciadopityaceaecylindrical 3.5-11 × 2.5- 5.0 except at tipequal

Taiwania cryptomerioides Extant Cupressaceae ellipsoidal to cylindrical (0.9-) 1.4-2.0 throughout longer than scale (-2.5) × 0.6- 1.1

1 Seed shape based on Parasciadopitys ( Yao et al., 1997 ). 2 Seed symmetry recorded from shape that includes wing (regardless of histological origin of wing). 3 Seeds with 180 ° rotational symmetry appear to have a narrow wing in the major plane due to their shape. In this species, the thickness of the integument at the position of the putative wing is only sometimes somewhat thicker than a subtle wing (see Figs. 6 and 7 of Ohana and Kimura [1995] ).

Each seed is asymmetrical with prominent sclerotesta and a equal size and thickness (Fig. 20A). Bracts and scales separate single lateral/basal wing ( Figs. 6, 8 – 10 ) comprised of paren- from each other, from the margin toward the center, in the chymatous scale tissue (Fig. 8, 10, 11). The seed body measures midregion of the bract-scale complex. Two inverted seeds are 2.9– 3.4 mm long and 1.2– 2.0 mm wide. The micropyle is ori- adaxially attached to each ovuliferous scale; each displays a ented toward the cone axis (Fig. 11, at m). Sclerotesta consists single lateral/basal wing derived from scale tissue (Figs. 19, of several layers of dark thick-walled cells ( Figs. 8, 11 ). Sar- 20C). There is a low interseminal ridge of scale tissue between cotesta is composed of a narrow zone of thin-walled cells (Fig. 11) the seeds. The cone axis is largely parenchymatous, with a ring that is attached to tissue of the wing (Fig. 10) at the chalaza of small and separate cauline bundles that produce very little (Figs. 8, 11). The nucellus is attached at the chalaza and appears secondary xylem. A single terete bract trace and two small scale to be free distally ( Figs. 8, 11 ), but the separation may be tapho- traces vascularize each bract-scale complex. Resin canals are nomic. No chamber has been identifi ed. present in the cone axis at the base of each complex, extending into the bract and the scale as a single row in each. Among the families of living and extinct conifers that pro- DISCUSSION duce large, compact, cylindrical cones with helically arranged bract-scale complexes, Eathiestrobus mackenziei is most simi- Eathiestrobus mackenziei is represented by a relatively large lar to those of Pinaceae, Cheirolepidiaceae, and Sciadopityaceae ( > 8 cm long) cylindrical seed cone with well-developed bracts ( Table 1 ). While some podocarps, (e.g., Saxegothaea ) produce and ovuliferous scales that are helically arranged and of relatively strobiloid seed cones and some seed cones of the taxodioid April 2012] ROTHWELL ET AL. — JURASSIC PINACEOUS SEED 715

Relative thickness Prominent of bract and abaxial bract Bract Apical lobes of # Seeds/ ovuliferous scale lobe ornamentation ovuliferous scale scale Seed position Seed orientation Seed symmetry Seed wing(s)

equal absent none present 2-5adaxial on inverted 1 180 ° rotational 2, lateral of in tegumentary scale tissue surface thicker than scale absent papillae absent 2 adaxial inverted 2 asymmetrical 1, chalazal of scale tissue on scale surface thicker than scale absent papillae present 3adaxial inverted 180 ° rotational 2, lateral of in tegumentary on scale tissue surface thinner than scaleabsent none present 1-2 in adaxial inverted 180 ° rotational absent pocket thinner than scaleabsent noneabsent 2 adaxial inverted asymmetrical 1, chalazal of scale tissue on scale surface thinner than scaleabsent noneabsent 2 adaxial inverted asymmetrical 1, chalazal of scale tissue on scale surface thicker than scaleabsent noneabsent 3 adaxial inverted 180 ° rotational3 narrow or absent on scale surface thinner than scale present present 9-13adaxial inverted ?? on scale surface equal absent trichomes present 5adaxial inverted 180 ° rotational 2, lateral of integumentary on scale tissue surface thinner than scaleabsent noneabsent 2 adaxial inverted asymmetrical 1, chalazal of scale tissue on scale surface thinner than scaleabsent noneabsent 2 adaxial inverted asymmetrical 1, chalazal of scale tissue on scale surface thinner than scaleabsent trichomes present (1-) 7-9 (-12)adaxial inverted at 180 ° rotational 2, lateral of in tegumentary on scale maturity tissue surface thicker than scale absent ?absent 2 adaxial inverted at 180 ° rotational 2, lateral of in tegumentary on scale maturity tissue surface

Cupressaceae, (e.g., some fossil Cunninghamiostrobus cones; While the number of seeds per scale is variable in some coni- Ohana and Kimura, 1995 ) can be elongate and cylindrical, the fer families, in other families (e.g., Araucariaceae and Pinaceae) basic cone structure of E. mackenziei is unlike those in cupres- seed number per scale is a diagnostic character ( Table 1 ). The soids or podocarps ( Table 1 ). Cones of Saxegothaea are fl eshy presence of two seeds per scale, as seen in E. mackenziei , oc- with prominent bracts and an aril surrounding the single , curs in Pinaceae and Cheirolepidiaceae, and occasionally in and without the prominent ovuliferous scale seen in E. mack- Sciadopityaceae and Cupressaceae ( Table 1 ; Clement-Westerhof enziei (Stiles, 1908). In species of Cunninghamiostrobus , the and van Konijnenburg-van Cittert, 1991 ). In all of these ovuliferous scale is even smaller, sometimes represented only families except Pinaceae, however, the number can be variable by a ridge of tissue distal to the seeds or free scale tips, and the in any one species and is not consistently two in any genus ex- bract is large (Ohsawa, 1994; Rothwell et al., 2011). Species of cept Taiwania . However, even Taiwania cones occasionally Araucariaceae have spherical or ovoid cones as in most taxo- have one seed per scale ( Silba, 1986 ). Cones of Taiwania lack dioid and cupressoid Cupressaceae (Stockey, 1982; Rothwell et al., a prominent ovuliferous scale, and the bract is the only structure 2011 ). In Cheirolepidiaceae, unwinged seeds occur under a seen externally, unlike the prominent ovuliferous scales pro- fl ap (Clement-Westerhof and van Konijnenburg-van Cittert, duced by E. mackenziei . 1991 ) or are enclosed in pocket ( Escapa et al., 2012) of ovulifer- Both a large bract and a large ovuliferous scale, as is charac- ous scale tissue on the adaxial surface. By contrast, the winged teristic of E. mackenziei ( Fig. 20 ), occur in Cheirolepidiaceae, seeds of E. mackenziei are borne directly on the adaxial surface Sciadopityaceae, some taxodioid Cupressaceae, and a few of the ovuliferous scale. Pinaceae (Table 1). The long tapered bract and scale of E. 716 AMERICAN JOURNAL OF BOTANY [Vol. 99

T ABLE 1. Continued.

Characters Sclerenchyma Secondary xylem in Sclerenchyma in Resin canal system Taxon in pith cone axis outer cortex in cone Resin canals in cortex

Telemachus/ absent separate strands absent absent absent Parasciadopitys Eathiestrobus absent separate strands absent interconnected with present mackenziei cortex Hughmillerites juddii absent continuous cylinderabsent discontinuous absent Pararaucaria present continuous cylinder strands accompanying absent absent patagonica trace only Pinus present continuous cylinderabsent interconnected with present belgica cortex Pityostrobus present continuous cylinder presentinterconnected with present californiensis cortex Cunninghamiostrobus present continuous cylinder presentinterconnected with present yubariensis cortex Sciadopitys absent continuous cylinderabsent interconnected with present yezo-koshizakae cortex Sciadopityostrobus absent continuous cylinder presentinterconnected with present kerae cortex Picea chihuahuana absent continuous cylinder presentinterconnected with present cortex Pseudolarix amabilis present separate strands present interconnected with present cortex Sciadopitys absen t continuous cylinder ?interconn ected with present verticillata cortex Taiwania ?? ? ? ? cryptomerioides mackenziei show no evidence of the apophysis or umbo (even and seed cones that currently are accepted as representing the though some abrasion of the cone has undoubtedly occurred) family Pinaceae (Table 1). Although the bract of Eathiestrobus that are characteristic of the genus Pinus , and bract and scale is virtually as wide as the ovuliferous scale, whereas all other are of nearly equal length ( Figs. 19, 20 ). Equal-sized bracts and species of living ( Farjon, 1984 , 1990 ) and extinct ( Smith and scales presumably also occur in Cupressaceae, but in that fam- Stockey, 2001 , 2002 ) Pinaceae have much narrower bracts, the ily, the two putatively equal-sized structures are considered to overwhelming number of concordant shared characters clearly be fused in many species (Table 1; Rothwell et al., 2011). In the places Eathiestrobus within the family Pinaceae ( Table 1 ; fossil family Cheirolepidiaceae, bract and ovuliferous scale are Miller, 1976 , 1988 ). As a result, the wide bract of E. mackenziei more or less free from each other as are the tips of Eathiestrobus , is a distinctive character that unequivocally distinguishes Eat- but the seeds are not exposed on the adaxial surface of the hiestrobus from all other genera of the Pinaceae. ovuliferous scale as they are in Eathiestrobus ( Table 1 ). In Another distinctive feature of E. mackenziei is the paucity of some species of the Cheirolepidiaceae, the ovuliferous scales secondary xylem in the cone axis. Nearly all living conifer are shed from the cone, while the bract remains attached to the cones of this size have more secondary xylem than occurs in cone axis (Jung, 1968). Since bract and ovuliferous scale are E. mackenziei . Among the living conifers with little secondary xy- approximately half fused in E. mackenziei, it is unlikely that the lem in the cone axis are those that shed their scales at maturity, ovuliferous scale would have been shed without the bract. In e.g., Abies and Cedrus ( Miller, 1976 ). Like E. mackenziei , those Sciadopityaceae, Sciadopitys verticillata has bract and ovulif- genera have separate strands of secondary rather erous scale that are fused at maturity, except at the tip (Table 1). than a continuous cylinder in the cone axis, but each has more Among fossil species of that family, Sciadopitys yezo-koshiza- secondary xylem than E. mackenziei . However, in Pseudolarix kae Ohsawa Nishida et Nishida (1991 ) and Sciadopityostrobus Gord., cones develop in a single year, have very little secondary kerae Saiki have varying amounts of fusion of the bract and scale xylem (see Miller, 1976 , pl. 1, fi g. 1 .), and the cone axis itself ( Table 1 ). As in E. mackenziei , the bract and scale of Scia dopitys disintegrates when the cone is “ ripe ” ( Farjon, 1990 ). In yezokoshizakae are equal in length. However, the bract of S. Pseudolarix amabilis (Nelson) Rehder, the pith of the cone axis yezokoshizakae is considerably thinner than the scale and has shows widely distributed sclereids interspersed with paren- an abaxial lobe that is absent from E. mackenziei ( Table 1 ). In ad- chyma cells (Miller, 1976), which upon drying allow the cone dition, all of these species of the Sciadopityaceae have trichomes axis to shrivel and the scales to separate from the axis (LePage on the bract, which are lacking in E. mackenziei ( Table 1 ). and Basinger, 1995). The Eathiestrobus cone axis is broad and A diagnostic combination of characters that includes (1) has very little secondary xylem. The cone also displays a few large cylindrical cones with numerous helically arranged bract- thick-walled sclereids near the outer margin of the pith. The scale complexes, (2) bract and scale that are distinct from each bracts have both abaxial and adaxial sclerenchyma and the ovu- other, (3) adaxially borne seeds, (4) inverted seeds, (5) consis- liferous scales have abaxial sclerenchyma, but there are no cel- tently two seeds per ovuliferous scale, and (6) seeds with single lular or in the seeds. Together, these wing of scale tissue that is located basally on the seed and on the characters suggest that the specimen may not be fully mature, and peripheral side of ovuliferous scale, occurs only in Eathie strobus they are consistent with the interpretation that Eathiestrobus April 2012] ROTHWELL ET AL. — JURASSIC PINACEOUS SEED 717

Resin canals Bract and Ovuliferous scale trace Ovuliferous scales with bract trace at ovuliferous scale # Vascular traces Derivation of ovuliferous shape in tangential vasculature at level of divergence traces separate at origin to bract Bract trace scale trace section at origin seed body

0 no1 slender from 1 strandterete row of bundles

0 yes 1 slender from 2 strands terete 2 bundles?

1 no more than 1 bundle stout absent N/A absent 0 no1 slender from 1 strand horseshoe shaped

2no 1 slender from 1 strand horseshoe shaped row of bundles

2 yes 1 slender from 1 strand horseshoe shaped row of bundles

3? no more than 1 bundle stout absent absent absent

3? no? 1 slender from 2 strands terete row of bundles

3? yes 1 stout from 1 strand abaxially concave row of bundles

1 yes 1 slender from 1 strand abaxially concave row of bundles

0 yes 1 slender from 1 strandterete row of bundles

1 yes 1 stout from 1 or 2 strands abaxially concave row of bundles

? ? more than 1 bundle stout ? ? ?

could have shed its scales at maturity in a manner that is similar members of the Gnetales (e.g., Friis et al., 2011 ), thus lending to that of extant Pseudolarix . further support for an Early Cretaceous age. With the discovery of Eathiestrobus , fossil evidence now ex- Identifi cation of the ovuliferous conifer cone scales from the tends a well-documented minimum age for the family Pinaceae Tsagan-Tsab Formation as Pseudolarix erenis Krassilov also based on both morphology and internal seed cone anatomy invites careful scrutiny. The material is described as consisting from the Lower Cretaceous (i.e., ca. 136 Ma; Stockey and of dispersed bract-scale complexes and isolated winged seeds Wiebe, 2008 ) to the Upper Jurassic (i.e., ca. 155 Ma; Fig. 21 ). that are associated with conifer vegetative remains that show This is roughly contemporaneous with the reported age of com- long-/short-shoot differentiation (plate 12, fi gs. 130, 131 pression specimens assigned to Pseudolarix erensis Krassilov and plate 13, fi gs. 143 – 167 of Krassilov, 1982 ). Two winged (1982) on the basis of dispersed bract-scale complexes and veg- seeds are clearly attached to some ovuliferous scales, but a bract etative remains from the Tsagan-Tsab Formation in Mongolia, is diffi cult to identify in the fi gure that reportedly shows that that were initially considered to be Early Cretaceous in age, but structure (plate 13, fi g. 144 of Krassilov, 1982). The fi gure in have more recently been reinterpreted as Late Jurassic by some question is identifi ed as an adaxial view of an ovuliferous scale. authors ( LePage and Basinger, 1995 ; LePage, 2003 ). Both the It has a bilobed apex, and a bilobed impression near the base age and taxonomic status of P. erensis are less certain than that is wider than it is long. A similar feature is present on the those of Eathiestrobus . specimen in plate 13, fi g. 151 of Krassilov (1982). If that fea- The Tsagan-Tsab Formation ranges from Late Jurassic to Early ture is a bract, then it is unlike the narrow, pointed bracts that Cretaceous in age and represents a diverse series of facies as- characterize all other species of Pseudolarix ( LePage and sociations that include volcanic tuffs, sandstones, shales, and marls Basinger, 1995 ). On the other hand, that bilobed feature is ex- from alluvial facies, and basalts (Krassilov, 1982; Ponomarenko tremely similar in size, shape, and position to the paired seed et al., 2009 ; Shuvalov, 2000 ). The basal parts of the Tsagan-Tsab bodies that remain attached to the ovuliferous scale of other Formation in some places are Late Jurassic in age, such as the specimens (i.e., plate 13, fi gs. 152, 153 of Krassilov, 1982 ), Suihent petrifi ed that has been dated as Late Jurassic suggesting that the specimens in question (plate 13, fi gs. 144, based on 40 Ar/ 39 Ar dating of sanadine crystals in tuffs ( Keller 151 of Krassilov, 1982) represent abaxial views of ovuliferous and Hendrix, 1997). However, the majority of the formation scales from which the seeds have been detached. is younger and Early Cretaceous in age. Ponomarenko et al. It is unclear how best to interpret the specimens that are (2009) presented a regional stratigraphic synthesis in which the described by Krassilov (1982) as Pseudolarix erensis. The three localities from which Krassilov (1982) reported Pseudola rix absence of a clear Pseudolarix -like bract from the fi gured erensis (i.e., Manlaj, Gurvan-Eren, and Bon-Tsagan) to be specimens is particularly troubling. An alternatively reason- Early Cretaceous based on regional correlation, lithostratig- able, but equally unsubstantiated, interpretation of that material raphy and biostratigraphy. When Krassilov (1982) described is that it consists of a combination of (1) ovuliferous scales the fl ora of Mongolia, he noted that P. erensis co-occurred shown from the abaxial surface that bear seeds (viz., plate 13, with angiosperms including Gurvanella Krassilov and Erenia fi gs. 152, 153 of Krassilov, 1982), (2) ovuliferous scales shown Krassilov (1982), that are now recognized as Early Cretaceous from the abaxial surface from which seeds have been shed 718 AMERICAN JOURNAL OF BOTANY [Vol. 99

Fig. 21. Minimum clade ages for conifers based on oldest well-documented fossil occurrences of crown group families and the two extant clades. , now often placed within the on the basis of molecular systematics, was omitted due to insuffi cient data. Note age disparity between earliest occurrence of for crown group pinoid and nonpinoid conifers (red and black lines, respectively, at right). Top of arrow signifi es previous widely accepted minimum age of Pinaceae from fossil evidence based on of Midoriphyllum piceoides Stockey et Wiebe (2008) , while ar- rowhead indicates oldest occurrence of family demonstrated by Eathiestrobus mackenziei . 1 = Rissikia media ( Townrow, 1967 ), 2 = Paleotaxus rediviva (Nathorst, 1908), 3 = phillipsi Carruthers (Arrondo and Petriella, 1980), 4 = Austrohamia minuta Escapa, Cuneo et Axsmith (Escapa et al., 2008), 5 = Eathiestrobus mackenziei Rothwell, Mapes, Stockey et Hilton (this paper), 6 = Sciadopitys yezo-koshizakae Ohsawa, M. Nishida et H. Nishida ( Ohsawa et al., 1991 ).

(plate 13, fi gs. 144, 151 of Krassilov, 1982), (3) ovuliferous as P. erensis apparently do not represent the genus Pseudolarix , scales shown from the adaxial surface, and (4) bracts that are they may still constitute one of the Early Cretaceous records for nearly as long and wide as the ovuliferous scales. If the latter the family Pinaceae. supposition is correct, then the bilobed specimens could be There are several additional compressed plant fossils from ovuliferous scales, while those with a rounded apex (e.g., fi gs. Triassic and Jurassic sediments that are suspected of represent- 146, 147 of Krassilov, 1982 ) could be bracts. Such an interpre- ing Pinaceae, but all continue to have equivocal familial affi ni- tation would lead to the recognition that the dispersed conifer ties (e.g., Seward, 1919). Among the most ancient of those is cone organs fi gured by Krassilov (1982) as ovuliferous scales Compsostrobus neotericus Delevoryas et Hope (1973), which are actually a combination of ovuliferous scales and bracts that is represented by lax seed cones. Those specimens occur in as- are nearly equivalent in size and shape, and thereby similar in sociation with the voltzialean seed cone, Florinostrobus an- that feature to Eathiestrobus . Although the specimens described drewsii (Delevoryas and Hope) Delevoryas and Hope, leafy April 2012] ROTHWELL ET AL. — JURASSIC PINACEOUS SEED 719 with elongated needle leaves, and pollen cones with two Pinaceae in Florin ’ s original transformational series for the evo- abaxial pollen sacs and saccate pollen from Upper Triassic de- lution of cone-scale complexes from Voltziaceae to Pinaceae posits of North Carolina ( Delevoryas and Hope, 1973 , 1975 , ( Florin, 1951 ). This suggests that the currently understood time 1987 ). The associated vegetative organs and pollen cones were frame for evolution of the pinaceous cone scale from the originally described in the same paper as C. neotericus, but it voltzialean ovuliferous dwarf shoot may be roughly accurate, but remains unclear whether such organs belong to C. neotericus , that evolution of all modern cone-scale complexes via a single or F. andrewsii, or some other conifer. The seed cones of C. transformational series ( Florin, 1951 ) is overly simplistic. As is neotericus have some characters that are reminiscent of Pinaceae emphasized by the conifer family Ferug- (i.e., helically arranged bract-scale complexes, and two inverted liocladaceae (Archangelsky and Cuneo, 1987), there has been a per ovuliferous scale; Delevoryas and Hope, 1973 ; great deal of divergent evolution among conifers since at least 1987 ), but other characters such as an attenuated micropylar the (Serbet et al., 2010). The recent proposal of a trans- canal and the absence of a seed wing are not characteristic of formational series for evolution of the cupressaceous bract- pinaceous conifers. As a result, Delevoryas and Hope assigned scale complex from that of voltzialean conifers (Rothwell et al., Compsostrobus to the family Compsostrobaceae Delevoryas 2011 ) provides evidence for the independent origin of modern and Hope (1973) . seed cone structure in Pinaceae and Cupressaceae, thus con- Schizolepis Braun is another apparently coniferous genus of fi rming that the pattern of conifer phylogeny is, indeed, more uncertain affi nities ( Seward, 1919 ) that often is compared to complex than previously interpreted ( Florin, 1951 ). Pinaceae (e.g., Wang et al., 1997 ; Zhang et al., 2011 ). Speci- While we do not yet know whether disparities between differing mens consist of bract-scale complexes that bear two inverted approaches to resolving conifer phylogeny result from an incom- seeds on the adaxial surface of a bi- or trilobed scale and that plete fossil record, or an inaccurate pattern of phylogeny inferred often form a lax cone of helically arranged bract-scale com- from systematic studies of living species only, or both, recent and plexes (Seward, 1919; Harris, 1979; Zhang et al., 2011). Over ongoing investigations are developing greater concordance among the past 165 years, more than 20 species from the overall data. The discovery of Eathiestrobus mackenziei in the through Lower Cretaceous deposits have been assigned to the Jurassic further narrows the discrepancy between the earliest oc- genus (Zhang et al., 2011). Whereas some ovuliferous scales of currence of crown group pinoid and nonpinoid conifers and thereby Schizolepis are narrowly attached in a lax strobilus, those of the reduces discordance between our understanding of conifer evolu- Pinaceae are broadly attached and form compact cones (Farjon, tion as provided by only paleontology on the one hand and system- 1990). All species of Schizolepis have ovuliferous scales that atic studies of only living species on the other. are deeply dissected into two, or less often, three lobes ( Zhang et al., 2011), while the ovuliferous scales of Pinaceae have an LITERATURE CITED entire margin. Some species of Schizolepis have a seed wing (e.g., Zhang et al., 2011) as do seeds of Pinaceae (Farjon, 1990), A RCHANGELSKY , S . , AND N. R. C UNEO. 1987 . Ferugliocladaceae, a new conifer but others do not (Harris, 1979). However, none are known to family from the Permian of . Review of Palaeobotany and have a membranous wing consisting of scale tissue, as do those Palynology 51 : 3 – 30 . of Pinaceae. A RRONDO , O. G. , AND B . P ETRIELLA . 1980 . Alicur á , nueva locali- Eathiestrobus fi rmly documents a Jurassic origin for dad plant í fera Li á sica, de la provincia de Neuqu é n, Argentina. Pinaceae. However, this earliest occurrence of the family Ameghiniana 17 : 200 – 215 . C LEMENT-WESTERHOF , J. A. , AND J. H. A. VAN KONIJNENBURG-VAN CITTERT . Pinaceae is still far later in geological history than one would 1991 . Hirmeriella muensteri: New data on the fertile organs leading expect for the fi rst occurrence of the sister group to all other to a revised concept of the Cheirolepidiaceae. Review of Palaeobotany living conifers (Fig. 21). The age of Eathiestrobus is contempo- and Palynology 68 : 147 – 179 . raneous with the earliest record for an anatomically preserved D ELEVORYAS , T . , AND R. C. H OPE . 1973 . Fertile coniferophyte remains seed cone of Cupressaceae (i.e., Hughmillerites juddii ; Roth well from the Late Triassic Deep River Basin, North Carolina. American et al., 2011 ), but both are more recent than the fi rst widely ac- Journal of Botany 60 : 810 – 818 . cepted fossil evidence for the families Cupressaceae (i.e., Aus- D ELEVORYAS , T ., AND R. C. HOPE . 1975 . Voltzia andrewsii, n. sp., an trohamia minuta Escapa, Cuneo et Axsmith; Escapa et al., Upper Triassic seed cone from North Carolina, U.S.A. Review of 2008; Fig. 21), Araucariaceae (i.e., Araucarites phillipsii Car- Palaeobotany and Palynology 20 : 67 – 95 . ruthers; Arrondo and Petriella, 1980), and Taxaceae (i.e., Pa- D ELEVORYAS , T . , AND R. C. HOPE . 1987 . Further observations on the Late Triassic conifers Compsostrobus neotericus and Voltzia andrewsii. laeotaxus rediviva Nathorst, 1908 ; Fig. 21 ). Review of Palaeobotany and Palynology 51 : 59 – 64 . Even older is the fi rst widely recognized occurrence of Podo- E SCAPA , I. R. 2009 . La tafofl ora de la formaci ó n Ca ñ ad ó n Asfalto, carpaceae (i.e., Rissikia media Townrow, 1967 ) in the Triassic Jurá sico Medio Superior de Chubut. Taxonomí a, bioestratigrafí a of Antarctica ( Fig. 21 ). While the minimum clade age for Podo- y paleofi togeograf í a. Ph.D. dissertation, Universidad Nacional del carpaceae cannot be independently verifi ed from that occur- Comahue, Bariloche, Argentina. rence because the fossil specimens upon which R. media is E SCAPA , I . , R . CÚ NEO , AND B . A XSMITH . 2008 . A new genus of the based ( Townrow, 1967 ) have been lost, the earliest fossil occur- Cupressaceae (sensu lato ) from the Jurassic of Patagonia: Implications rence of nonpinoid conifers is clearly considerably older (Fig. for conifer megasporangiate cone homologies. Review of Palaeobotany 21; Taylor et al., 2009) than that of Pinaceae (i.e., Eathiestro- and Palynology 151 : 110 – 122 . bus E SCAPA , I. H. , G . W . R OTHWELL , R. A. STOCKEY , AND N. R. CÚ NEO . 2012 . ; Fig. 21 ). Since the oldest representatives of sister groups Seed cone anatomy of Cheirolepidiaceae (Coniferales): Reinter- are expected to be of equivalent geological antiquity, paleonto- preting Pararaucaria patagonica Wieland. American Journal of logical evidence remains markedly discordant with the hypoth- Botany . esis that Pinaceae forms the sister group to all other living F ARJON , A. 1984 . Pines: Drawings and descriptions of the genus Pinus . conifers (e.g., Quinn et al., 2002 ; Rai et al., 2008 ). Koninklijke Brill NV, Leiden, Netherlands. On the other hand, E. mackenziei is younger than the voltzialean F ARJON , A. 1990 . 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