- Email: [email protected]
Squamastrobus gen. N., A fertile podocarp from the early cretaceous of Patagonia, Argentina
Review of Palaeobotany and Palynology, 59 (1989): 109 126
109
Elsevier Science Publishers B.V., Amsterdam - - Printed in The Netherlands
SQUAMASTROBUS GEN. N., A FERTILE PODOCARP FROM THE EARLY CRETACEOUS OF PATAGONIA, ARGENTINA SERGIO ARCHANGELSKY and GEORGINA DEL FUEYO DivisiOn Paleobotdnica, Museo Argentino de Ciencias Naturales "B. Rivadavia", Av. Angel Gallardo 470, Buenos Aires 1405 (Argentina) CONICET (Received April 20, 1988; revised and accepted October 3, 1988)
Abstract Archangelsky, S. and del Fueyo, G., 1989. Squamastrobus gen. n., a fertile podocarp from the early Cretaceous of Patagonia, Argentina. Rev. Palaeobot. Palynol., 59: 109-126.
Squamastrobus tigrensis nov. gen. et sp. has been found in early Cretaceous strata (Baquer5 Formation), Santa Cruz Province, Argentina. It is based on branches with squamiform leaves, laterally attached pollen cones and terminally disposed seed cones. The cuticle of leaves and female bract-scale complexes was studied in their general structure and ultrastructure. The pollen cones contain bisaccate pollen grains that are similar both structurally and ultrastructurally with extant and fossil members of the Podocarpaceae. The seed cones are compact structures resembling some taxa found in Mesozoic Gondwana strata. Comparisons made with living and extinct members of the Podocarpaceae suggest some phylogenetic links between Mesozoic cone-bearing forms with the extant genera Microcachrys and Pherosphaera. Finally, some considerations on the origin of Mesozoic podocarps are also included in regard to recently discovered Permian conifers from Gondwana.
Introduction The family Podocarpaceae is widely distributed in Cretaceous strata of Patagonia where pollen assemblages are dominated by conifers, mainly Cheirolepidiaceae; pollen with two and three sacci are also common. Megafossil remains assignable to conifers are abundant, usually as sterile twigs belonging to several genera, some with affinities with the Podocarpaceae. Florin (1940) suggested that most Mesozoic Elatocladus impressions from the Southern Hemisphere probably belong to this family. When these leaves are found with a cuticle their assignment to the podocarps is more certain, and separate genera have been established on this ground (as Coronelia Florin, op. cit.). Yet it is only with fertile specimens, especially with the pollen cones, 0034-6667/89/$03.50
that a more natural relationship can be established at a family level. The few seed structures that have been described from southern lands (Rissikia, Mataia, Trisacocladus etc.) partly differ from living genera in their cone-like habit. These Mesozoic taxa suggest that during the Cretaceous several lineages were developing. Among the coniferous twigs known in early Cretaceous strata of Patagonia, those bearing scale-like leaves assigned to the genus Brachyphyllum are the most abundant. In this paper we describe fertile pollen and seed structures organically attached to twigs that have been referred to Brachyphyllum tigrense (Traverso, 1966; Archangelsky and del Fueyo, 1987). So far, podocarp remains described with fertile structures from these strata have leaves that resemble living members in their morphology
~'} 1989 Elsevier Science Publishers B.V.
110
and anatomy. Three genera were referred to the Podocarpaceae: Trisacocladus, with pollen cones having pollen with three air bladders (Trisaccites type) and seed cones with a thick central axis bearing orthotropous seed-scale complexes, Apterocladus, with pollen cones having grains with three rudimentary sacci (CaUialasporites type) and sterile twigs named Podocarpus dubius (Archangelsky, 1966). Squamastrobus is the new genus proposed to combine vegetative remains of Brachyphyllum tigrense Traverso with pollen and seed structures in organic connection. The pollen has two sacci and is similar in morphology, structure and ultrastructure with extant members of the group; the leaves and their cuticle can also be compared with some taxa presently known in the Southern Hemisphere (though not in Patagonia); finally, the seed cones, although partly known in their organization, differ from other fossil or extant taxa. The exceptional preservation of the mummified remains allowed their study with both scanning and transmission electron microscopy. Materials and m e t h o d s The specimens were recovered from the Baquer6 Formation, dated as latest Barremian to early Aptian (Archangelsky et al., 1984). They were fbund in 1985 at the Bajo Tigre locality in Santa Cruz province during a combined CONICET-NSF expedition. The precise location of the bed is shown in map 2, fossiliferous site 7 (Archangelsky, 1967). The
abundant mummified 1 material includes twigs, pollen and seed cones. The leaf cuticle was easily removed from the matrix and treated twice with 40% nitric acid followed by 5% ammonium hydroxide and then washed in distilled water. To remove some residue, ultrasound was used for 10 seconds. For optical observation cuticles were mounted in glycerine jelly. For SEM observation the cuticles of leaves, their sections and pollen sacs were suspended in 1:1 water-alcohol and dropped on a double face scotch tape adhered to a stub, and after drying it was coated with goldpalladium. For TEM observation, leaf fragments, pollen sacs and seed cone bracts were stained with 1% OsO4 for 2 hours at room temperature, washed for 30 minutes in distilled water and dehydrated in an ascendent alcohol series [25%, 50%, 70%, 95% and 100% (15' each and twice with 100°/0)], followed by acetone 100% (twice, 15' each). The material was then infiltrated using a rotator with the following mixtures: acetone 3/Spurt 1, 6 hours, acetone 1/Spurr 1, 6 hours and 2 changes with Spurr, each for 6 and 16 hours. Then the fragments were included in moulds and dried in vacuum at 70°C for 48 hours. Ultrathin sections (ab. 800 A thick) were made with a diamond knife using a SORVAL manual ultramicrotome. The 1The term mummification used here refers to fossils with tissues t h a t are preserved in a way t h a t their s t r u c t u r e and u l t r a s t r u c t u r e reflect exactly living a n a l o g u e s (leaf cuticles, pollen). Comparative studies of their most minute s t r u c t u r e s are possible because diagenetic processes during fossilization did not affect them.
PLATEI 1 8.
1. 2. 3. 4,
5. 6,
7. 8.
Squamastrobus tigrensis
gen. n. Vegetative part. B r a n c h e s of first (arrow), second and third orders. BA PB 11312. Ultimate and p e n u l t i m a t e order branching. BA Pb 11325. External view of a leaf showing slightly s u n k e n stomata, smooth periclinal wall; anticlinal flanges are also evident. SEM x 400. External view of distal part of a leaf showing papillae. SEM x 400. Section of abaxial cuticle of leaf. A thick externally smooth periclinal wall and anticlinal flanges are seen; a stoma (arrow) with s u p r a s t o m a t i c chamber (U-shaped) and a partly cutinised hypodermis are also shown. SEM x 500. A detail showing cutinised periclinal wall, anticlinal flanges and hypodermis. SEM x 1000. Section of abaxial cuticle showing periclinal wall, anticlinal flanges and a stoma (arrow). x 400. Section of a b a s a l m o s t part of leaf showing extra-cutinised component (arrow). x 400.
111
PLATE I
112
sections were then mounted in single hole grids coated with F o r m v a r and stained with KMnO4 (5-10') and Uranil acetate (30"). A Leitz Dialux microscope was used for light microscopy; photomicrographs were t aken with a Canon FN camera using Kodak Panatomic film. A Jeol JSM-35CF microscope was used for SEM observations while a Jeol J E M 100C of the CEVAN-CONICET Institute was used for TEM. All the specimens are lodged in the Paleobotanical Collection of the Buenos Aires N at ur a l History Museum (BA PB for megafossils and BA PB Pm for slides).
Description The specimen BA PB 11312 (Plate I, 1) has up to four orders of branches. Branches are radially and irregularly inserted. The main branch is 2 cm wide; second order branches are 0.5 cm wide, with penultimate branches up to 2.5 mm wide and the last order branches are short and I mm wide. The widest main branch is 2.8 cm and it was found in the specimen BA PB 11313. Second order branches vary from 4 6 mm in width. Third order branches (Plate I, 2) are the commonest varying from 1.5 to 2.5 mm in width, the longest seen attaining 5.4 cm (BA PB 11321). Ultimate branches are up to 1.6 cm long and 0.5-1 mm wide (BA PB 11325, Plate I, 2). Leaves are scale-like, ovate, adpressed, with entire margins, helically disposed with a 3/8 phyllotaxis. The largest (found in second to fourth order branches) are 3.8 mm long x 1.7 mm wide; they have a rostrate apex and an oval leaf base, 2.7 mm long x 1.5 mm
wide. Width ratio of leaves 1:1.2-2.4. Smaller leaves have an obtuse apex. In first order branches (BA PB 11312, Plate I, 1) leaves are up to 5.5 mm long (with adaxial cuticle 3.8 mm long) and in second order branches they are 3.8 mm long (with a 2 mm long adaxial cuticle); in third order branches, leaves 3.3 mm long have a 1.2 mm long adaxial cuticle. (A detailed description and illustration of different leaf types can be seen in Traverso, 1966). Both cuticles are smooth externally, but contours of epidermal cells (the interception of anticlinal flanges with external periclinal wall), especially those between stomatal rows can be seen (Plate I, 3). Towards the apex of leaves external round papillae are present on abaxial cuticle (Plate I, 4); it shows epidermal cells with smooth periclinal walls in internal view (Plate I, 5); the cuticle is 5 pm(10.4 pm)118.2 ~m thick (20 measurements) (Plate I, 6). Anticlinal flanges are continuous, not interrupted by pits and smooth from base to top where they expand laterally (Plate I, 6, 7); they are 7.8(15.6)46.8 ~m wide (17 measurements) and 7.8(10.4)13 ~m high (26 measurements). Remnants of cutinised hypodermal cells are seen (Plate I, 5, 6). Leaf bases develop extra cutin t hat has no definite structure, organization or thickness (Plate I, 8). It may have functioned as a protective layer in the abcission area or as an agent for water retention. The leaf margins have a discontinuous serrulate wing that lacks in basal portions. In the distal half of the leaf, the serrate wing is 1Figures in b r a c k e t s a r e t h e m e a n v a l u e s of all m e a s u r e ments.
P L A T E II 9 14. 9. 10. 11. 1 2 13. 14.
Squamastrobus tigrensis gen. n. V e g e t a t i v e part. A b a x i a l leaf c u t i c l e s h o w i n g i r r e g u l a r s t o m a t a l files BA Pb P m 1. x 100. L e a f m a r g i n s h o w i n g s e r r u l a t e edge. B A Pb P m 1. x 400. A b a x i a l l e a f c u t i c l e s h o w i n g s h a p e of cells in a n d b e t w e e n s t o m a t a l rows. R e m n a n t s of h y p o d e r m a l cells a r e also s e e n (arrows). BA Pb P m 2. x 400. T w o focci of a s t o m a s h o w i n g g u a r d cells (fig.12) a n d a p r o x i m a l s e c t o r of s u b s i d i a r y cells w i t h s t r i a t i o n s (fig.13). BA Pb P m 2. x 1000. I n t e r n a l view of two s t o m a t a s h o w i n g F l o r i n rings, a cycle of s u b s i d i a r y cells a n d a n t i c l i n a l flanges. C u t i n i s e d h y p o d e r m i s cells a r e s e e n at t h e left b o t t o m corner. S E M x 400.
:>
114 up to 43.3 pm wide and has p e r p e n d i c u l a r to oblique cells of r o u n d e d to a c u t e c o n t o u r (Plate II, 10). On b o t h cuticles epidermal cells h a v e different shapes in r e g a r d to t h e i r disposition b e t w e e n s t o m a t a l rows or not. In s t o m a t a l rows t h e y are mostly i s o d i a m e t r i c while bet w e e n s t o m a t a l rows t h e y are from subisodiametric to r e c t a n g u l a r e l o n g a t e (Plate II, 11). In the adaxial cuticle, in s t o m a t a l rows, t h e y are 2 6 p m l o n g x 2 3 . 4 pm wide, with an a r e a of 608.4~m2; b e t w e e n s t o m a t a l rows, 4 5 . 8 p m long x 18.2 ~m wide, with an a r e a 851.7 ~m 2. In the abaxial cuticle, cells in a row b e t w e e n s t o m a t a are 28.6 pm with an a r e a 817.9 pm 2 and b e t w e e n s t o m a t a l rows, 49.4 ~m long x 15.6 pm wide, with an a r e a 770.6 pm 2 (total measurements, 920). Leaves are a m p h i s t o m a t i c with m o n o c y c l i c s t o m a t a (rarely imperfectly dicyclic). F o u r to five subsidiary cells are radially, sometimes elliptically placed; t h e y are p o l y g o n a l and i s o d i a m e t r i c or oblong with r o u n d e d sides. S u b s i d i a r y cells of n e i g h b o u r i n g s t o m a t a are often in contact. S t o m a t a are c o m m o n l y placed in rows and h a v e oblique o r i e n t a t i o n ; l o n g i t u d i n a l and t r a n s v e r s e s t o m a t a l orientation are also seen. S t o m a t a l rows s e p a r a t e d by 2 6 rows of epidermal r e c t a n g u l a r to e l o n g a t e cells (Plate II, 9). S t o m a t a l index is 95 per sq. mm. T h e F l o r i n ring is up to 5.4 ~m thick, elliptical, slightly sunken, c o n t i n u o u s and with gently sloping sides. L e n g t h - b r e a d t h ratio: 21/34. T h e s t o m a t a l a p p a r a t u s is r o u n d e d to elliptical ( e l o n g a t i o n i n d i s t i n c t l y oriented, P l a t e I, 3). Anticlinal flanges s e p a r a t i n g c o m m o n epidermal and subsidiary cells are of the same size or smaller t h a n flanges b e t w e e n n o r m a l epider-
mal cells; a n t i c l i n a l flanges s e p a r a t i n g subsidiary from g u a r d cells are m u c h smaller. Subsidiary cells are slightly smaller t h a n neighb o u r i n g epidermal cells (Plate II, 11, 14). The i n n e r surface of periclinal wall of subsidiary cells with fine s t r i a t i o n s r a d i a l l y or parallel o r i e n t e d to s t o m a t a l m o u t h (Plate II, 13). Width of s t o m a t a l c h a m b e r 20.6(31)44.2 ~m; length, 30.9(40.6)52 ~m. S u p r a s t o m a t a l chamber U to V shaped in section with widening m o u t h t o w a r d s the surface (Plate I, 5, 7). G u a r d cells slightly cutinised, with l a t e r a l l y a r c h e d o u t e r and i n n e r sides, t h i n n i n g t o w a r d s poles w h e r e t h e y meet and slightly p r o t r u d e (Plate II, 12, 14). G u a r d cells 4.2(8.2)10.3 ~m wide. The s t r u c t u r e of the cuticle a r o u n d a stoma as seen with T E M shows the F l o r i n ring, cutinised a n t i c l i n a l flanges and r e m n a n t s of cutin on g u a r d cells (Plate III, 15). The u l t r a s t r u c t u r e of the e x t e r n a l periclinal wall shows r e m n a n t s of e p i c u t i c u l a r wax (Plate III, 18). T h e cuticle is layered. T h e e x t e r n a l l a y e r is lamellated, the most c o m p a c t lamellae are 50/~ t h i c k (Plate III, 19); i n t e r n a l l y , lamellae become more s e p a r a t e d (up to 200 A, P l a t e III, 18) and an i n t e r f a c e to the solid, t h i c k c o m p o n e n t of the cuticle is seen (Plate III, 17). The i n n e r m o s t g r a n u l a r to spongy layer, is approxim a t e l y 0.6 ~m t h i c k (Plate III, 16). The pollen cones are a t t a c h e d l a t e r a l l y to third o r d e r twigs (BA PB 11311, P l a t e IV, 20); t h e y are elongated, cylindrical, t h i n n i n g towards base and apex, 12(14.3)18 mm long x 1.2(2.4)3.5 mm wide (Plate IV, 21). Central axis 0 . 2 - 0 . 4 m m wide, with n o r m a l l y att a c h e d and s h o r t l y p e d u n c u l a t e microsporophylls, helically disposed, distally e x p a n d e d
PLATE Ill 15 19. Squamastrobus tigrensis gen. n. Leaf cuticle ultrastructure (TEM). 15. Section through a stoma showing Florin ring (arrow), mouth, remnants of guard cells (G) and anticlinal flanges of subsidiary cells (S). x 2000. 16. Detail of inner zone of periclinal wall cuticle showing a granular (degraded?) structure, x 50,000. 17. Detail of outer zone of periclinal wall cuticle showing external laminated components with an interface to a solid structure (bottom). x 50,000. 18. Detail of external lamination of the cuticle and remnants of epicuticular wax(?) (arrow). x 50,000. 19. Detail of lamination (arrow) in the outer part of periclinal wall at the stomatal mouth region, x 80,000.
.-]
y~
21
2
116 and s t r o n g l y curved, up to 90 ° , o v e r l a p p i n g a d j a c e n t s p o r o p h y l l s (Plate IV, 21). Two(?)subspherical pollen sacs (slightly e l o n g a t e d due to compression), 0.4(0.7)1 mm in d i a m e t e r (Plate IV, 25), h a v e a light yellow colour, c o n t r a s t i n g with the s u r r o u n d i n g d a r k e r tissue (Plate IV, 21). Obliquely o r i e n t e d scales are placed in a close spiral at the cone base. P o l l e n sacs are easily detached; t h e y are composed of a compact mass of pollen g r a i n s with a m e m b r a n e cover. The e x t e r n a l g r a n u l o s e wall Of pollen sacs has no visible cellular s t r u c t u r e , but a b u n d a n t bodies of different sizes and shapes a d h e r e with no p a r t i c u l a r o r i e n t a t i o n (Plate IV, 26). Pollen g r a i n s are bisaccate, of the Podocarpidites type (Plate IV, 22-24), with s t r o n g l y r u g u l a t e body in its p r o x i m a l side; sacci p e n d a n t (Plate IV, 24, 26), often folded, with u s u a l l y i s o d i a m e t r i c i r r e g u l a r endoreticulation, 2 4 pm wide (Plate IV, 22, 23). Exine 2 pm thick; on the distal side of the body an i r r e g u l a r l e p t o m a is seen (Plate IV, 22). M e a s u r e m e n t s (in 20 grains) give a t o t a l l e n g t h of 38(52.5)55 pm, t o t a l w i d t h of 23(31)38 pro, a body l e n g t h of 28(34)39 ~m, a body h e i g h t of 12(21.6)33 ~m, a s a c c u s l e n g t h of 15(21.6)25 ~m, a sac h e i g h t of 14(20.6)28 I~m and a d i s t a n c e b e t w e e n sac bases of 3(6.1)13 pro. In section, the pollen sac shows c o m p a c t l y disposed and s t r o n g l y folded g r a i n s (Plate IV, 26-28). The s p o r o d e r m consists of two d i s t i n c t layers, an inner, c o n t i n u o u s nexine and an outer, more
electron-dense sexine. The nexine is homogeneous and lamellated, with slightly w a v y o u t l i n e in section view (Plate IV, 29). Sections in proximal p a r t s of the c o r p u s show an e x t e r n a l l a y e r (sexine) composed of s p o r o p o l l e n i n rods t h a t e x t e r n a l l y fuse to form a c o n t i n u o u s n o n pitted, s t r o n g l y s i n u o u s t e c t u m (that corresponds to the r u g u l a t e s c u l p t u r e in surface view). The rods are l o n g e r n e a r the proximal pole area, b e c o m i n g s h o r t e r t o w a r d s the apert u r a l a r e a and the base of the sacci (Plate IV, 27, 29). B e n e a t h this e x t e r n a l layer, the alveolar sexine shows in section large spaces and i r r e g u l a r r o u n d e d s p o r o p o l l e n i n u n i t s (Plate IV, 29, 30, 31) t h a t are s i t u a t e d directly on the nexine and seem to i n t e r d i g i t a t e with it (Plate IV, 30). The i n n e r p a r t of the sexine is s t r o n g l y r e d u c e d t o w a r d s the a p e r t u r a l a r e a a n d the sacci. S p o r o d e r m sections t h r o u g h the sacci show a s m o o t h c o n t i n u o u s o u t e r c o v e r t h a t is an e x t e n s i o n of the w a v y t e c t u m of the corpus. Loose s p o r o p o l l e n i n units are present b e n e a t h the o u t e r l a y e r as i n t e r n a l rod-like extensions (endomuri) t h a t i r r e g u l a r l y a n a s t o m o s e in the p e r i p h e r a l a r e a of the sacci to form an imperfect reticulum. A l t h o u g h the pollen is still f o u n d as a c o m p a c t mass inside the sacs, individual grains are usually separated (Plate IV, 28). The clear differentiation of the sporoderm layers suggests t h a t the pollen was almost mature. This is also supported by the r e c o v e r y of isolated grains from the sacs t h a t have
PLATE IV 20-31. 20. 21. 22 23. 24. 25. 26. 27 28. 29. 30. 31.
Squamastrobus tigrensis gen. n. Pollen cone. Pollen cone in organic connection to a leafy branch. Holotype, BA PB 11311. x 2. A detail of the same showing central axis and pollen sacs. x 8. Two focci of an isolated grain from a pollen sac of the holotype, x 850. Another grain in equatorial view, isolated from the holotype, x 850. A view of a pollen sac. SEM x 90. Bisaccate grains adhering to the inner surface of the sac membrane. SEM x 400. Sections through grains from a pollen sac. The sinuous tectum of the corpus (C), sacci (S) and leptoma (L) are seen. TEM x 2000. A detail of the leptoma area showing the thin exine, rod like components leaving large spaces and a sinuous tectum (arrow). TEM x 6000. A detail of the edge of the leptoma showing the nexine (partly lamellated) and sexine globular components (arrow). TEM × 40,000. Section through the corpus on proximal side of grain showing the foot layer with granulose to globose components, a columella (arrow) and wavy tectum. TEM x 40,000.
-3
"--1
118
attained their mature size and shape (Plate IV, 22, 24) suggesting that they fossilized at a time when their content was ready for dispersal. Seed cones are terminal and attached to third order branches (Plate V, 32, 37, BA PB 11340, 11332). They are elongated, cylindrical with a thinned base and an obtuse apex, 1.5(2.8)5.5 cm long x 0.7(1.2)1.3 cm wide. Central axis l m m wide (BA PB 11372), bearing compactly and normally attached bract-scale complexes that are helically disposed. Bracts with a wide base, separated, with slightly deflexed and acuminate apex (Plate V, 38, 39), rhomboidal in cross section with expanded lateral angles (Plate V, 33-36). Each bract bears a single elongated body that is situated near the cone axis (Plate V, 38, 39). Eventually, these bodies (ovuliferous scales ?) are connected (or partially fused) to the bracts as suggested by their disposition (Plate V, 39, arrow). Bracts distally cutinised bearing stomata on the abaxial side, forming short illdefined rows and oriented mostly obliquely (Plate VI, 45, 46). There are about 20 stomata per sq. mm. Epidermal cells on stomatal cuticle 34 x 21 ~m wide, isodiametric or slightly elongated. Margins serrulate (Plate VI, 40) with distally placed papillae (Plate VI, 43). Hypodermis cutinised. The bract cuticle becomes thinner towards the cone axis where it has no stomata, papillae or cutinised hypodermis and the cells are more elongated, up to 591~m long x 12 gm wide. Cell contours disappear at the most basal part where the cuticle is granulose. Several types of pollen grains adhere to this cuticle (Classopollis, Cyclusphaera, Podocarpidites, among others) (Plate VI, 44). Stomata similar to those found in vegetative leaves, i.e. monocyclic, with 4 5 radially placed polygonal to isodiametric subsidiary cells, sometimes in contact. A transfer of a cone (Plate V, 34) shows bracts with a rhomboidal section, one with a small salient cutinised pyramid-like structure (Plate V, 35, 36, arrows) and a similar cuticle to the outer bract membrane, i.e. thick, with stomata and serrulate margins. However it differs in the lack of papillae, epidermal cells t h a t tend to be all
isodiametric, and a higher stomatal index (48 against 20 per sqmm); stomata are usually transversely oriented. This unique cuticle may represent a fold where bract and scale fuse or directly the scale. No other internal cutinised membranes inside or between the rhomboidal bracts have been seen, suggesting that perhaps the cones were still immature. TEM observation of the bract cuticle shows well developed periclinal walls, anticlinal flanges and hypodermis (Plate VI, 41). The external layer of the cuticle presents lamellae that are 50 • thick. This lamellation seems to end at the periphery, and the rest of the cutin has a solid ultrastructure (Plate VI, 42). Taking into account all the characters that have been described we propose the new generic name Squamastrobus with the following diagnosis: G e n u s Squamastrobus nov. Type species: Squamastrobus tigrensis.
Diagnosis: Conifer twigs with up to fourth order branching. Branches radially and irregularly inserted bearing helically disposed leaves. Leaves scale-like, with cuticle externally smooth and amphistomatic. Stomata placed in rows, monocyclic to imperfectly dicyclic with Florin ring. Elongated pollen cones laterally attached to twigs bearing helically disposed compact microsporophylls with sacs including bisaccate grains. Seed cones terminal, elongated, composed of compact bract-scale complexes normally and helically disposed on a central axis. Bracts partly fused to ovuliferous scales(?), cutinized, with stomata. Leaf and bract cuticle with a three layered ultrastructure.
Squamastrobus tigrensis sp. nov. (Plates I-VI) Diagnosis: Conifer twigs bearing scale-like leaves up to 5 mm long with rostrate to obtuse apex, adpressed and disposed with a 3/8 phyllotaxis. Abaxial side slightly longer than adaxial side (Brachyphyllum type).
119
PLATE V
32-39. 32. 33-34. 35-36. 37. 38-39.
Squamastrobus tigrensis gen. n. Seed cone. Seed cone b o r n e d i s t a l l y on a b r a n c h . P a r a t y p e , BA P B 11340. × 1.5. Seed cone in t h e r o c k m a t r i x (fig.33) a n d a t r a n s f e r (fig.34). R h o m b o i d a l b r a c t - s c a l e c o m p l e x e s are s e e n in section. BA PB 11348. D e t a i l s at t h e b a s e of t h e t r a n s f e r (fig.34) s h o w i n g s h a p e of b r a c t scale c o m p l e x e s a n d a m e d i a l r o u n d c u t i n i s e d d o m e (arrow). Scale g i v e n by t h e h e a d of a n e n t o m o l o g i c a l pin. A seed cone a t t a c h e d to t h e d i s t a l p a r t of a b r a n c h (arrow). P a r a t y p e BA P B 11332. Detail of t h e a c u m i n a t e a p e x of o v u l i f e r o u s c o m p l e x e s (fig.38, arrow) t h a t i n c l u d e e l o n g a t e d bodies (fig.39, arrows). P a r a t y p e , BA Pb 11332. Scale g i v e n by t h e h e a d of a n e n t o m o l o g i c a l pin.
120 Leaf cuticles distally papillate at abaxial side, up to 18.2 ~m thick. Anticlinal flanges not interrupted by pits up to 46.8 pm thick. Epidermal cells on adaxial side isodiametric in stomatal rows, up to 23.4 ~m; between stomatal rows, subisodiametric to rectangular-elongate up to 45.8 pm long x 18.2 pm wide. Epidermal cells on abaxial side, in stomatal rows up to 28.6 ~m, and up to 49.4 ~m long x 15.6 ~m wide between stomatal rows. Leaves amphistomatic. Stomata monocyclic to imperfectly dicyclic. Subsidiary cells typically 4-5, isodiametric to oblong, sometimes in contact with neighbouring stomata. Stomata placed in rows with mainly oblique orientation (but longitudinal and transverse orientation is also seen). Florin ring slightly sunken. Stomatal apparatus rounded to elliptical. Subsidiary cells smaller than surrounding epidermal cells, with fine inner striations. Stomatal chamber up to 52 ~m long x 44.2 pm wide. Guard cells partially cutinised, up to 10.3 pm wide. Cutin structured in three layers, the external is lamellated, the medial solid (with no ultrastructure) and the inner is granular to spongy. Pollen cones attached laterally to third order twigs, elongated-cylindrical, up to 18 mm long x 3,5 mm wide. Microsporophylls compact, helically disposed on a central axis, expanded and distally curved, overlapping adjacent sporophylls. Pollen sacs subspherical to oval, up to l mm, bearing bisaccate grains of the Podocarpidites type. Pollen with a distal irregular leptoma and pendant sacci, up to 55 ~m long x 38 pm wide. Corpus rugulate proximally. Exine two layered up to 2 ~Lm thick composed of a thin internal lamellated nexine and an outer sexine. Seed cones terminal, usually disposed on third order branches, elongated with thinned base and obtuse apex, up to 5.5 cm long x 1.3 cm wide. Bract-scale complexes normally and helically disposed on a central axis, compact. Bracts with wide base and a slightly deflexed acuminate apex. Each bract bears a partly fused single elongated body near the cone axis (ovuliferous scales ?). Bracts distally cutinised with short stomatal rows on abaxial side;
stomata obliquely oriented, ca. 20 per sq. mm. Epidermal cells on stomatal cuticle isodiametric to elongate, up to 21 x 34 ~m wide. Bract cuticle distally papillate with serrulate margins. Cells more elongated towards cone axis, proximally granulose. Stomatal structure as for vegetative leaves. Cuticle of leaves and bracts with a layered ultrastructure; external layer with thin compact lamellae, median layer with few more spaced lamellae, otherwise solid and internally with a granular to spongy layer (due to decay ?). The median layer is the thickest cuticular component. Holotype: BA PB 11311 (twigs with pollen cone). Paratypes: BA PB 11335 (pollen cone with twig), 11336 (pollen cone with twig), 11340 (seed cone with twig), 11332 and 11341 (seed cone with twig). Other material studied: BTO horizon, BA PB 11313, 11330, 11337, 11338 (pollen cones), BA PB 11325, 11330, 11333 (seed cones) and BA PB Pm 16-18, 27, 28, 36 38. BTA horizon, BA PB 11339, 11342, 11344-11349, 11368-11373 (seed cones) and BA PB Pm 31-35, 39-45. Sterile twigs (Brachyphyllum tigrense Traverso), BTO horizon, BA PB 11312, 1131511322, 11326-11329. BTA horizon, BA PB 11343. BA PB Pm in BTO and BTA horizons, 1-15, 19-26. Locality: Estancia Bajo Tigre, Santa Cruz province, Argentina. Horizon: Baquer5 Formation, lower member, BTO and BTA fossiliferous levels. Age: Early Cretaceous (latest Barremian to earliest Aptian). Derivatio nominis: Squama = scale and strobus=cone-like, to signify that scale-like leafy twigs bear cones. The specific epithet, tigrensis refers to the locality Bajo Tigre.
Comparisons Three podocarps are known for the Baquer6 Formation (Archangelsky, 1966), viz. Trisacocladus tigrensis, Apterocladus lanceolatus and Podocarpus dubius. Trisacocladus differs in having long leaves, pollen with three air sacci
121
PLATE VI
40 46. 40. 41. 42. 43. 44. 45 46.
Squamastrobus tigrensis gen. n. B r a c t - s c a l e cuticle. Apex of t h e scale s h o w i n g e n l o n g a t e d cells a n d s e r r u l a t e m a r g i n . P A PB P m 32. x 40. S e c t i o n t h r o u g h t h e c u t i c l e s h o w i n g p e r i c l i n a l wall a n d a n t i c l i n a l flanges. T E M x 3000. A detail of t h e e x t e r n a l p a r t of t h e p e r i c l i n a l wall c u t i c l e s h o w i n g a t h i n l a m e l l a t e d b a n d (arrow). T E M x 100,000. Papillae. BA PB P m 34. x 400. D i f f e r e n t pollen g r a i n s t h a t a d h e r e to t h e cuticle. BA P B P m 33. x 400. S t o m a t a i n d i s t i n c t l y o r i e n t e d a n d e p i d e r m a l cells, m o r e e l o n g a t e d t o w a r d s t h e m a r g i n (fig.46). BA P B P m 32, 34, respectively, x 400.
122
(Trisaccites type) and a smaller seed cone with a thick central axis bearing orthotropous ovules. Apterocladus differs in having long leaves and pollen with three rudimentary air sacci (CaUialasporites type). Podocarpus dubius is known with only sterile twigs that differ from Squamastrobus in their long linear shape and cuticular structure. Several other genera with fertile remains have been described in Gondwana. The Jurassic strata of the Rajmahal Hills yielded petrified remains of vegetative and reproductive structures. Nipanioruha Rao (as described by Rao, 1947, 1949, emended by Vishnu-Mittre, 1959 and redescribed by Suthar and Sharma, 1987) has long and bilateral leaves; the pollen cones differ in having pollen with three sacci while seed cones are smaller, although having a similar compact nature and helical arrangement of the ovuliferous complexes; bracts, however, have a strong keel, not observed in Squamastrobus. Nipaniostrobus Rao (as described by Rao, 1943, Vishnu-Mittre, 1959 and Suthar and Sharma, 1987) has shoots with short linear leaves; the seed cones bear compact and differentiated bract-scale complexes helically disposed on a central axis; ovules have a curved micropyle and a short epimatium at the base. These cones are much smaller than in Squamastrobus. Mehtaia Vishnu-Mittre (as described by Vishnu-Mittre, 1959 and Suthar and Sharma, 1987) has shoots with short overlapping and spreading scale-like leaves and much smaller seed cones (the longest, 10 mm against 55 mm in Squamastrobus); the cones have loose to compact short bract-scale complexes disposed on a thick, fleshy axis, each bearing a large erect ovule. There is no evidence of sterile tissue related to the ovules as to suggest an epimatium or a scale. Sitholeya Vishnu-Mittre (1959) has short scale-like overlapping leaves and terminal single-seeded strobili with an inverted seed, much like modern Dacrydium and Podocarpus. Townrow (1967a) described Rissikia, a Triassic podocarp from Africa and Australia. It differs in possessing long bilateral leaves, rounded shape of the pollen cones t h a t pro-
duced bisaccate-striate pollen and thin spikelike female structures with trifid bracts. Mataia is another podocarp described by Townrow (op. cit.) from Jurassic strata of Australia and New Zealand. It also has long bifacial leaves and spike-like female structures composed of bracts and ovuliferous scales (each scale with two small inverted ovules). Townrow (1967a) described Nothodacrium from Jurassic strata of Antarctica; it differs from Squamastrobus in the shape of leaves and the laterally placed female cone that has free bracts and seed-scale complexes; associated male cones probably produced three winged pollen (Callialasporites type). Among living members of the Podocarpaceae, Squamastrobus shares the scale-like leaf type with Dacrydium, some Podocarpus species, Microcachrys and Microstrobos. Only the first two genera are now living in Argentina. The cuticular structure is also similar to some of the living representatives that have scalelike leaves. Serrulate margins are similar to those found in Microstrobos hookeriana (Florin, 1931, fig.68e). However in all living genera stomata tend to be longitudinally oriented and forming files. There are some exceptions like Dacrydium colensoi Hooker or Podocarpus ustus Brongniart et Grisebach, where stomata form ill-defined rows and may be indistinctly oriented. Vegetative parts of Podocarpus parlatorei Pilger, a species living in northern Argentina (del Fueyo, 1988) show a leaf hypodermis composed of fibers, not cutinised as they are in Squamastrobus. Stomata are similarly distributed in files though longitudinally oriented. The Florin ring is common to both living and fossil forms but the guard cells are poorly preserved in Squamastrobus. Epidermal cell walls of the living form are composed of an outer uniform layer (cuticle proper plus cutinised layer in the sense of Lyshede, 1982) and an inner laminated cellulosic layer. In Squamastrobus the epidermal cell walls are externally laminated, followed by a poorly laminated interface area and a solid nonlaminated median layer becoming granular towards the base. This ultrastructure is consistent with the
123 layering found in other fossil cuticles (Ticoa harrisii, Archangelsky et al., 1986). Squamastrobus pollen cones, as in most species of the family, have pollen with two sacci. Exceptions are Microcachrys, Microstrobos and Dacrycarpus that have pollen with three sacci. Saxegothaea has grains with no sacci and is referred to a different family by some authors, the Saxegothaeaceae (Gaussen, 1973; Woltz, 1985). The sporoderm organization in Squamastrobus is similar to extant members of the family. Pocknall (1981a, b) provided an account on the general morphology and the organization at an ultrastructural level for some members of Dacrydium, Dacrycarpus, Phyllocladus and Podocarpus from New Zealand. The ~region of weakness" found at the proximal roots of the sacci (Pocknall, op. cit.) is also known for Trisacocladus Archangelsky (Gamerro, 1965; Baldoni and Taylor, 1982). This sporoderm thinning may be related to a harmomegathical function (Baldoni and Taylor, op. cit.). The sporoderm in Squamastrobus has a two layered sexine; the external or ectosexine may be continuous (as in several extant members and Squamastrobus) or perforate-foveolate (Trisacocladus); the inner layer or endosexine is alveolate to collumelate, much in the same way as in many living podocarps (Pocknall, 1981a, b). Our collumelate component shows affinities with extant members rather than with the fossil Trisacocladus. This organization suggests a collumelate layer with a continuous and folded tectum-like layer having the same electron density. Collumelae (or rods as found in Trisacocladus) have an irregular distribution, leaving spaces of different sizes that produce an alveolate organization, comparable with the endosexine of cycad pollen (Baldoni and Taylor, op. cit.). The innermost part of the sexine is closely related to the nexine layer, showing interdigitaded components (Plate IV, 30, 31). The electron darker units appear as granules, merged with the electron lighter lamellate units around the whole corpus (including the apertural area). This ectosexine foot-layer is a common feature in extant and fossil podocarps so far analyzed.
The nexine in living and fossil podocarps is lamellated. Its preservation in extinct taxa varies according to the state of fossilization; in Squamastrobus only small areas show this organization (Plate IV, 30) while in Trisacocladus it has not been seen. Both genera belong to the podocarps and show minor structural differences suggesting that during the early Cretaceous there were at least two types of organization in some sporopollenin components, specially in the sexine layer. Most living Podocarpaceae have '~reduced" seed cones with only one or two ovules (~strobili" in Florin's terminology). However, compact cone structures with several ovuliferous complexes are known in Saxegothaea, Microstrobos and Microcachrys where seedscale units are axillary disposed on bracts. Phyllocladus has also compact seed cones but their axillary fertile complexes are much reduced. Female spike-like structures are known in few species, viz. Dacrydium franklinii Hooker, Podocarpus spicatus R. Brown and P. andinus Poepp. (Florin, 1958). Discussion
Squamastrobus may be placed in the family Podocarpaceae considering the similarities that exist with extant and fossil members of the group. The new genus supports the Gondwana affinity of the family during the Cretaceous when it was strongly diversified. Other coeval conifers, like the Araucariaceae, are different in that most characters remained the same since early Mesozoic times. Isolated scales (or bract-scale complexes) of Squamastrobus have not been found, although seed cones are common components in the plant bed. This may suggest that either the cones were all immature or the ovuliferous scales remained attached to the cone axis after maturation. The second hypothesis is probably more consistent, because isolated scales belonging to other seed cones (Tomaxellia, Araucarites) are abundant in these strata. Bract and scale were probably fused in one unit, partly cutinised in the distal portion of each compo-
124 nent, with stomata of the same kind as those found in vegetative leaves. Jurassic and Cretaceous podocarps had diversified female cones, consisting of fertile and sterile components with either compact
(Nipanioruha, Nipaniostrobus, Squamastrobus) or lax disposition (Mehtaia, Rissikia, Mataia, Trisacocladus). Probably, the cone habit predominated at t h a t time. However, single-seeded cones (Sitholeya), the commonest condition among extant members of the family, are also known in the Mesozoic. Phylogenetic links probably exist between some extant podocarps (Microcachrys, Phaerosphaera) and the Mesozoic cone-bearing taxa. Some living members with lax spike-like cones (i.e. Podocarpus spicatus) and similar Mesozoic genera (Mehtaia, Rissikia) may be phylogenetically related as well. However, they can also represent merely a state of reduction to a single-ovule stage. The epimatium in extant podocarps is a supplementary protective structure. In the fossil Nipaniostrobus, Mataia and Nipanioruha the folded overtips of the ovuliferous scales may represent the forerunner of the epimatium (Miller, 1977). The structure was also related to an ovule recurvation process (Vishnu-Mittre, 1959) or a modification of a portion of the seedscale complex (Suthar and Sharma, 1987). Squamastrobus shares most characters with several genera of the family but individually differs from all. The long history, wide geographic distribution caused by lands that drifted apart during the Mesozoic, and the presence of monotypic genera (or genera represented by few geographically widely separated species), clearly indicate that the Podocarpaceae is a heterogeneous family that was affected by abrupt palaeoclimatic and palaeoenvironmental changes. These stresses were and are responsible for the development of different lineages within the family resulting in a particular distribution of its extant members. The wide variation in chromosome number (from 9 to 19) also suggests the heterogeneity of the family (Hair and Beusenberg, 1958). Miller (1982) using two numerical analyses
found that the Pinaceae, Araucariaceae and Podocarpaceae sort out closely, suggesting some kind of relationship. However, this sorting was not consistent enough to recognize particular ancestors among the known Voltziaceae. Most Triassic and Jurassic genera from Gondwana were not considered by this author at that time. To trace the origin of Mesozoic podocarps, Townrow (1967a) suggested that Buriadia and Paranocladus (both Permian) were possible candidates though no fructifications were known at that time. More recently, seedbearing units were found in different areas of Gondwana and related to both palaeozoic genera. Two families are known, viz. the Buriadiaceae (Pant, 1982) and Ferugliocladaceae (Archangelsky and C6neo, 1987). The fertile shoots of Genoites, a Permian Buriadiaceae from Patagonia (Cfineo, 1986), are lax spike-like structures bearing ovules axillary on sterile appendages, not differentiated from normal leaves; these ovuliferous structures tend to have a distal disposition on the fertile branches. Some Mesozoic podocarps, specially those with lax cones may well have been in the same lineage with the Buriadiaceae with the subtending leaves transformed into bracts and a more compact structure of the bract-ovule complexes. The Ferugliocladaceae had compact cones of a similar size and shape to Squamastrobus. They differ in the separation of bract and ovuliferous scales. In Ferugliocladus, the ovuliferous scale is an elaborate structure, adapted for dispersal (Archangelsky and C6neo, 1987). The genus Ugartecladus had simple ovules (or ovuliferous scales), free from the bracts. Such cone organization may have developed into a Nipaniostrobus or Squamastrobus type by ovule recurvation and bractscale partial fusion. This would suggest another lineage leading to the Podocarpaceae. At this point of our knowledge it seems that Townrow's original suggestion may have some firm ground. It is still premature to speculate further until we know more about Permian, and specially Triassic podocarps in order to
125
define more precise boundaries between the three families that have been discussed. Nevertheless, the Buriadiaceae and the Ferugliocladaceae offer a good ancestral stock of exclusively Gondwanan distribution from which some Mesozoic conifers may have evolved like the Podocarpaceae and/or the Araucariaceae (Archangelsky, 1985). Not less important is the palaeogeographic distribution of the Permian genera Genoites, Ferugliocladus and Ugartecladus, t h a t are found near the place from where Squamastrobus has been recovered (southern Patagonia).
Acknowledgements We are grateful to the Consejo Nacional de Investigaciones Cientificas y T~cnicas (CONICET) and International Cooperative Science Program of the National Science Foundation (BSR-8313786 to T.N. Taylor) for support of this project. We wish to t h a n k Liliana Seoane for technical assistance, Miguel Archangelsky for photographic work and Isabel Farlas for useful suggestions with TEM work. We are most grateful to CEVAN-CONICET for the use of the TEM.
References Archangelsky, S., 1966. New Gymnosperms from the Tic6 Flora, Santa Cruz province, Argentina. Bull. Br. Mus. Nat. Hist. Geol., 13:259 295. Archangelsky, S., 1967. Estudio de la Formaci6n BaquerS, Cretficico inferior de S a n t a Cruz, Argentina. Rev. Mus. La Plata, Secc., Paleontol., 5:63 171. Archangelsky, S., 1985. Aspectos evolutivos de las conlferas gondwfinieas del Paleozoico. Bull. Sect. Sci., 8: 115 124. Archangelsky, S. and Cdneo, R., 1987. Ferugliocladaceae, a new Conifer family from the Permian of Gondwana. Rev. Palaeobot. Palynol., 51: 3-30. Archangelsky, S. and del Fueyo, G., 1987. Sobre una Podocarpficea f~rtil del Cretficico inferior de la provincia S a n t a Cruz, Repdblica Argentina. Act. VII Simp. Argent. Paleobot. Palinol., Buenos Aires, pp.85 88. Archangelsky, S., Baldoni, A., Gamerro, J.C. and Seiler, J., 1984. Palinologia estratigrfifica del Cretficico de Argentina austral. III. Distribucibn de las especies y conclusiones. Ameghiniana, 21(1): 15 33. Archangelsky, S., Taylor, T.N. and Kurmann, M.H., 1986. U l t r a s t r u c t u r a l studies of fossil plant cuticles: Ticoa
harrisii from the early Cretaceous of Argentina. Bot. J. Linn. Soc., 92:101 116. Baldoni, A.M. and Taylor, T.N., 1982. The ultrastructure of Trisaccites pollen from the Cretaceous of southern Argentina. Rev. Palaeobot. Palynol., 38:23 33. Cfineo, R., 1986. Ejemplares f~rtiles de Genoites patagonica Feruglio (Buriadiaceae, Coniferopsida ?) del P~rmico de Chubut, Repdblica Argentina. Ameghiniana, 22: 269-279. del Fueyo, G., 1988. Anatomia y ontogenia foliar de Podocarpus parlatorei (Podocarpaceae). Bol. Soc. Arg. Bot. 353 367. Florin, R., 1931. U n t e r s u c h u n g e n zur stammesgeschichte der coniferales. K. Sven. Vetenskapakad. Handl., 10: 3 588. Florin, R., 1940. The Tertiary Fossil Conifers of South Chile and their phytogeographical significance. Kungl. Sv. Vetenskapakad. Handl., 19(2): 1-107. Florin, R., 1958. Notes on the systematics of the Podocarpaceae. Acta Horti Bergiani, 17(11): 403 411. Gamerro, J.C., 1965. Morfologia del polen de la conifera Trisacocladus tigrensis Archang. de la Formaci6n Baquer6, Provincia de S a n t a Cruz, Ameghiniana, 4: 31-38. Gaussen, H., 1973. Les Gymnospermes actuelles et fossiles. Trav. Lab. For. Toulouse, 2(1): 1 43. Hair, J.B. and Beusenberg, E . J , 1958. Chromosomal evolution in the Podocarpaceae. Nature, 181(4623): 1584 1586. Lyshede, O.B., 1982. Structure of the outer epidermal wall in xerophytes. In: The Plant Cuticle, D.F. Cutler, K.L. Alvin and C.E. Price (Editors). Linn. Soc. London, Sympos. Ser., 10: 87-98. Miller, C.N., 1977. Mesozoic Conifers. Bot. Rev., 43(2): 217 280. Miller, C.N., 1982. Current status of Paleozoic and Mesozoic Conifers. Rev. Palaeobot. Palynol., 37: 99- 114. Pant, D.D., 1982. Some Lower Gondwana Gymnosperms and their relationships. Rev. Palaeobot. Palynol., 37: 55 70. Pocknall, D.T., 1981a. Pollen morphology of the New Zealand species of Dacrydium Solander, Podocarpus L'Heritier and Dacrycarpus Endlicher (Podocarpaceae). N.Z.J. Bot., 14:67 95. Pocknall, D.T., 1981b. Pollen morphology of Phyllocladus L.C. et A. Rich. N.Z.J. Bot., 19:259 266. Rao, A.R., 1943. Nipaniostrobus, a new genus of Dacrydium-like seed-bearing cones and other silicified plants from the Rajmahal Series. Proc. Nat. Acad. Sci., India, 13(2): 113 132. Rao, A.R., 1947. Nipanioruha granthia gen. et sp. nov.; a new petrified coniferous shoot from the Rajmahal Hills, Bihar. In: M.O.P. Iyengar commem, volume, Indian Bot. Soc., pp.389 397. Rao, A.R., 1949. The megastrobilus of Nipanioruha granthia Rao, A.R. Curr. Sci., India, 18:447 448. Suthar, O.P. and Sharma, B.D., 1987. Petrified fructifications of conifers from the Jurassic of Rajmahal Hills, India. Geophytology, 16(2): 159 165. Townrow, J.A., 1967a. On Rissikia and Mataia podocarpaceous conifers from the lower Mesozoic of southern lands. Pap. Proc. R. Soc. Tasmania, 101:103 136.
126 Townrow, J.A., 1967b. On a conifer from the Jurassic of East Antarctica. Pap. Proc. R. Soc. Tasmania, 101: 137-147. Traverso, N.E., 1966. Brachyphyllum tigrense n u e v a con~fera de la FormaciSn BaquerS, Cret~cico de S a n t a Cruz. Ameghiniana, 4: 189-194.
Vishnu.Mittre, 1959. Studies on the fossil flora of Nipania (Rajmahal Series), Bihar. Coniferales. Palaeobotanist, 6(2): 82-112. Woltz, P., 1985. Place des Gymnospermes end~miques des Andes M~ridionales dans la v~g~tation du Chili. Lazaroa, 8: 293-314.
109
Elsevier Science Publishers B.V., Amsterdam - - Printed in The Netherlands
SQUAMASTROBUS GEN. N., A FERTILE PODOCARP FROM THE EARLY CRETACEOUS OF PATAGONIA, ARGENTINA SERGIO ARCHANGELSKY and GEORGINA DEL FUEYO DivisiOn Paleobotdnica, Museo Argentino de Ciencias Naturales "B. Rivadavia", Av. Angel Gallardo 470, Buenos Aires 1405 (Argentina) CONICET (Received April 20, 1988; revised and accepted October 3, 1988)
Abstract Archangelsky, S. and del Fueyo, G., 1989. Squamastrobus gen. n., a fertile podocarp from the early Cretaceous of Patagonia, Argentina. Rev. Palaeobot. Palynol., 59: 109-126.
Squamastrobus tigrensis nov. gen. et sp. has been found in early Cretaceous strata (Baquer5 Formation), Santa Cruz Province, Argentina. It is based on branches with squamiform leaves, laterally attached pollen cones and terminally disposed seed cones. The cuticle of leaves and female bract-scale complexes was studied in their general structure and ultrastructure. The pollen cones contain bisaccate pollen grains that are similar both structurally and ultrastructurally with extant and fossil members of the Podocarpaceae. The seed cones are compact structures resembling some taxa found in Mesozoic Gondwana strata. Comparisons made with living and extinct members of the Podocarpaceae suggest some phylogenetic links between Mesozoic cone-bearing forms with the extant genera Microcachrys and Pherosphaera. Finally, some considerations on the origin of Mesozoic podocarps are also included in regard to recently discovered Permian conifers from Gondwana.
Introduction The family Podocarpaceae is widely distributed in Cretaceous strata of Patagonia where pollen assemblages are dominated by conifers, mainly Cheirolepidiaceae; pollen with two and three sacci are also common. Megafossil remains assignable to conifers are abundant, usually as sterile twigs belonging to several genera, some with affinities with the Podocarpaceae. Florin (1940) suggested that most Mesozoic Elatocladus impressions from the Southern Hemisphere probably belong to this family. When these leaves are found with a cuticle their assignment to the podocarps is more certain, and separate genera have been established on this ground (as Coronelia Florin, op. cit.). Yet it is only with fertile specimens, especially with the pollen cones, 0034-6667/89/$03.50
that a more natural relationship can be established at a family level. The few seed structures that have been described from southern lands (Rissikia, Mataia, Trisacocladus etc.) partly differ from living genera in their cone-like habit. These Mesozoic taxa suggest that during the Cretaceous several lineages were developing. Among the coniferous twigs known in early Cretaceous strata of Patagonia, those bearing scale-like leaves assigned to the genus Brachyphyllum are the most abundant. In this paper we describe fertile pollen and seed structures organically attached to twigs that have been referred to Brachyphyllum tigrense (Traverso, 1966; Archangelsky and del Fueyo, 1987). So far, podocarp remains described with fertile structures from these strata have leaves that resemble living members in their morphology
~'} 1989 Elsevier Science Publishers B.V.
110
and anatomy. Three genera were referred to the Podocarpaceae: Trisacocladus, with pollen cones having pollen with three air bladders (Trisaccites type) and seed cones with a thick central axis bearing orthotropous seed-scale complexes, Apterocladus, with pollen cones having grains with three rudimentary sacci (CaUialasporites type) and sterile twigs named Podocarpus dubius (Archangelsky, 1966). Squamastrobus is the new genus proposed to combine vegetative remains of Brachyphyllum tigrense Traverso with pollen and seed structures in organic connection. The pollen has two sacci and is similar in morphology, structure and ultrastructure with extant members of the group; the leaves and their cuticle can also be compared with some taxa presently known in the Southern Hemisphere (though not in Patagonia); finally, the seed cones, although partly known in their organization, differ from other fossil or extant taxa. The exceptional preservation of the mummified remains allowed their study with both scanning and transmission electron microscopy. Materials and m e t h o d s The specimens were recovered from the Baquer6 Formation, dated as latest Barremian to early Aptian (Archangelsky et al., 1984). They were fbund in 1985 at the Bajo Tigre locality in Santa Cruz province during a combined CONICET-NSF expedition. The precise location of the bed is shown in map 2, fossiliferous site 7 (Archangelsky, 1967). The
abundant mummified 1 material includes twigs, pollen and seed cones. The leaf cuticle was easily removed from the matrix and treated twice with 40% nitric acid followed by 5% ammonium hydroxide and then washed in distilled water. To remove some residue, ultrasound was used for 10 seconds. For optical observation cuticles were mounted in glycerine jelly. For SEM observation the cuticles of leaves, their sections and pollen sacs were suspended in 1:1 water-alcohol and dropped on a double face scotch tape adhered to a stub, and after drying it was coated with goldpalladium. For TEM observation, leaf fragments, pollen sacs and seed cone bracts were stained with 1% OsO4 for 2 hours at room temperature, washed for 30 minutes in distilled water and dehydrated in an ascendent alcohol series [25%, 50%, 70%, 95% and 100% (15' each and twice with 100°/0)], followed by acetone 100% (twice, 15' each). The material was then infiltrated using a rotator with the following mixtures: acetone 3/Spurt 1, 6 hours, acetone 1/Spurr 1, 6 hours and 2 changes with Spurr, each for 6 and 16 hours. Then the fragments were included in moulds and dried in vacuum at 70°C for 48 hours. Ultrathin sections (ab. 800 A thick) were made with a diamond knife using a SORVAL manual ultramicrotome. The 1The term mummification used here refers to fossils with tissues t h a t are preserved in a way t h a t their s t r u c t u r e and u l t r a s t r u c t u r e reflect exactly living a n a l o g u e s (leaf cuticles, pollen). Comparative studies of their most minute s t r u c t u r e s are possible because diagenetic processes during fossilization did not affect them.
PLATEI 1 8.
1. 2. 3. 4,
5. 6,
7. 8.
Squamastrobus tigrensis
gen. n. Vegetative part. B r a n c h e s of first (arrow), second and third orders. BA PB 11312. Ultimate and p e n u l t i m a t e order branching. BA Pb 11325. External view of a leaf showing slightly s u n k e n stomata, smooth periclinal wall; anticlinal flanges are also evident. SEM x 400. External view of distal part of a leaf showing papillae. SEM x 400. Section of abaxial cuticle of leaf. A thick externally smooth periclinal wall and anticlinal flanges are seen; a stoma (arrow) with s u p r a s t o m a t i c chamber (U-shaped) and a partly cutinised hypodermis are also shown. SEM x 500. A detail showing cutinised periclinal wall, anticlinal flanges and hypodermis. SEM x 1000. Section of abaxial cuticle showing periclinal wall, anticlinal flanges and a stoma (arrow). x 400. Section of a b a s a l m o s t part of leaf showing extra-cutinised component (arrow). x 400.
111
PLATE I
112
sections were then mounted in single hole grids coated with F o r m v a r and stained with KMnO4 (5-10') and Uranil acetate (30"). A Leitz Dialux microscope was used for light microscopy; photomicrographs were t aken with a Canon FN camera using Kodak Panatomic film. A Jeol JSM-35CF microscope was used for SEM observations while a Jeol J E M 100C of the CEVAN-CONICET Institute was used for TEM. All the specimens are lodged in the Paleobotanical Collection of the Buenos Aires N at ur a l History Museum (BA PB for megafossils and BA PB Pm for slides).
Description The specimen BA PB 11312 (Plate I, 1) has up to four orders of branches. Branches are radially and irregularly inserted. The main branch is 2 cm wide; second order branches are 0.5 cm wide, with penultimate branches up to 2.5 mm wide and the last order branches are short and I mm wide. The widest main branch is 2.8 cm and it was found in the specimen BA PB 11313. Second order branches vary from 4 6 mm in width. Third order branches (Plate I, 2) are the commonest varying from 1.5 to 2.5 mm in width, the longest seen attaining 5.4 cm (BA PB 11321). Ultimate branches are up to 1.6 cm long and 0.5-1 mm wide (BA PB 11325, Plate I, 2). Leaves are scale-like, ovate, adpressed, with entire margins, helically disposed with a 3/8 phyllotaxis. The largest (found in second to fourth order branches) are 3.8 mm long x 1.7 mm wide; they have a rostrate apex and an oval leaf base, 2.7 mm long x 1.5 mm
wide. Width ratio of leaves 1:1.2-2.4. Smaller leaves have an obtuse apex. In first order branches (BA PB 11312, Plate I, 1) leaves are up to 5.5 mm long (with adaxial cuticle 3.8 mm long) and in second order branches they are 3.8 mm long (with a 2 mm long adaxial cuticle); in third order branches, leaves 3.3 mm long have a 1.2 mm long adaxial cuticle. (A detailed description and illustration of different leaf types can be seen in Traverso, 1966). Both cuticles are smooth externally, but contours of epidermal cells (the interception of anticlinal flanges with external periclinal wall), especially those between stomatal rows can be seen (Plate I, 3). Towards the apex of leaves external round papillae are present on abaxial cuticle (Plate I, 4); it shows epidermal cells with smooth periclinal walls in internal view (Plate I, 5); the cuticle is 5 pm(10.4 pm)118.2 ~m thick (20 measurements) (Plate I, 6). Anticlinal flanges are continuous, not interrupted by pits and smooth from base to top where they expand laterally (Plate I, 6, 7); they are 7.8(15.6)46.8 ~m wide (17 measurements) and 7.8(10.4)13 ~m high (26 measurements). Remnants of cutinised hypodermal cells are seen (Plate I, 5, 6). Leaf bases develop extra cutin t hat has no definite structure, organization or thickness (Plate I, 8). It may have functioned as a protective layer in the abcission area or as an agent for water retention. The leaf margins have a discontinuous serrulate wing that lacks in basal portions. In the distal half of the leaf, the serrate wing is 1Figures in b r a c k e t s a r e t h e m e a n v a l u e s of all m e a s u r e ments.
P L A T E II 9 14. 9. 10. 11. 1 2 13. 14.
Squamastrobus tigrensis gen. n. V e g e t a t i v e part. A b a x i a l leaf c u t i c l e s h o w i n g i r r e g u l a r s t o m a t a l files BA Pb P m 1. x 100. L e a f m a r g i n s h o w i n g s e r r u l a t e edge. B A Pb P m 1. x 400. A b a x i a l l e a f c u t i c l e s h o w i n g s h a p e of cells in a n d b e t w e e n s t o m a t a l rows. R e m n a n t s of h y p o d e r m a l cells a r e also s e e n (arrows). BA Pb P m 2. x 400. T w o focci of a s t o m a s h o w i n g g u a r d cells (fig.12) a n d a p r o x i m a l s e c t o r of s u b s i d i a r y cells w i t h s t r i a t i o n s (fig.13). BA Pb P m 2. x 1000. I n t e r n a l view of two s t o m a t a s h o w i n g F l o r i n rings, a cycle of s u b s i d i a r y cells a n d a n t i c l i n a l flanges. C u t i n i s e d h y p o d e r m i s cells a r e s e e n at t h e left b o t t o m corner. S E M x 400.
:>
114 up to 43.3 pm wide and has p e r p e n d i c u l a r to oblique cells of r o u n d e d to a c u t e c o n t o u r (Plate II, 10). On b o t h cuticles epidermal cells h a v e different shapes in r e g a r d to t h e i r disposition b e t w e e n s t o m a t a l rows or not. In s t o m a t a l rows t h e y are mostly i s o d i a m e t r i c while bet w e e n s t o m a t a l rows t h e y are from subisodiametric to r e c t a n g u l a r e l o n g a t e (Plate II, 11). In the adaxial cuticle, in s t o m a t a l rows, t h e y are 2 6 p m l o n g x 2 3 . 4 pm wide, with an a r e a of 608.4~m2; b e t w e e n s t o m a t a l rows, 4 5 . 8 p m long x 18.2 ~m wide, with an a r e a 851.7 ~m 2. In the abaxial cuticle, cells in a row b e t w e e n s t o m a t a are 28.6 pm with an a r e a 817.9 pm 2 and b e t w e e n s t o m a t a l rows, 49.4 ~m long x 15.6 pm wide, with an a r e a 770.6 pm 2 (total measurements, 920). Leaves are a m p h i s t o m a t i c with m o n o c y c l i c s t o m a t a (rarely imperfectly dicyclic). F o u r to five subsidiary cells are radially, sometimes elliptically placed; t h e y are p o l y g o n a l and i s o d i a m e t r i c or oblong with r o u n d e d sides. S u b s i d i a r y cells of n e i g h b o u r i n g s t o m a t a are often in contact. S t o m a t a are c o m m o n l y placed in rows and h a v e oblique o r i e n t a t i o n ; l o n g i t u d i n a l and t r a n s v e r s e s t o m a t a l orientation are also seen. S t o m a t a l rows s e p a r a t e d by 2 6 rows of epidermal r e c t a n g u l a r to e l o n g a t e cells (Plate II, 9). S t o m a t a l index is 95 per sq. mm. T h e F l o r i n ring is up to 5.4 ~m thick, elliptical, slightly sunken, c o n t i n u o u s and with gently sloping sides. L e n g t h - b r e a d t h ratio: 21/34. T h e s t o m a t a l a p p a r a t u s is r o u n d e d to elliptical ( e l o n g a t i o n i n d i s t i n c t l y oriented, P l a t e I, 3). Anticlinal flanges s e p a r a t i n g c o m m o n epidermal and subsidiary cells are of the same size or smaller t h a n flanges b e t w e e n n o r m a l epider-
mal cells; a n t i c l i n a l flanges s e p a r a t i n g subsidiary from g u a r d cells are m u c h smaller. Subsidiary cells are slightly smaller t h a n neighb o u r i n g epidermal cells (Plate II, 11, 14). The i n n e r surface of periclinal wall of subsidiary cells with fine s t r i a t i o n s r a d i a l l y or parallel o r i e n t e d to s t o m a t a l m o u t h (Plate II, 13). Width of s t o m a t a l c h a m b e r 20.6(31)44.2 ~m; length, 30.9(40.6)52 ~m. S u p r a s t o m a t a l chamber U to V shaped in section with widening m o u t h t o w a r d s the surface (Plate I, 5, 7). G u a r d cells slightly cutinised, with l a t e r a l l y a r c h e d o u t e r and i n n e r sides, t h i n n i n g t o w a r d s poles w h e r e t h e y meet and slightly p r o t r u d e (Plate II, 12, 14). G u a r d cells 4.2(8.2)10.3 ~m wide. The s t r u c t u r e of the cuticle a r o u n d a stoma as seen with T E M shows the F l o r i n ring, cutinised a n t i c l i n a l flanges and r e m n a n t s of cutin on g u a r d cells (Plate III, 15). The u l t r a s t r u c t u r e of the e x t e r n a l periclinal wall shows r e m n a n t s of e p i c u t i c u l a r wax (Plate III, 18). T h e cuticle is layered. T h e e x t e r n a l l a y e r is lamellated, the most c o m p a c t lamellae are 50/~ t h i c k (Plate III, 19); i n t e r n a l l y , lamellae become more s e p a r a t e d (up to 200 A, P l a t e III, 18) and an i n t e r f a c e to the solid, t h i c k c o m p o n e n t of the cuticle is seen (Plate III, 17). The i n n e r m o s t g r a n u l a r to spongy layer, is approxim a t e l y 0.6 ~m t h i c k (Plate III, 16). The pollen cones are a t t a c h e d l a t e r a l l y to third o r d e r twigs (BA PB 11311, P l a t e IV, 20); t h e y are elongated, cylindrical, t h i n n i n g towards base and apex, 12(14.3)18 mm long x 1.2(2.4)3.5 mm wide (Plate IV, 21). Central axis 0 . 2 - 0 . 4 m m wide, with n o r m a l l y att a c h e d and s h o r t l y p e d u n c u l a t e microsporophylls, helically disposed, distally e x p a n d e d
PLATE Ill 15 19. Squamastrobus tigrensis gen. n. Leaf cuticle ultrastructure (TEM). 15. Section through a stoma showing Florin ring (arrow), mouth, remnants of guard cells (G) and anticlinal flanges of subsidiary cells (S). x 2000. 16. Detail of inner zone of periclinal wall cuticle showing a granular (degraded?) structure, x 50,000. 17. Detail of outer zone of periclinal wall cuticle showing external laminated components with an interface to a solid structure (bottom). x 50,000. 18. Detail of external lamination of the cuticle and remnants of epicuticular wax(?) (arrow). x 50,000. 19. Detail of lamination (arrow) in the outer part of periclinal wall at the stomatal mouth region, x 80,000.
.-]
y~
21
2
116 and s t r o n g l y curved, up to 90 ° , o v e r l a p p i n g a d j a c e n t s p o r o p h y l l s (Plate IV, 21). Two(?)subspherical pollen sacs (slightly e l o n g a t e d due to compression), 0.4(0.7)1 mm in d i a m e t e r (Plate IV, 25), h a v e a light yellow colour, c o n t r a s t i n g with the s u r r o u n d i n g d a r k e r tissue (Plate IV, 21). Obliquely o r i e n t e d scales are placed in a close spiral at the cone base. P o l l e n sacs are easily detached; t h e y are composed of a compact mass of pollen g r a i n s with a m e m b r a n e cover. The e x t e r n a l g r a n u l o s e wall Of pollen sacs has no visible cellular s t r u c t u r e , but a b u n d a n t bodies of different sizes and shapes a d h e r e with no p a r t i c u l a r o r i e n t a t i o n (Plate IV, 26). Pollen g r a i n s are bisaccate, of the Podocarpidites type (Plate IV, 22-24), with s t r o n g l y r u g u l a t e body in its p r o x i m a l side; sacci p e n d a n t (Plate IV, 24, 26), often folded, with u s u a l l y i s o d i a m e t r i c i r r e g u l a r endoreticulation, 2 4 pm wide (Plate IV, 22, 23). Exine 2 pm thick; on the distal side of the body an i r r e g u l a r l e p t o m a is seen (Plate IV, 22). M e a s u r e m e n t s (in 20 grains) give a t o t a l l e n g t h of 38(52.5)55 pm, t o t a l w i d t h of 23(31)38 pro, a body l e n g t h of 28(34)39 ~m, a body h e i g h t of 12(21.6)33 ~m, a s a c c u s l e n g t h of 15(21.6)25 ~m, a sac h e i g h t of 14(20.6)28 I~m and a d i s t a n c e b e t w e e n sac bases of 3(6.1)13 pro. In section, the pollen sac shows c o m p a c t l y disposed and s t r o n g l y folded g r a i n s (Plate IV, 26-28). The s p o r o d e r m consists of two d i s t i n c t layers, an inner, c o n t i n u o u s nexine and an outer, more
electron-dense sexine. The nexine is homogeneous and lamellated, with slightly w a v y o u t l i n e in section view (Plate IV, 29). Sections in proximal p a r t s of the c o r p u s show an e x t e r n a l l a y e r (sexine) composed of s p o r o p o l l e n i n rods t h a t e x t e r n a l l y fuse to form a c o n t i n u o u s n o n pitted, s t r o n g l y s i n u o u s t e c t u m (that corresponds to the r u g u l a t e s c u l p t u r e in surface view). The rods are l o n g e r n e a r the proximal pole area, b e c o m i n g s h o r t e r t o w a r d s the apert u r a l a r e a and the base of the sacci (Plate IV, 27, 29). B e n e a t h this e x t e r n a l layer, the alveolar sexine shows in section large spaces and i r r e g u l a r r o u n d e d s p o r o p o l l e n i n u n i t s (Plate IV, 29, 30, 31) t h a t are s i t u a t e d directly on the nexine and seem to i n t e r d i g i t a t e with it (Plate IV, 30). The i n n e r p a r t of the sexine is s t r o n g l y r e d u c e d t o w a r d s the a p e r t u r a l a r e a a n d the sacci. S p o r o d e r m sections t h r o u g h the sacci show a s m o o t h c o n t i n u o u s o u t e r c o v e r t h a t is an e x t e n s i o n of the w a v y t e c t u m of the corpus. Loose s p o r o p o l l e n i n units are present b e n e a t h the o u t e r l a y e r as i n t e r n a l rod-like extensions (endomuri) t h a t i r r e g u l a r l y a n a s t o m o s e in the p e r i p h e r a l a r e a of the sacci to form an imperfect reticulum. A l t h o u g h the pollen is still f o u n d as a c o m p a c t mass inside the sacs, individual grains are usually separated (Plate IV, 28). The clear differentiation of the sporoderm layers suggests t h a t the pollen was almost mature. This is also supported by the r e c o v e r y of isolated grains from the sacs t h a t have
PLATE IV 20-31. 20. 21. 22 23. 24. 25. 26. 27 28. 29. 30. 31.
Squamastrobus tigrensis gen. n. Pollen cone. Pollen cone in organic connection to a leafy branch. Holotype, BA PB 11311. x 2. A detail of the same showing central axis and pollen sacs. x 8. Two focci of an isolated grain from a pollen sac of the holotype, x 850. Another grain in equatorial view, isolated from the holotype, x 850. A view of a pollen sac. SEM x 90. Bisaccate grains adhering to the inner surface of the sac membrane. SEM x 400. Sections through grains from a pollen sac. The sinuous tectum of the corpus (C), sacci (S) and leptoma (L) are seen. TEM x 2000. A detail of the leptoma area showing the thin exine, rod like components leaving large spaces and a sinuous tectum (arrow). TEM x 6000. A detail of the edge of the leptoma showing the nexine (partly lamellated) and sexine globular components (arrow). TEM × 40,000. Section through the corpus on proximal side of grain showing the foot layer with granulose to globose components, a columella (arrow) and wavy tectum. TEM x 40,000.
-3
"--1
118
attained their mature size and shape (Plate IV, 22, 24) suggesting that they fossilized at a time when their content was ready for dispersal. Seed cones are terminal and attached to third order branches (Plate V, 32, 37, BA PB 11340, 11332). They are elongated, cylindrical with a thinned base and an obtuse apex, 1.5(2.8)5.5 cm long x 0.7(1.2)1.3 cm wide. Central axis l m m wide (BA PB 11372), bearing compactly and normally attached bract-scale complexes that are helically disposed. Bracts with a wide base, separated, with slightly deflexed and acuminate apex (Plate V, 38, 39), rhomboidal in cross section with expanded lateral angles (Plate V, 33-36). Each bract bears a single elongated body that is situated near the cone axis (Plate V, 38, 39). Eventually, these bodies (ovuliferous scales ?) are connected (or partially fused) to the bracts as suggested by their disposition (Plate V, 39, arrow). Bracts distally cutinised bearing stomata on the abaxial side, forming short illdefined rows and oriented mostly obliquely (Plate VI, 45, 46). There are about 20 stomata per sq. mm. Epidermal cells on stomatal cuticle 34 x 21 ~m wide, isodiametric or slightly elongated. Margins serrulate (Plate VI, 40) with distally placed papillae (Plate VI, 43). Hypodermis cutinised. The bract cuticle becomes thinner towards the cone axis where it has no stomata, papillae or cutinised hypodermis and the cells are more elongated, up to 591~m long x 12 gm wide. Cell contours disappear at the most basal part where the cuticle is granulose. Several types of pollen grains adhere to this cuticle (Classopollis, Cyclusphaera, Podocarpidites, among others) (Plate VI, 44). Stomata similar to those found in vegetative leaves, i.e. monocyclic, with 4 5 radially placed polygonal to isodiametric subsidiary cells, sometimes in contact. A transfer of a cone (Plate V, 34) shows bracts with a rhomboidal section, one with a small salient cutinised pyramid-like structure (Plate V, 35, 36, arrows) and a similar cuticle to the outer bract membrane, i.e. thick, with stomata and serrulate margins. However it differs in the lack of papillae, epidermal cells t h a t tend to be all
isodiametric, and a higher stomatal index (48 against 20 per sqmm); stomata are usually transversely oriented. This unique cuticle may represent a fold where bract and scale fuse or directly the scale. No other internal cutinised membranes inside or between the rhomboidal bracts have been seen, suggesting that perhaps the cones were still immature. TEM observation of the bract cuticle shows well developed periclinal walls, anticlinal flanges and hypodermis (Plate VI, 41). The external layer of the cuticle presents lamellae that are 50 • thick. This lamellation seems to end at the periphery, and the rest of the cutin has a solid ultrastructure (Plate VI, 42). Taking into account all the characters that have been described we propose the new generic name Squamastrobus with the following diagnosis: G e n u s Squamastrobus nov. Type species: Squamastrobus tigrensis.
Diagnosis: Conifer twigs with up to fourth order branching. Branches radially and irregularly inserted bearing helically disposed leaves. Leaves scale-like, with cuticle externally smooth and amphistomatic. Stomata placed in rows, monocyclic to imperfectly dicyclic with Florin ring. Elongated pollen cones laterally attached to twigs bearing helically disposed compact microsporophylls with sacs including bisaccate grains. Seed cones terminal, elongated, composed of compact bract-scale complexes normally and helically disposed on a central axis. Bracts partly fused to ovuliferous scales(?), cutinized, with stomata. Leaf and bract cuticle with a three layered ultrastructure.
Squamastrobus tigrensis sp. nov. (Plates I-VI) Diagnosis: Conifer twigs bearing scale-like leaves up to 5 mm long with rostrate to obtuse apex, adpressed and disposed with a 3/8 phyllotaxis. Abaxial side slightly longer than adaxial side (Brachyphyllum type).
119
PLATE V
32-39. 32. 33-34. 35-36. 37. 38-39.
Squamastrobus tigrensis gen. n. Seed cone. Seed cone b o r n e d i s t a l l y on a b r a n c h . P a r a t y p e , BA P B 11340. × 1.5. Seed cone in t h e r o c k m a t r i x (fig.33) a n d a t r a n s f e r (fig.34). R h o m b o i d a l b r a c t - s c a l e c o m p l e x e s are s e e n in section. BA PB 11348. D e t a i l s at t h e b a s e of t h e t r a n s f e r (fig.34) s h o w i n g s h a p e of b r a c t scale c o m p l e x e s a n d a m e d i a l r o u n d c u t i n i s e d d o m e (arrow). Scale g i v e n by t h e h e a d of a n e n t o m o l o g i c a l pin. A seed cone a t t a c h e d to t h e d i s t a l p a r t of a b r a n c h (arrow). P a r a t y p e BA P B 11332. Detail of t h e a c u m i n a t e a p e x of o v u l i f e r o u s c o m p l e x e s (fig.38, arrow) t h a t i n c l u d e e l o n g a t e d bodies (fig.39, arrows). P a r a t y p e , BA Pb 11332. Scale g i v e n by t h e h e a d of a n e n t o m o l o g i c a l pin.
120 Leaf cuticles distally papillate at abaxial side, up to 18.2 ~m thick. Anticlinal flanges not interrupted by pits up to 46.8 pm thick. Epidermal cells on adaxial side isodiametric in stomatal rows, up to 23.4 ~m; between stomatal rows, subisodiametric to rectangular-elongate up to 45.8 pm long x 18.2 pm wide. Epidermal cells on abaxial side, in stomatal rows up to 28.6 ~m, and up to 49.4 ~m long x 15.6 ~m wide between stomatal rows. Leaves amphistomatic. Stomata monocyclic to imperfectly dicyclic. Subsidiary cells typically 4-5, isodiametric to oblong, sometimes in contact with neighbouring stomata. Stomata placed in rows with mainly oblique orientation (but longitudinal and transverse orientation is also seen). Florin ring slightly sunken. Stomatal apparatus rounded to elliptical. Subsidiary cells smaller than surrounding epidermal cells, with fine inner striations. Stomatal chamber up to 52 ~m long x 44.2 pm wide. Guard cells partially cutinised, up to 10.3 pm wide. Cutin structured in three layers, the external is lamellated, the medial solid (with no ultrastructure) and the inner is granular to spongy. Pollen cones attached laterally to third order twigs, elongated-cylindrical, up to 18 mm long x 3,5 mm wide. Microsporophylls compact, helically disposed on a central axis, expanded and distally curved, overlapping adjacent sporophylls. Pollen sacs subspherical to oval, up to l mm, bearing bisaccate grains of the Podocarpidites type. Pollen with a distal irregular leptoma and pendant sacci, up to 55 ~m long x 38 pm wide. Corpus rugulate proximally. Exine two layered up to 2 ~Lm thick composed of a thin internal lamellated nexine and an outer sexine. Seed cones terminal, usually disposed on third order branches, elongated with thinned base and obtuse apex, up to 5.5 cm long x 1.3 cm wide. Bract-scale complexes normally and helically disposed on a central axis, compact. Bracts with wide base and a slightly deflexed acuminate apex. Each bract bears a partly fused single elongated body near the cone axis (ovuliferous scales ?). Bracts distally cutinised with short stomatal rows on abaxial side;
stomata obliquely oriented, ca. 20 per sq. mm. Epidermal cells on stomatal cuticle isodiametric to elongate, up to 21 x 34 ~m wide. Bract cuticle distally papillate with serrulate margins. Cells more elongated towards cone axis, proximally granulose. Stomatal structure as for vegetative leaves. Cuticle of leaves and bracts with a layered ultrastructure; external layer with thin compact lamellae, median layer with few more spaced lamellae, otherwise solid and internally with a granular to spongy layer (due to decay ?). The median layer is the thickest cuticular component. Holotype: BA PB 11311 (twigs with pollen cone). Paratypes: BA PB 11335 (pollen cone with twig), 11336 (pollen cone with twig), 11340 (seed cone with twig), 11332 and 11341 (seed cone with twig). Other material studied: BTO horizon, BA PB 11313, 11330, 11337, 11338 (pollen cones), BA PB 11325, 11330, 11333 (seed cones) and BA PB Pm 16-18, 27, 28, 36 38. BTA horizon, BA PB 11339, 11342, 11344-11349, 11368-11373 (seed cones) and BA PB Pm 31-35, 39-45. Sterile twigs (Brachyphyllum tigrense Traverso), BTO horizon, BA PB 11312, 1131511322, 11326-11329. BTA horizon, BA PB 11343. BA PB Pm in BTO and BTA horizons, 1-15, 19-26. Locality: Estancia Bajo Tigre, Santa Cruz province, Argentina. Horizon: Baquer5 Formation, lower member, BTO and BTA fossiliferous levels. Age: Early Cretaceous (latest Barremian to earliest Aptian). Derivatio nominis: Squama = scale and strobus=cone-like, to signify that scale-like leafy twigs bear cones. The specific epithet, tigrensis refers to the locality Bajo Tigre.
Comparisons Three podocarps are known for the Baquer6 Formation (Archangelsky, 1966), viz. Trisacocladus tigrensis, Apterocladus lanceolatus and Podocarpus dubius. Trisacocladus differs in having long leaves, pollen with three air sacci
121
PLATE VI
40 46. 40. 41. 42. 43. 44. 45 46.
Squamastrobus tigrensis gen. n. B r a c t - s c a l e cuticle. Apex of t h e scale s h o w i n g e n l o n g a t e d cells a n d s e r r u l a t e m a r g i n . P A PB P m 32. x 40. S e c t i o n t h r o u g h t h e c u t i c l e s h o w i n g p e r i c l i n a l wall a n d a n t i c l i n a l flanges. T E M x 3000. A detail of t h e e x t e r n a l p a r t of t h e p e r i c l i n a l wall c u t i c l e s h o w i n g a t h i n l a m e l l a t e d b a n d (arrow). T E M x 100,000. Papillae. BA PB P m 34. x 400. D i f f e r e n t pollen g r a i n s t h a t a d h e r e to t h e cuticle. BA P B P m 33. x 400. S t o m a t a i n d i s t i n c t l y o r i e n t e d a n d e p i d e r m a l cells, m o r e e l o n g a t e d t o w a r d s t h e m a r g i n (fig.46). BA P B P m 32, 34, respectively, x 400.
122
(Trisaccites type) and a smaller seed cone with a thick central axis bearing orthotropous ovules. Apterocladus differs in having long leaves and pollen with three rudimentary air sacci (CaUialasporites type). Podocarpus dubius is known with only sterile twigs that differ from Squamastrobus in their long linear shape and cuticular structure. Several other genera with fertile remains have been described in Gondwana. The Jurassic strata of the Rajmahal Hills yielded petrified remains of vegetative and reproductive structures. Nipanioruha Rao (as described by Rao, 1947, 1949, emended by Vishnu-Mittre, 1959 and redescribed by Suthar and Sharma, 1987) has long and bilateral leaves; the pollen cones differ in having pollen with three sacci while seed cones are smaller, although having a similar compact nature and helical arrangement of the ovuliferous complexes; bracts, however, have a strong keel, not observed in Squamastrobus. Nipaniostrobus Rao (as described by Rao, 1943, Vishnu-Mittre, 1959 and Suthar and Sharma, 1987) has shoots with short linear leaves; the seed cones bear compact and differentiated bract-scale complexes helically disposed on a central axis; ovules have a curved micropyle and a short epimatium at the base. These cones are much smaller than in Squamastrobus. Mehtaia Vishnu-Mittre (as described by Vishnu-Mittre, 1959 and Suthar and Sharma, 1987) has shoots with short overlapping and spreading scale-like leaves and much smaller seed cones (the longest, 10 mm against 55 mm in Squamastrobus); the cones have loose to compact short bract-scale complexes disposed on a thick, fleshy axis, each bearing a large erect ovule. There is no evidence of sterile tissue related to the ovules as to suggest an epimatium or a scale. Sitholeya Vishnu-Mittre (1959) has short scale-like overlapping leaves and terminal single-seeded strobili with an inverted seed, much like modern Dacrydium and Podocarpus. Townrow (1967a) described Rissikia, a Triassic podocarp from Africa and Australia. It differs in possessing long bilateral leaves, rounded shape of the pollen cones t h a t pro-
duced bisaccate-striate pollen and thin spikelike female structures with trifid bracts. Mataia is another podocarp described by Townrow (op. cit.) from Jurassic strata of Australia and New Zealand. It also has long bifacial leaves and spike-like female structures composed of bracts and ovuliferous scales (each scale with two small inverted ovules). Townrow (1967a) described Nothodacrium from Jurassic strata of Antarctica; it differs from Squamastrobus in the shape of leaves and the laterally placed female cone that has free bracts and seed-scale complexes; associated male cones probably produced three winged pollen (Callialasporites type). Among living members of the Podocarpaceae, Squamastrobus shares the scale-like leaf type with Dacrydium, some Podocarpus species, Microcachrys and Microstrobos. Only the first two genera are now living in Argentina. The cuticular structure is also similar to some of the living representatives that have scalelike leaves. Serrulate margins are similar to those found in Microstrobos hookeriana (Florin, 1931, fig.68e). However in all living genera stomata tend to be longitudinally oriented and forming files. There are some exceptions like Dacrydium colensoi Hooker or Podocarpus ustus Brongniart et Grisebach, where stomata form ill-defined rows and may be indistinctly oriented. Vegetative parts of Podocarpus parlatorei Pilger, a species living in northern Argentina (del Fueyo, 1988) show a leaf hypodermis composed of fibers, not cutinised as they are in Squamastrobus. Stomata are similarly distributed in files though longitudinally oriented. The Florin ring is common to both living and fossil forms but the guard cells are poorly preserved in Squamastrobus. Epidermal cell walls of the living form are composed of an outer uniform layer (cuticle proper plus cutinised layer in the sense of Lyshede, 1982) and an inner laminated cellulosic layer. In Squamastrobus the epidermal cell walls are externally laminated, followed by a poorly laminated interface area and a solid nonlaminated median layer becoming granular towards the base. This ultrastructure is consistent with the
123 layering found in other fossil cuticles (Ticoa harrisii, Archangelsky et al., 1986). Squamastrobus pollen cones, as in most species of the family, have pollen with two sacci. Exceptions are Microcachrys, Microstrobos and Dacrycarpus that have pollen with three sacci. Saxegothaea has grains with no sacci and is referred to a different family by some authors, the Saxegothaeaceae (Gaussen, 1973; Woltz, 1985). The sporoderm organization in Squamastrobus is similar to extant members of the family. Pocknall (1981a, b) provided an account on the general morphology and the organization at an ultrastructural level for some members of Dacrydium, Dacrycarpus, Phyllocladus and Podocarpus from New Zealand. The ~region of weakness" found at the proximal roots of the sacci (Pocknall, op. cit.) is also known for Trisacocladus Archangelsky (Gamerro, 1965; Baldoni and Taylor, 1982). This sporoderm thinning may be related to a harmomegathical function (Baldoni and Taylor, op. cit.). The sporoderm in Squamastrobus has a two layered sexine; the external or ectosexine may be continuous (as in several extant members and Squamastrobus) or perforate-foveolate (Trisacocladus); the inner layer or endosexine is alveolate to collumelate, much in the same way as in many living podocarps (Pocknall, 1981a, b). Our collumelate component shows affinities with extant members rather than with the fossil Trisacocladus. This organization suggests a collumelate layer with a continuous and folded tectum-like layer having the same electron density. Collumelae (or rods as found in Trisacocladus) have an irregular distribution, leaving spaces of different sizes that produce an alveolate organization, comparable with the endosexine of cycad pollen (Baldoni and Taylor, op. cit.). The innermost part of the sexine is closely related to the nexine layer, showing interdigitaded components (Plate IV, 30, 31). The electron darker units appear as granules, merged with the electron lighter lamellate units around the whole corpus (including the apertural area). This ectosexine foot-layer is a common feature in extant and fossil podocarps so far analyzed.
The nexine in living and fossil podocarps is lamellated. Its preservation in extinct taxa varies according to the state of fossilization; in Squamastrobus only small areas show this organization (Plate IV, 30) while in Trisacocladus it has not been seen. Both genera belong to the podocarps and show minor structural differences suggesting that during the early Cretaceous there were at least two types of organization in some sporopollenin components, specially in the sexine layer. Most living Podocarpaceae have '~reduced" seed cones with only one or two ovules (~strobili" in Florin's terminology). However, compact cone structures with several ovuliferous complexes are known in Saxegothaea, Microstrobos and Microcachrys where seedscale units are axillary disposed on bracts. Phyllocladus has also compact seed cones but their axillary fertile complexes are much reduced. Female spike-like structures are known in few species, viz. Dacrydium franklinii Hooker, Podocarpus spicatus R. Brown and P. andinus Poepp. (Florin, 1958). Discussion
Squamastrobus may be placed in the family Podocarpaceae considering the similarities that exist with extant and fossil members of the group. The new genus supports the Gondwana affinity of the family during the Cretaceous when it was strongly diversified. Other coeval conifers, like the Araucariaceae, are different in that most characters remained the same since early Mesozoic times. Isolated scales (or bract-scale complexes) of Squamastrobus have not been found, although seed cones are common components in the plant bed. This may suggest that either the cones were all immature or the ovuliferous scales remained attached to the cone axis after maturation. The second hypothesis is probably more consistent, because isolated scales belonging to other seed cones (Tomaxellia, Araucarites) are abundant in these strata. Bract and scale were probably fused in one unit, partly cutinised in the distal portion of each compo-
124 nent, with stomata of the same kind as those found in vegetative leaves. Jurassic and Cretaceous podocarps had diversified female cones, consisting of fertile and sterile components with either compact
(Nipanioruha, Nipaniostrobus, Squamastrobus) or lax disposition (Mehtaia, Rissikia, Mataia, Trisacocladus). Probably, the cone habit predominated at t h a t time. However, single-seeded cones (Sitholeya), the commonest condition among extant members of the family, are also known in the Mesozoic. Phylogenetic links probably exist between some extant podocarps (Microcachrys, Phaerosphaera) and the Mesozoic cone-bearing taxa. Some living members with lax spike-like cones (i.e. Podocarpus spicatus) and similar Mesozoic genera (Mehtaia, Rissikia) may be phylogenetically related as well. However, they can also represent merely a state of reduction to a single-ovule stage. The epimatium in extant podocarps is a supplementary protective structure. In the fossil Nipaniostrobus, Mataia and Nipanioruha the folded overtips of the ovuliferous scales may represent the forerunner of the epimatium (Miller, 1977). The structure was also related to an ovule recurvation process (Vishnu-Mittre, 1959) or a modification of a portion of the seedscale complex (Suthar and Sharma, 1987). Squamastrobus shares most characters with several genera of the family but individually differs from all. The long history, wide geographic distribution caused by lands that drifted apart during the Mesozoic, and the presence of monotypic genera (or genera represented by few geographically widely separated species), clearly indicate that the Podocarpaceae is a heterogeneous family that was affected by abrupt palaeoclimatic and palaeoenvironmental changes. These stresses were and are responsible for the development of different lineages within the family resulting in a particular distribution of its extant members. The wide variation in chromosome number (from 9 to 19) also suggests the heterogeneity of the family (Hair and Beusenberg, 1958). Miller (1982) using two numerical analyses
found that the Pinaceae, Araucariaceae and Podocarpaceae sort out closely, suggesting some kind of relationship. However, this sorting was not consistent enough to recognize particular ancestors among the known Voltziaceae. Most Triassic and Jurassic genera from Gondwana were not considered by this author at that time. To trace the origin of Mesozoic podocarps, Townrow (1967a) suggested that Buriadia and Paranocladus (both Permian) were possible candidates though no fructifications were known at that time. More recently, seedbearing units were found in different areas of Gondwana and related to both palaeozoic genera. Two families are known, viz. the Buriadiaceae (Pant, 1982) and Ferugliocladaceae (Archangelsky and C6neo, 1987). The fertile shoots of Genoites, a Permian Buriadiaceae from Patagonia (Cfineo, 1986), are lax spike-like structures bearing ovules axillary on sterile appendages, not differentiated from normal leaves; these ovuliferous structures tend to have a distal disposition on the fertile branches. Some Mesozoic podocarps, specially those with lax cones may well have been in the same lineage with the Buriadiaceae with the subtending leaves transformed into bracts and a more compact structure of the bract-ovule complexes. The Ferugliocladaceae had compact cones of a similar size and shape to Squamastrobus. They differ in the separation of bract and ovuliferous scales. In Ferugliocladus, the ovuliferous scale is an elaborate structure, adapted for dispersal (Archangelsky and C6neo, 1987). The genus Ugartecladus had simple ovules (or ovuliferous scales), free from the bracts. Such cone organization may have developed into a Nipaniostrobus or Squamastrobus type by ovule recurvation and bractscale partial fusion. This would suggest another lineage leading to the Podocarpaceae. At this point of our knowledge it seems that Townrow's original suggestion may have some firm ground. It is still premature to speculate further until we know more about Permian, and specially Triassic podocarps in order to
125
define more precise boundaries between the three families that have been discussed. Nevertheless, the Buriadiaceae and the Ferugliocladaceae offer a good ancestral stock of exclusively Gondwanan distribution from which some Mesozoic conifers may have evolved like the Podocarpaceae and/or the Araucariaceae (Archangelsky, 1985). Not less important is the palaeogeographic distribution of the Permian genera Genoites, Ferugliocladus and Ugartecladus, t h a t are found near the place from where Squamastrobus has been recovered (southern Patagonia).
Acknowledgements We are grateful to the Consejo Nacional de Investigaciones Cientificas y T~cnicas (CONICET) and International Cooperative Science Program of the National Science Foundation (BSR-8313786 to T.N. Taylor) for support of this project. We wish to t h a n k Liliana Seoane for technical assistance, Miguel Archangelsky for photographic work and Isabel Farlas for useful suggestions with TEM work. We are most grateful to CEVAN-CONICET for the use of the TEM.
References Archangelsky, S., 1966. New Gymnosperms from the Tic6 Flora, Santa Cruz province, Argentina. Bull. Br. Mus. Nat. Hist. Geol., 13:259 295. Archangelsky, S., 1967. Estudio de la Formaci6n BaquerS, Cretficico inferior de S a n t a Cruz, Argentina. Rev. Mus. La Plata, Secc., Paleontol., 5:63 171. Archangelsky, S., 1985. Aspectos evolutivos de las conlferas gondwfinieas del Paleozoico. Bull. Sect. Sci., 8: 115 124. Archangelsky, S. and Cdneo, R., 1987. Ferugliocladaceae, a new Conifer family from the Permian of Gondwana. Rev. Palaeobot. Palynol., 51: 3-30. Archangelsky, S. and del Fueyo, G., 1987. Sobre una Podocarpficea f~rtil del Cretficico inferior de la provincia S a n t a Cruz, Repdblica Argentina. Act. VII Simp. Argent. Paleobot. Palinol., Buenos Aires, pp.85 88. Archangelsky, S., Baldoni, A., Gamerro, J.C. and Seiler, J., 1984. Palinologia estratigrfifica del Cretficico de Argentina austral. III. Distribucibn de las especies y conclusiones. Ameghiniana, 21(1): 15 33. Archangelsky, S., Taylor, T.N. and Kurmann, M.H., 1986. U l t r a s t r u c t u r a l studies of fossil plant cuticles: Ticoa
harrisii from the early Cretaceous of Argentina. Bot. J. Linn. Soc., 92:101 116. Baldoni, A.M. and Taylor, T.N., 1982. The ultrastructure of Trisaccites pollen from the Cretaceous of southern Argentina. Rev. Palaeobot. Palynol., 38:23 33. Cfineo, R., 1986. Ejemplares f~rtiles de Genoites patagonica Feruglio (Buriadiaceae, Coniferopsida ?) del P~rmico de Chubut, Repdblica Argentina. Ameghiniana, 22: 269-279. del Fueyo, G., 1988. Anatomia y ontogenia foliar de Podocarpus parlatorei (Podocarpaceae). Bol. Soc. Arg. Bot. 353 367. Florin, R., 1931. U n t e r s u c h u n g e n zur stammesgeschichte der coniferales. K. Sven. Vetenskapakad. Handl., 10: 3 588. Florin, R., 1940. The Tertiary Fossil Conifers of South Chile and their phytogeographical significance. Kungl. Sv. Vetenskapakad. Handl., 19(2): 1-107. Florin, R., 1958. Notes on the systematics of the Podocarpaceae. Acta Horti Bergiani, 17(11): 403 411. Gamerro, J.C., 1965. Morfologia del polen de la conifera Trisacocladus tigrensis Archang. de la Formaci6n Baquer6, Provincia de S a n t a Cruz, Ameghiniana, 4: 31-38. Gaussen, H., 1973. Les Gymnospermes actuelles et fossiles. Trav. Lab. For. Toulouse, 2(1): 1 43. Hair, J.B. and Beusenberg, E . J , 1958. Chromosomal evolution in the Podocarpaceae. Nature, 181(4623): 1584 1586. Lyshede, O.B., 1982. Structure of the outer epidermal wall in xerophytes. In: The Plant Cuticle, D.F. Cutler, K.L. Alvin and C.E. Price (Editors). Linn. Soc. London, Sympos. Ser., 10: 87-98. Miller, C.N., 1977. Mesozoic Conifers. Bot. Rev., 43(2): 217 280. Miller, C.N., 1982. Current status of Paleozoic and Mesozoic Conifers. Rev. Palaeobot. Palynol., 37: 99- 114. Pant, D.D., 1982. Some Lower Gondwana Gymnosperms and their relationships. Rev. Palaeobot. Palynol., 37: 55 70. Pocknall, D.T., 1981a. Pollen morphology of the New Zealand species of Dacrydium Solander, Podocarpus L'Heritier and Dacrycarpus Endlicher (Podocarpaceae). N.Z.J. Bot., 14:67 95. Pocknall, D.T., 1981b. Pollen morphology of Phyllocladus L.C. et A. Rich. N.Z.J. Bot., 19:259 266. Rao, A.R., 1943. Nipaniostrobus, a new genus of Dacrydium-like seed-bearing cones and other silicified plants from the Rajmahal Series. Proc. Nat. Acad. Sci., India, 13(2): 113 132. Rao, A.R., 1947. Nipanioruha granthia gen. et sp. nov.; a new petrified coniferous shoot from the Rajmahal Hills, Bihar. In: M.O.P. Iyengar commem, volume, Indian Bot. Soc., pp.389 397. Rao, A.R., 1949. The megastrobilus of Nipanioruha granthia Rao, A.R. Curr. Sci., India, 18:447 448. Suthar, O.P. and Sharma, B.D., 1987. Petrified fructifications of conifers from the Jurassic of Rajmahal Hills, India. Geophytology, 16(2): 159 165. Townrow, J.A., 1967a. On Rissikia and Mataia podocarpaceous conifers from the lower Mesozoic of southern lands. Pap. Proc. R. Soc. Tasmania, 101:103 136.
126 Townrow, J.A., 1967b. On a conifer from the Jurassic of East Antarctica. Pap. Proc. R. Soc. Tasmania, 101: 137-147. Traverso, N.E., 1966. Brachyphyllum tigrense n u e v a con~fera de la FormaciSn BaquerS, Cret~cico de S a n t a Cruz. Ameghiniana, 4: 189-194.
Vishnu.Mittre, 1959. Studies on the fossil flora of Nipania (Rajmahal Series), Bihar. Coniferales. Palaeobotanist, 6(2): 82-112. Woltz, P., 1985. Place des Gymnospermes end~miques des Andes M~ridionales dans la v~g~tation du Chili. Lazaroa, 8: 293-314.