Taxodiaceous pollen cones from the Upper ... - Science Direct

Review of Palaeobotany and Palynology, 70 (1991): 67-76 Elsevier Science Publishers B.V., Amsterdam

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Taxodiaceous pollen cones from the Upper Cretaceous (Horseshoe Canyon Formation) of Drumheller, Alberta, Canada Rudolph

Serbet" and Ruth A. Stockey b

aDepartment of Botany, Ohio University, Athens, OH 45701, U.S.A. bDepartment of Botany, UniversiO, of Alberta, Edmonton, Alta. T6G 2E9. Canada (Received February 1, 1990; revised and accepted December 15, 1990)

ABSTRACT Serbet, R. and Stockey, R.A., 1991. Taxodiaceous pollen cones from the Upper Cretaceous (Horseshoe Canyon Formation) of Drumheller, Alberta, Canada. Rev. Palaeobot. Palynol., 70: 67-76. One hundred permineralized cones, 1.0-1.2 mm x 1.5-2.0 mm, some attached to branching systems, have been examined from the Upper Cretaceous ironstones in the Horseshoe Canyon Formation near Drumheller, Alberta. Cones are borne laterally and terminally on specialized shoots. Microsporophylls are helically arranged on the cone axis with one large resin canal and two pollen sacs per microsporophyll. Pollen is 12-16 ~tm in diameter with one exit papilla that forms a low protuberance on the grain. External surfaces of grains are scabrate with numerous orbicules and macrogranules while the nexine is laminated. Arrangement of cones on branches is similar to those of Taxodium whereas the number of pollen sacs per microsporophyll is similar to Sequoia and Sequoiadendron. Pollen morphology is similar to Metasequoia and Taxodium, while ultrastructurally it most closely resembles that of Metasequoia. This combination of morphological features is unlike that found in any living taxodiaceous genus. These remains are therefore described as Drumhellerakurmanniae gen. et sp. nov. This study reveals the importance of whole plant reconstructions in the recognition of other fossil Taxodiaceae due to the scarcity of distinctive morphological characters in isolated organs. Furthermore, the large number of fossil plant specimens associated with these taxodiaceous remains in the Horseshoe Canyon Formation show enormous potential for reconstructions of several types of seed plants.

Introduction W h i l e the U p p e r C r e t a c e o u s H o r s e s h o e C a n y o n F o r m a t i o n has been intensively studied for its f a u n a l c o m p o s i t i o n (Russell, 1989), floral studies have o n l y recently begun. T h e p r e s e r v a t i o n o f p l a n t m a t e r i a l as c o m p r e s s i o n s a n d calcified a n d silicified p e r m i n e r a l i z a t i o n s offers a u n i q u e o p p o r tunity to s t u d y these o r g a n i s m s as p a r t s o f whole p l a n t s for which e x t e r n a l m o r p h o l o g y a n d internal a n a t o m y are k n o w n . By far, the t a x o d i a c e o u s r e m a i n s are the m o s t c o m m o n a m o n g the p l a n t s preserved in these s w a m p y , w e t l a n d h a b i t a t s (Russell, 1989). T h e fossil r e c o r d o f the T a x o d i a c e a e , a l t h o u g h extensive, is difficult to i n t e r p r e t since i s o l a t e d o r g a n s are usually k n o w n in only one p r e s e r v a t i o n 0034-6667/91/$03.50

m o d e . T h e fossil pollen c o n e - b e a r i n g b r a n c h e s studied here p o i n t o u t the small n u m b e r o f taxon o m i c a l l y significant c h a r a c t e r s available in this family. T h e U p p e r C r e t a c e o u s a p p e a r s to have been an i m p o r t a n t p e r i o d o f time for t a x o d i a c e o u s evolution. The small n u m b e r o f distinct t a x a described to date, r a t h e r t h a n reflecting diversity, m o s t likely represents the lack o f d i a g n o s t i c m o r p h o l o g i c a l c h a r a c t e r s in this family a n d underscores the need for the study o f whole p l a n t s in u n d e r s t a n d i n g this diversity.

Materials and methods C o n e - b e a r i n g b r a n c h e s were studied f r o m two different lithologies, an o r a n g e to r e d - b r o w n d o -

© 1991 Elsevier Science Publishers B.V. All rights reserved

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lomitic/siliceous ironstone layer and a light grey sandstone layer from the Upper Cretaceous Horseshoe Canyon Formation, Alberta, Canada (Russell, 1983). Permineralized ironstone specimens occur at the Drumheller locality No.l, just north of the turn-off to Drumheller airport on Highway 9, universal transverse Mercator grid UN803052, and occur about half way between coal seams 7 and 8 (Gibson, 1977). Sandstone specimens occur in a coarse to fine-grained gray sandstone at the Horseshoe Canyon viewpoint locality, 15km southwest of Drumheller, universal transverse Mercator grid UM696977, and occur between coal seams No. 10 and 11 (Gibson, 1977). Associated with the pollen cones at these localities are several types of taxodiaceous ovulate cones, Taxodioxylon wood, stems with attached leaves of several morphological types, cupressaceous cones, twigs and leaves, Ginkgo leaves and seeds, Nilssonia leaves, Equisetum rhizomes and tubers, lycopod megaspores and cercidiphyllaceous fruits and leaves. Ironstone blocks were sectioned and prepared using the cellulose acetate peel technique (Joy et al., 1956). Peels were first demineralized in 15% nitric acid for 30 s to soften the peel and loosen the excess matrix (G.W. Rothwell, pers. commun., 1989), then in saturated oxalic acid for 30 s to remove iron oxides, in 15% sulfuric acid for 30 s to remove iron pigments and lastly in 50% hydrochloric acid for 30 s to remove the remaining dolomitic material. After the acid treatments, saturated sodium bicarbonate was used as a neutralizer and, finally, peels were rinsed in distilled water and allowed to air dry. Peels were cleared in xylene and mounted on microscope slides using Eukitt (O. Kindler, Germany) mounting medium. Peel sections used for scanning electron microscopy were treated in 50% hydrochloric acid for 5 s, rinsed with distilled water, air dried, mounted on stubs with double-sided tape and coated with 150A of Au using a Nanotek sputter coater. Specimens were examined on a Cambridge Stereoscan 250 at 20 kV. Pollen specimens for transmission electron microscopy were demineralized in concentrated hydrofluoric acid and washed with several changes of distilled water. The acetate matrix was then dissolved in several changes of acetone. Pollen

R. SERBET AND R.A STOCKEY

grains were fixed in 2% OsO 4 in 0.05 M sodium cacodylate buffer, pH 7.0 for 2 h, washed in distilled water, dehydrated with acetone and embedded in Spurr's (1969) resin. Sections were cut with a diamond knife, collected on Formvar-coated grids and stained according to Daddow (1983) with uranyl acetate and lead citrate (Venable and Coggleshall, 1965). Sections were examined with a Philips EM 410 at 80 kV. Results

Systematic description Order: CON1FERALES Family: TAXODIACEAE Genus: Drumhellera Serbet et Stockey gen. nov.

Species: D. kurmanniae Serbet et Stockey sp. nov. Diagnosis: Branching systems_at least 20 cm long with helically arranged pollen cones attached in axils of needle-like leaves. Cone-bearing axes 1.52.0 mm in diameter; pith with thick-walled parenchyma. Twelve to 13 scalariform to reticulate protoxylem strands. Secondary xylem, 8-10 cells thick with uniseriate circular-bordered pits and helical thickenings. Secondary phloem of banded sieve cells, parenchyma and fibers. Two-zoned cortex, resin canals in outer cortex. Cone axes with imbricate, helically arranged, scale leaves grading to ensheathing leaves with one vascular strand, one central resin canal and abaxial hypoderrnis. Microsporophylls helical, with inflated apex, heeled abaxially with one central resin canal, two to three (usually 2) pollen sacs. Cells of pollen sac wall radially elongated, thick-walled. Pollen non-saccate, 12-161xm in equatorial diameter (av. 14~m), with slightly protruding distal leptoma, circular to elliptical aperture, scabrate sexine, multi-lamellate nexine; germinal zone covering 1/2 to 1/3 of grain. Sexine macrogranular with Ubisch bodies. HoloO,pe: University of Alberta Paleobotanical Collection (UAPC-ALTA) specimen No. P9017 G,H Paratypes: P9030 F, P9092 G

TAXODIACEOUS POLLEN CONES FROM UPPER CRETACEOUS OF DRUMHELLER

Locality: 2 km north of Drumheller on Highway 9, just below Drumheller airport U.T.M. Grid Ref. UN 803052. Stratigraphic position: Horseshoe Canyon Formation, between coal seams 7 and 8. Age: Upper Cretaceous (Maastrichtian) Etymology: The species is named for Dr. Marie H. Kurmann, Royal Botanical Gardens, Kew who has done the most complete review of taxodiaceous pollen.

Description Branching systems up to 20 cm in length have been found bearing pollen cones in a helical arrangement. The most extensive permineralized specimen (Plate I, 1, 2, 4) shows nine attached cones. Cones are attached in the axils of needlelike leaves (Plate I, 4). Cone bearing axes are small about 1.5-2.0 mm in diameter (Plate I, 3). These axes have a central pith composed of thick-walled parenchyma cells (Plate I, 5). The pith is surrounded by about 12-13 protoxylem strands, secondary xylem 8-10cells wide, composed of angular tracheids and narrow vascular rays, secondary phloem with a banded appearance of alternating sieve cells, parenchyma and fibers, and a broad two-zoned cortex (Plate I, 3, 5, 6). Larger twigs with the same anatomy are found in the same blocks. These twigs often show several growth increments (Plate II, 1). In silicified specimens, phloem and complete cortical tissues are often preserved (Plate II, 1). The outer cortex has cells with dark contents and a ring of resin canals (Plate II, 1). Protoxylem elements exhibit scalariform to reticulate secondary wall thickenings whereas secondary xylem tracheids show uniseriate circular-bordered pits and delicate helical thickenings (Plate II, 3). Cone axes bear a series of small, imbricate, helically arranged scale leaves (Plate I, 1-4, Plate II, 4). These leaves grade into more elongate ensheathing leaves that surround the cones (Plate I, 3; Plate II, 4, 7). Ensheathing leaves show a single vascular strand, one centrally located resin canal and an abaxial hypodermis (Plate II, 6, 7). This canal disappears in the most distal leaf sections (Plate II, 5).

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Microsporophylls are helically arranged on the cone axis (Plate III, 1). Each microsporophyll has one large centrally located resin canal (Plate III, 1, 2) an upturned distal tip and an inflated abaxial heel (Plate III, 2). There are two abaxial pollen sacs per microsporophyll (Plate II, 4; Plate III, 2). Pollen sac walls are composed of radially elongate rectangular cells with prominently thickened walls (Plate III, 3, 5). Several cones exhibit intact pollen sacs with numerous non-saccate pollen grains (Plate III, 4). Pollen is small, averaging 141am in equatorial diameter (range 12-16) (Table I, Plate III, 6). Grains are variable within individual pollen sacs and can have a slightly protruding distal leptoma (Plate IV, 3) to a more pronounced protruding distal leptoma (Plate III, 6, Plate IV, 2). Apertures vary from circular (Plate IV, 2) to slightly elliptical (Plate IV, 3). Remains of the tapetum are often present in pollen sacs (Plate IV, 1, 2). Grain ornamentation consists of scabrate sexine covered by solid macrogranules and hollow Ubisch bodies (Plate IV, 4, 5). The distal germinating end has less ornament than the proximal end, and is extensive, covering from 1/3 to 1/2 of the entire grain surface (Plate IV, 5). The nexine is laminated with a large number of lamellae (Plate IV, 5, 6).

Discussion Pollen cone attachment of the Drumheller cones is similar to that in several extant taxa of Taxodiaceae excluding Sequoia and Sequoiadendron (Table I). The helical arrangement of subtending leaves and microsporophylls is like that in most genera except Metasequoia which is decussate. The exception with respect to sporophyll arrangement is M. milleri from the Middle Eocene Princeton chert which is helical (Rothwell and Basinger, 1979). These authors, however, suggest a change of microsporophyll orientation during ontogeny in extant M. glyptostroboides. The number of pollen sacs per microsporophyll in Drumhellera is usually two. This number is similar to Sequoiadendron and Sequoia, but unlike the usual three in Metasequoia or the larger numbers (5-9) seen in Taxodium (Table I). The distal leptoma (exit papilla) in grains of Drumhellera is

70

R SERBETAND R.A. STOCKE¥

a low protuberance as in Taxodium and unlike the long and sometimes sharply bent papillae in some genera such as Sequoia and Sequoiadendron (Table I). The average equatorial diameter of Drumhellera pollen is much less than any living or fossil genus described (M.H. Kurmann, pers. commun. 1989). The range of diameter, however, is closest to that of Metasequoia glyptostroboides (Table I). The large area occupied by the distal

germinal zone is also similar to Metasequoia, as is the large number of nexine lamellae (M.H. Kurmann, pers. commun., 1989). Taking all of these comparative characters together it is apparent that Drumhellera shares characters with several extant and extinct taxa, but that these cone-bearing branches do not fit into any described taxon. Drumhellera cones show the closest similarities to Metasequoia and Taxodium. Other authors have

PLATEI Drumhellera kurmanniae gen. et sp. nov. 1. Longitudinal section of cone-bearing branch. P9017 H1 bot #2. x 10. 2. Longitudinal section of cone-bearing branch in fig.l at another level, P9017 H1 bot #78. x 10. 3. Transverse section of branch with attached pollen cone. P9017 G3 top a//7. x 21.5. 4. Longitudinal section of branch bearing pollen cone in axil of needle-like leaf (L). 9017 H1 bot ,#32. x 25. 5. Transverse section of small twig. P9017 G 3 top b #2. x 60. 6. Radial longitudinal section of small twig showing primary xylem (IX), secondary xylem (2X) and two-zoned cortex (C). P9017 HI bot # 46. x 150. PLATE I1

(see p. 72)

Drumhellera kurmanniae gen. et sp. nov. l. Transverse section of associated twig. P9030 F bot #0. x 130. 2. Radial longitudinal section of primary xylem. P9017 H 1 bot #42. x 550. 3. Radial longitudinal section of secondary xylem. P9017 Ha bot #42. x 550. 4. Longitudinal section of cone with subtending scale-leaves and ensheathing leaves. P9092G side #5. x 25. 5. Transverse section of ensheathing leaf distal tip. P9017 H 3 bot #5. x 190. 6. Transverse section of ensheathing leaf with adaxial vascular strand, central resin, canal and abaxial hypodermis. P9017 H 3 bot #5. x 75. 7. Oblique transverse section of pollen cone showing helically arranged ensheathing leaves. P9017 H3 bot #4, x 36. P = p i t h , R = resin canal, SC = scale leaf. PLATE III

(see p. 73)

Drumhellera kurmanniae gen. et sp. nov. 1, Tangential longitudinal section of pollen cone showing helically arranged microsporophylls indicated by resin canals. P9092 G side #11. x 70. 2, Longitudinal section of microsporophylls. Note attached pollen sacs at top. P9092 G side #7. x 70. 3. Pollen sac walls. P9017 H a bot #76. x 600. 4, Pollen grains in microsporangia. P9017 G 3 bot #0. x 350. 5, Wall thickenings in pollen sac walls. P9017 H a bot #69. x 600. 6, Pollen grains. P9017 G 3 bot #0. x 1140. PLATE IV

(see p. 74)

Drumhellera kurrnanniae gen. et sp. nov. pollen. 1. Pollen grains in tapetal tissue. Note nexine and sexine separation. P9017 G3 bot HI. x 1450. 2. Slightly protruding distal leptoma with circular aperture. P9017 G3 bot #1. x 5875. 3. Distal leptoma with elliptical aperture. P9017 G3 bot #1. x 5625. 4. Proximal surface with macrogranules and Ubisch bodies. P9017 G3 bot #1. x 4750. 5. Longitudinal section showing large distal germinal zone, laminated nexine and scabrate sexine on proximal surface. P9017 G3 bot #2. x 5415. 6. Laminated nexine and scabrate sexine near proximal end of grain. P9017 G3 bot #2. x 11,467.

~

i~ ~

~"

m~

r~

c~

r~

r~

b

pll

m~

TAXODIACEOUS POLLEN CONES FROM UPPER CRETACEOUS OF DRUMHELLER

PLATE

III

(for explanation see p. 70)

73

74 PLATE

R. SERBETAND R.A STOCKEY IV

(for explanation see p. 70)

TABLE ! Comparison of Drumhellera kurmanniae to pollen cones of other Taxodiaceae Taxon

Taxodium distichum T. mucronatum

Glyptostrobus pensilis

Sequoia sempervirens

Sequoiadendron giganteum

Metasequoia glyptostroboides

Metasequoia milleri

Metasequoia occidentalis

Parataxodium wigginsii

Drumhellera kurmanniae

Pollen cone Attachment

Terminally and laterally on specialized shoots

Terminally on unspecialized shoots








Arrangement of subtending scale-leaves

Helical

Helical

Helical

Helical

Decussate

Decussate

Decussate

Decussate

Helical

Arrangement of microsporophylls

Helical

Helical

Helical

Helical

Decussate

Helical

Decussate?

Number of pollen sacs per microsporopbyll

5-9

3-4

2-5 usually 3

2-5 usually 3

3

3

3

Pollen Exit papilla

Low protuberance

Short, bent sharply

Long, bent sharply

Very long, bent sharply

Moderate length, bent sharply

Moderate length, erect

Low protuberance

Mean equatorial diameter (~tm)

25.6

30.8

34.7

28.4

24.3

23

14

Range (pm)

22.9 27.9

25.4 31.8

30.5-40.6

25.4-30.5

17.2-26.5

19-27

12-16

Features

(Modified from Basinger, 1981, Arnold and Lowther, 1955, pollen data from M.H. Kurmann, 1989 and pers. commun., 1989)

Helical

76

noted similarities of fossil conifers to these two taxa. Arnold and Lowther (1955) described Parataxodium wigginsii from the Upper Cretaceous of Alaska. That conifer probably had pollen cones borne terminally and laterally on specialized branches (Table I). However, those cones were described from compressions only. The decussate to sub-opposite arrangement of those cones may be a difficult character to assess in compressions. The arrangement of microsporophylls and pollen are unknown for that taxon making comparison to Drumhellera difficult. The same can be said of the widespread Metasequoia occidentalis (Paleocene to Middle Miocene) which may represent several taxa that are as yet indistinguishable. The only other permineralized pollen cones described, Metasequoia milleri (Rothwell and Basinger, 1979), are more closely comparable to M. glyptostroboides. The lack of distinguishing characters between these taxa points toward a close relationship. Metasequoia milleri cones have one resin canal per microsporophyll like those in Drumhellera, however, this canal splits into three distal to the sporangia, a character not observed in Drumhellera. The regular condition of three pollen sacs per microsporophyll, thin-walled sporangial walls, and pollen with an erect protruding leptoma are further differences between M. milleri and the Drumheller cones. The similarity of several previously described Upper Cretaceous conifers to both extant Metasequoia and Taxodium, including Parataxodium (Arnold and Lowther, 19.55) and now Drumhellera, points toward a possible common ancestry for the two extant genera. The combination of characters observed in Drumhellera, however, points toward the necessity of knowing these conifers as whole plants due to the lack of recognizable taxonomically useful characters in isolated organs.

Acknowledgements We thank George Braybrook, University of Alberta, Edmonton and Michael W. Folsom, Univer-

R. SERBETAND R.A. STOCKEY

sity of New Mexico, Albuquerque, for their assistance with scanning and transmission electron microscopy respectively. Thanks especially to Marie H. Kurmann, Royal Botanical Gardens, Kew for data on extant taxodiaceous pollen, Dr. Dennis R. Braman, Tyrrell Museum of Palaeontology for help with stratigraphy and Dr. Gar. W. Rothwell, Ohio University for photographic assistance. This study was supported in part by Natural Sciences and Engineering Research Council of Canada (NSERC) grant A6908 to R.A. Stockey and the Department of Botany, University of Alberta.

References Arnold, C.A. and Lowther, J.S., 1955. A new Cretaceous conifer from northern Alaska. Am. J. Bot., 42: 522-528. Basinger, J.F., 1981. The vegetative body of Metasequoia milleri from the Middle Eocene of southern British Columbia. Can. J. Bot., 59: 2379-2410. Daddow, L.Y.M., 1983. A double lead stain method for enhancing contrast of ultrathin sections in electron microscopy: a modified multiple staining technique. J. Microsc., 129: 147-153. Gibson, D.W., 1977. Upper Cretaceous and Tertiary coalbearing strata in the Drumheller-Ardley region, Red Deer River valley, Alberta. Geol. Surv. Can. Pap., 76-35: 1-41. Joy, K.W., Willis, A.J. and Lacey, W.S., 1956. A rapid cellulose peel technique in paleobotany. Ann. Bot. (London) NS., 20: 635-637. Kurmann, M.H., 1989. Pollen morphology and ultrastructure in conifers. Am. J. Bot. (Supplement), 76: 220-221. Rothwell, G.W. and Basinger, J.F., 1979. Metasequoia milleri n. sp., anatomically preserved pollen cones from the Middle Eocene (Allenby Formation) of British Columbia. Can. J. Bot., 57: 958-970. Russell, D.A.,1989. An Odyssey in Time; The Dinosaurs of North America. National Museum of Natural Sciences, Canada, Univ. Toronto Press, 240 pp. Russell, L.S., 1983. Evidence for an unconformity at the Scollard-Battle contact, Upper Cretaceous strata, Alberta. Can. J. Earth Sci., 20:1219 123l. Spurr, A.R., 1969, A low-viscosity epoxy resin embedding medium for electron microscopy. J. Ultrastruct. Res., 26: 31-43. Venable, J.H. and Coggleshall, R., 1965. A simplified lead citrate stain for use in electron microscopy. J. Cell Biol., 25: 407.