Cuticular study of Bennettitales from the Springhill Formation, Lower Cretaceous of Patagonia, Argentina

Cretaceous Research (2001) 22, 461–479 doi:10.1006/cres.2001.0266, available online at http://www.idealibrary.com on

Cuticular study of Bennettitales from the Springhill Formation, Lower Cretaceous of Patagonia, Argentina Liliana Villar de Seoane CONICET, Divisio´n Paleobota´nica, Museo Argentino de Ciencias Naturales ‘‘B. Rivadavia’’, Av. A. Gallardo 470, (1405) Buenos Aires, Argentina Revised manuscript accepted 29 May 2001

Cuticles of leaves and scale-leaves belonging to the order Bennettitales are discussed using light microscopy (LM) and scanning and transmission electron microscopy (SEM and TEM). The cuticles occur in the Springhill Formation (Lower Cretaceous) of Santa Cruz Province, Argentina. The fossil group is represented by seven species of which one is new and three other species have their diagnosis emended by ultrastructural analysis. The species studied are Otozamites patagonicus sp. nov., Otozamites archangelskyi Baldoni & Taylor, 1983, Pterophyllum trichomatosum Archangelsky & Baldoni, 1972, Ptilophyllum valvatum Villar de Seoane, 1995, Ptilophyllum antarcticum (Halle) Archangelsky & Baldoni, 1972, Cycadolepis coriacea Mene´ndez, 1966 and Cycadolepis involuta Mene´ndez, 1966. The leaves and scale-leaves show xeromorphic characters such as sculptured surfaces, sunken stomata and a thick external wall in the epidermis. The xeromorphic characters could indicate high temperatures, low humidity and arid soils. These palaeoenvironmental conditions may have been associated with volcanic activity. The presence of carbonized specimens also suggests the development of forest fires produced by dry seasonal conditions or regional volcanic activity.  2001 Academic Press K W: Bennettitales; cuticles; Lower Cretaceous; Springhill Formation; Santa Cruz Province; Argentina.

1. Introduction In this report, the cuticles of bennettitalean leaves and scale-leaves found in the Springhill Formation are described using light microscopy (LM) and scanning and transmission electron microscopy (SEM and TEM). This is the first time that TEM has been used to analyse bennettitalean cuticles from the Springhill Formation. The fossil group is represented by seven species. One of these is a new species (Otozamites patagonicus sp. nov.), and three other species (Pterophyllum trichomatosum Archangelsky & Baldoni, 1972, Ptilophyllum valvatum Villar de Seoane, 1995 and Cycadolepis coriacea Mene´ndez, 1966) have their diagnosis emended on the basis of ultrastructural studies. The cuticular features of Otozamites archangelskyi Baldoni & Taylor, 1983, Ptilophyllum antarcticum (Halle) Archangelsky & Baldoni, 1972 and Cycadolepis involuta Mene´ndez, 1966 are also described. The Bennettitales were an important group of plants in Mesozoic floras worldwide; they were 0195–6671/01/040461+19 $35.00/0

particularly well-represented in Argentinean Jurassic and Cretaceous floras. Their global stratigraphic range extends from the Triassic to Upper Cretaceous (Watson & Sincock, 1992) and their anatomy is mainly characterized by having a paracytic stomatal apparatus. In the last four decades, Delevoryas (1963, 1965), Harris (1969, 1973, 1974), Crepet (1972, 1974), Taylor (1973), Sharma (1974), Krassilov (1978), Doyle & Donoghue (1986), Crane (1986, 1988), Sincock & Watson (1988), Watson & Sincock (1992), and Boyd (1998) have presented taxonomic, morphological and anatomical studies of these plants from different countries. In Argentina, Halle (1913), Frenguelli (1935), Mene´ndez (1957, 1966), Archangelsky & Baldoni (1972), Baldoni (1974, 1977), and Villar de Seoane (1999) have worked on bennettitalean floras from several localities such as Bahı´a Esperanza (Upper Jurassic–Lower Cretaceous of the Antarctic Peninsula), Lago San Martı´n (Upper Jurassic of Santa Cruz Province), Bajo de los Baguales (Middle Jurassic  2001 Academic Press

462

L. Villar de Seoane

Figure 1. a, map showing the location of the Estancia El Salitral (Springhill Formation), Santa Cruz Province, Argentina. b, detail (adapted of Cortin˜ as & Arbe, 1981).

of Neuque´ n Province), Baquero´ Group and Paso Roballos (Lower Cretaceous of Santa Cruz Province), describing new genera and species of leaves, female cones and scale-leaves. The Springhill Formation has an important Mesozoic flora composed of plants belonging to the orders Filicales, Cycadales, Bennettitales and Coniferales. In 1976, Archangelsky undertook the first cuticular study, using light microscopy, of plants found in the formation where the remains of Bennettitales are dominant. Later, Baldoni (1979), Baldoni & Taylor (1983), and Villar de Seoane (1995) studied different leaves, scale-leaves and ovuliferous scales from the same formation.

2. Material and methods The Springhill Formation, which crops out in Patagonia (Santa Cruz Province in Argentina and Magallanes Province in Chile), Tierra del Fuego and the Argentinean Sea, has an average thickness of 30–40 m, with a maximum of 130–150 m. The formation includes a lower section, mainly continental with plant fossils, and an upper marine section with invertebrates and dinoflagellates. Regionally, it consists of at least three backstepping but individually

prograding sandstone intervals, which may or may not be in contact with each other. Locally, the basal part or even the entire formation may be missing. The Springhill Formation has yielded fossil remains in different wells and outcrops (Riccardi, 1988). The fossil material described here occurs in the Estancia El Salitral, Río Chico Department, approximately 100 km south-east of Perito Moreno, along the road where the provincial routes 1209 and 2105 are joined. The site is located in the north-west of Santa Cruz Province, to the south of Buenos Aires Lake and the north of Posadas Lake, within part of the Andean chain, between parallels 46–48S and the meridians 72–70 (Figure 1). These outcrops have been described by Cortin˜ as & Arbe (1981). Previous geological studies of the Springhill Formation have suggested an Early Berriasian–Late Valanginian age, but Ottone & Aguirre-Urreta (2000) have recently suggested an Early Hauterivian–Early Barremian age for the Estancia El Salitral outcrops through their invertebrate and palynological analyses. The fossils studied are mainly represented by carbonized foliage leaves and scale-leaves. Their cuticles were prepared for light microscopy and scanning and transmission electron microscopy. The material was cleared with dilute sodium hypochlorite.

Cuticular study of Bennettitales from Argentina

The preparations were mounted in glycerine jelly for observation by light microscopy, or directly on circular stubs and coated with gold-palladium for SEM. For TEM, cuticle fragments were embedded in Spurr low viscosity resin (Spurr, 1969). Sections were cut with a diamond knife on a SORVAL manual ultramicrotome, and mounted in single hole grids coated with Formvar, stained with KMnO4 (5–10 min) and Uranyl acetate (30 s). The type specimens are deposited in the Palaeobotanical Collection of the Buenos Aires Natural History Museum (BA Pb). The terminology of Holloway (1982) and Lyshede (1978, 1982) was used for the ultrastructural analysis.

3. Systematic palaeontology Order Bennettitales Genus Otozamites Braun, 1843 Type species. Zamites brevifolius Braun, in Mu¨ nster, 1843 Otozamites archangelskyi Baldoni & Taylor, 1983 Figure 2 Material studied. BA Pb 11661; BA Pb Pm 399; and BA Pb MEB 76. Description. The leaves are imparipinnate, up to 8 cm long and 2 cm wide. The pinnae are alternate, elongated and distally falcate, up to 1.0 cm long and 0.4 cm wide. Pinnae bases are imbricate along the adaxial surface of the rachis and their insertion angle is 40–45. The pinnae have entire margins and acute apices. The veins radiate asymmetrically from the base, are sub-parallel and dichotomous (Figure 2a). The adaxial epidermis has rectangular to isodiametric cells 45–78
m long and 34–59
m wide, with very sinuous walls 2.5–3.0
m wide. These sinuosities are 14.0
m in height and have a density of 10–15 through each 100
m (Figure 2c). The sinuosities of the anticlinal walls are higher than the periclinal walls. The cells are irregularly disposed and their surface is granulate (Figure 2c). The abaxial epidermis has rectangular to isodiametric cells 39–70
m long and 25–42
m wide, and their walls are less sinuous and thicker (4–5
m) than the adaxial walls. The cells form ill-defined rows and their surface is ornamented by simple papillae and globose hairs (Figure 2b).

463

The simple papillae are 12.0
m in diameter and 15.0
m in height. They are hollow and have a central position in the cell (Figure 2b). The globose hairs are sparse and their bases occupy all the cellular surface. On the internal surface of both epidermises, there are circular bodies (Figure 2d) which are probably glandular trichomes. The leaves are hypostomatic with the stomata regularly disposed between the veins. The stomatal apparatuses are 56–76
m long and 48–67
m wide (Figure 2e); each subsidiary cell has two simple papillae. Each papilla is near the aperture closing it with the papilla of the opposite cell. The guard cells are sunken and have a strong dorsal thickening and thin polar appendages (Figure 2e). Comparison. The specimens are morphologically and anatomically similar to the material described by Baldoni & Taylor (1983) from the same formation, varying only in the length of the epidermal cells and stomata. Otozamites patagonicus sp. nov. Figures 3, 4a–c Derivation of name. The species name refers to the geographic region of Patagonia in Argentina. Holotype. BA Pb 11660; BA Pb Pm 394, 395, 396, 397, 398; BA Pb MEB 75; and BA Pb MET 171. Type locality. Estancia El Salitral, Santa Cruz Province, Argentina. Stratigraphic horizon. Springhill Formation, Lower Cretaceous. Diagnosis. Leaves imparipinnate. Pinnae alternate, elongated, up to 1.2 cm long and 0.4 cm wide, with entire margins and rounded apex. Veins radiate asymmetrically from region of attachment. Adaxial epidermis smooth with rectangular to isodiametric cells 69
m long and 39
m wide. Abaxial epidermis densely ornamented with compound and simple papillae. Epidermal cells 74
m long and 37
m wide, rectangular to isodiametric with very sinuous walls. Leaves hypostomatic. Paracytic stomatal apparatus up to 70
m long and 55
m wide; each subsidiary cell with two marginal papillae. Ultrastructurally, cuticular membrane formed by an upper layer 0.50
m thick; a middle layer 4.50
m thick; and a lower layer 0.25
m thick. Description. The fossil leaves are 6 cm long and 2.3 cm wide in the middle zone, decreasing to the apex (Figure 3a). The pinnae are imbricated on the adaxial surface of the rachis and their insertion angle is

464

L. Villar de Seoane

Figure 2. Otozamites archangelskyi Baldoni & Taylor 1983. a, general view of specimen, BA Pb 11661. b, detail of the abaxial epidermis with papillae (arrows), BA Pb Pm 399. c, detail of the adaxial epidermal cells, BA Pb MEB 76. d, detail of a circular body, BA Pb MEB 76. e, internal view of the guard cells and subsidiary cells, BA Pb MEB 76. Scale bar represents 0.5 cm in a, 10
m in b–e.

Figure 3. Otozamites patagonicus sp. nov. a, general view of the holotype, BA Pb 11660. b, detail of the abaxial epidermal cells, BA Pb MEB 75. c, detail of a compound papilla, BA Pb Pm 394. d, detail of simple papillae, BA Pb MEB 75. e, external view of the stoma with papillate subsidiary cells, BA Pb MEB 75. f, internal view of the stoma, BA Pb MEB 75. Scale bar represents 0.5 cm in a, 10
m in b–f.

466

L. Villar de Seoane

60–80. The veins are sub-parallel (Figure 3a). The adaxial epidermis has cells irregularly disposed (Figure 3b), with highly sinuous walls. These sinuosities are 15.0
m tall and have a density of 10–15 per 100
m. The abaxial epidermal cells have walls that are more sinuous than the adaxial cells, form ill-defined rows and have two types of papillae. The compound papillae are 29.0
m in diameter and the walls are very thick (17.0
m wide). They are formed by 6–8 papillae (Figure 3c), which are shorter and less hollow than the simple papillae. The latter are 17.0
m in diameter with walls 2.8
m wide (Figure 3d). They are hollow and have a central position on the epidermal cell. The stomata are regularly disposed between the veins of the abaxial epidermis. Each subsidiary cell has two simple papillae, each of which is at the polar margin of the cell, overhanging the stomatal aperture (Figure 3e). The guard cells are sunken and have a strong dorsal thickening and thin polar appendages (Figure 3f). Ultrastructurally, the external wall of the epidermis is formed of three layers (Figure 4a). The upper layer is granulate, dark and thin, with granules densely distributed (Figure 4c); the middle layer is light and very thick. The structure is amorphous and shows a transitional zone with the upper layer, where the granules are more dispersed (Figure 4c). The lower layer is dark and thinner than the upper layer (Figure 4a). The granulate layers do not have regular structure apart from their granulate texture. The TEM observations made at high magnification (80 k) have not demonstrated the presence of any net,

lamellae or microchannels, and shown only granules of different electronic density, uniformly disposed (Figure 4c). In the section of one stoma, differences between the external wall of the subsidiary cell and its papillae are observed (Figure 4a). The subsidiary cell wall shows the three layers described. The wall of the papillae also has three layers, but their structures are different (Figure 4b). The upper layer is slightly reticulate, up to 0.75
m thick. The fine channels are irregularly and obliquely disposed to the surface (Figure 4b). The middle layer is reticulate, up to 1.3
m thick. It is very similar to the upper layer, but the net is formed by light channels, showing charcoal fragments (black points) within it (Figure 4b). The lower layer is reticulate-alveolate, up to 2.0
m thick. In the basal region of the papilla, this layer is reticulate and has dark and thin channels disposed parallel to the surface. These channels are interlaced and form a strong net with small charcoal fragments in it (Figure 4b). By contrast, the apical region of the papilla has an alveolate lower layer with irregular and elongate lacunae forming a net with thick and translucent channels disposed parallel to the surface, keeping thin channels between them (Figure 4a). The wall of the guard cells is very thin but the three layers described are clearly preserved (Figure 4a).

Species

Ep. cells

Stomata

39–78 25–59
m

56–76 48–67
m

Locality

Pinna: Size

O. archangelskyi O. grandis

Springhill

10.4 cm

acute

Baquero´

62 cm

obtuse

20 per cm

O. linearis O. ornatus

Antarctica Baquero´

obtuse obtuse

30 per cm

O. patagonicus O. parviauriculata O. parvus

Springhill

O. sanctaecrucis O. waltonii

Springhill

1.2 0.3 cm 1.2 0.4 cm 2.3 0.7 cm 1.2 0.2 cm 1.7 cm

Baquero´

10.4 cm

Baquero´ Springhill

Apex

Veins

rounded obtuse

35 per cm

acute

25–30 per cm

Comparison. Otozamites patagonicus sp. nov. has been compared with the other species of the same genus from Springhill Formation, Baquero´ Group and Antarctic Peninsula. The differences are summarized in the following table:

44–117 39–57
m 56–84 31–59
m 65–80 35–43
m 59–70 28–34
m

obtuse acute

20–25 per cm

40–86 30–65
m

Papillae simple

Hairs globose

Granules X

simple & compound

—

—

7834
m

simple

—

X

53–81 45–62
m 4033
m

X

—

two types

—

X

—

6050
m

simple & compound simple & compound simple & compound simple

gemmate

—

4515
m

simple

X

—

5240
m

Cuticular study of Bennettitales from Argentina

467

Figure 4. a–c, Otozamites patagonicus sp. nov. a, transverse (TS) section of the external wall of a stoma with a longitudinal section of the papillae, BA Pb MET 171. b, detail of the TS section of the papilla wall, BA Pb MET 171. c, detail of the granular upper layer, BA Pb MET 171. d, e, Pterophyllum trichomatosum (Archangelsky & Baldoni) emend. d, transverse (TS) section of the external wall of the epidermis and the papilla, BA Pb MET 169. e, detail of the granules of the upper layer, BA Pb MET 169. P, papilla; GC, guard cells; UL, upper layer; ML, middle layer; LL, lower layer. Scale bar represents 5
m in a and d, 0.5
m in b, c and e.

468

L. Villar de Seoane

Genus Pterophyllum Brongniart, 1828 Type species. Pterophyllum longifolium Brongniart, 1828 Pterophyllum trichomatosum Baldoni, 1972 Figures 4d–e, 5a–e

Archangelsky

&

Material studied. BA Pb 11662, 11663; BA Pb Pm 400, 401, 402, 403, 404; BA Pb MEB 73, 74; and BA Pb MET 169. Emended diagnosis. Pinnae alternate, elongated and distally falcate, up to 1.9 cm long and 0.4 cm wide, with entire margins and acute apex. Veins entering parallel from the attachment region with a concentration of four per 1 mm. Adaxial epidermis smooth with rectangular to isodiametric cells 59
m long and 27
m wide. Very sinuous walls. Abaxial epidermis densely ornamented with simple papillae and hairs. Rectangular to isodiametric epidermal cells 65
m long and 28
m wide, also with very sinuous walls. Leaves hypostomatic. Paracytic stomatal apparatus 57
m long and 62
m wide, each subsidiary cell with a marginal papilla. Ultrastructure of external wall of the epidermis consists of an upper layer 0.40
m thick; a middle layer 3.50
m thick; and a lower layer 0.40
m thick. Description. This species is known from fragments of pinnate leaves 5.5 cm long and 3.8 cm wide with a straight, longitudinally striate rachis 0.1 cm wide (Figure 5a). The pinnae are attached close to lateral margins of rachis, arising at an angle of 60. The adaxial epidermal cells are regularly disposed (Figure 5c) and have very sinuous anticlinical walls. The wall sinuosities are 13.0
m high and have a density of 10 per 100
m. The abaxial epidermal cells have walls that are similar to those of the adaxial cells; they form ill-defined rows and their surface bears simple papillae (Figure 5b), 13.0
m in diameter and 17.0
m high. They are hollow and have a central position in the epidermal cell. The hairs are hollow and have a globose apical region and a basal diameter of 25
m at the base. They are less common than the papillae (Figure 5b). The stomata are regularly disposed between the veins of the abaxial epidermis. Each subsidiary cell has one marginal papilla (Figure 5e). The papilla is located near the internal margin of the cell and closes the stomatal aperture with the papilla of the opposite cell (Figure 5e). The guard cells are sunken and have the same anatomical characters as the other species (Figure 5d).

Ultrastructurally, the external wall of the epidermis is seen to consist of three layers (Figure 4d). The upper layer is dark, compact and thin; the middle layer is light, amorphous and very thick; and the lower layer is dark, compact and thin. At high magnification (80 k) the three layers show a granulate structure (Figure 4e). The granules are small and densely distributed. The external wall of the papillae has three layers with the same structural characters as the epidermal wall (Figure 5d). The middle layer of the papilla as in the cellular wall, shows small charcoal fragments within its structure (Figure 5d). The Figure 5d shows the presence of large charcoal fragments on the cuticular surface, especially between the cellular wall and the papillae. These charcoal fragments are partially loosened by the diamond knife during sectioning leaving hollows in the resin. Comparison. The specimens examined are similar to those described by Archangelsky & Baldoni (1972) from the Baquero´ Group; the diagnosis is emended by the ultrastructural information obtained from the new specimens. Pterophyllum sp. (Mene´ ndez, 1966) from the same group, has larger pinnae and smaller papillae. Genus Ptilophyllum Morris, 1840 Type species. Ptilophyllum acutifolium Morris, in Grant, 1840 Ptilophyllum antarcticum (Halle) Archangelsky & Baldoni, 1972 Figure 5f–g Material studied. BA Pb 11665, 11666; BA Pb Pm 408, 409; BA Pb MEB 43. Remarks. This species is not described here because the material is similar to the leaves analysed by Archangelsky (1976), Baldoni (1979), and Villar de Seoane (1995) from the Springhill Formation. It has also been recorded from the Baquero´ Group (Mene´ ndez 1966; Archangelsky & Baldoni 1972). Ptilophyllum valvatum Villar de Seoane 1995 Figures 6, 7a–d Material studied. BA Pb 11664; BA Pb Pm 405, 406, 407; BA Pb MEB 68; and BA Pb MET 170. Emended diagnosis. Pinnate leaves. Pinnae alternate to subalternate, elongated and distally falcate, up to

Figure 5. a–e, Pterophyllum trichomatosum (Archangelsky & Baldoni) emend. a, general view of specimen, BA Pb 11662. b, detail of the abaxial epidermis with papillae and hair (arrow), BA Pb Pm 400. c, detail of the adaxial epidermal cells, BA Pb MEB 73. d, internal view of the stomata, BA Pb MEB 73. e, external view of the stomata with papillate subsidiary cells, BA Pb MEB 73. f, g, Ptilophyllum antarcticum (Halle) Archangelsky & Baldoni 1972. f, general view of specimen, BA Pb 11666. g, detail of the stoma surrounded by papillate subsidiary cells, BA Pb MEB 43. Scale bar represents 0.5 cm in a and f, 20
m in b–e and g.

Figure 6. Ptilophyllum valvatum (Villar de Seoane) emend. a, general view of specimen, BA Pb 11664. b, general view of the adaxial epidermis, BA Pb Pm 405. c, external view of the papillae (arrows) on the abaxial epidermis, BA Pb Pm 405. d, internal view of a hair base (arrow), BA Pb MEB 68. e, outer view of a stoma with papillate subsidiary cells, BA Pb MEB 68. f, inner view of the guard cells and subsidiary cells, BA Pb MEB 68. Scale bar represents 0.5 cm in a, 10
m in d–f, and 20
m in b and c.

Cuticular study of Bennettitales from Argentina

3.3 cm long and 0.4 cm wide, with entire margins. Veins parallel, arising from the broad basal attachment. Adaxial epidermis smooth with rectangular to isodiametric cells 69.0
m long and 32.0
m wide, with strongly sinuous walls. Abaxial epidermis densely covered with compound papillae and hairs. Rectangular to isodiametric epidermal cells 66
m long and 38
m wide, with very sinuous walls. Leaves hypostomatic. Paracytic stomatal apparatus 63
m long and 50
m wide; each subsidiary cell with compound papillae. Ultrastructurally, cuticular membrane formed by an upper layer 1.0
m thick; a middle layer 3.50
m thick; and a lower layer 0.50
m thick. Description. The known fragments of pinnate leaf are about 3.7 cm long and 4.9 cm wide. The pinnae are attached on the adaxial surface of the rachis, arising at an angle of 45–60. The veins have a concentration of 35–40 per cm (Figure 6a). The adaxial epidermal cells are regularly disposed and have sinuous walls. The sinuosities are 8.5
m high and have a density of 15 per 100
m (Figure 6b). The abaxial epidermal cells have walls that are similar to those of the adaxial cells and form ill-defined rows. The abaxial epidermis bears compound papillae and hairs (Figure 6c). The compound papillae are up to 30.6
m in diameter and the walls are 11.3
m wide. They are hollow and are formed by three or four

Species P. antarcticum P. angustus P. ghiense P. hislopi P. longipinnatum P. valvatum

Locality

471

Ultrastructurally, the external wall of the epidermis consists of three granulate layers (Figure 7a, b). The upper layer is dark and thin. It is composed of irregularly disposed granules of varying size (Figure 7c, d). The middle layer is thicker and light (Figure 7c). The granules are very small and homogeneously distributed. The lower layer is the thinnest of the three and dark (Figure 7c). The granules are irregularly disposed and have a density similar to that of the upper layer. Observations at high magnification (125 k) have demonstrated that the layers are not lamellate, but comprise granules of different size and density (Figure 7d). The lower layer of the anticlinal wall is strongly developed (Figure 7b). The layers of the external wall of the papillae have the same distribution and granulate structure as the epidermal wall (Figure 7a). Comparison. The material is similar to the leaves I have described previously (Villar de Seoane, 1995) from this formation; the diagnosis is emended by ultrastructural data obtained from the new material. Ptilophyllum valvatum has been compared with other species of the same genus found in the Springhill Formation, Baquero´ Group, Bajo de los Baguales and Paso Roballos. The differences are indicated in the following table:

Pinna: Size

Apex

Veins

Ep. cells

Stomata

Papillae

Hairs

Baquero´ Springhill Springhill

4.50.4 cm

rounded

40–50 per cm

4530
m

acute

Paso Roballos Baquero´ Bajo de los Baguales Baquero´ Springhill

4.50.6 cm

acute

75–81 37–44
m

5027
m

1.70.4 cm

acute

simple & compound simple & compound simple & compound simple

X

30.4 cm

52–75 23–35
m 4015
m

30.3 cm 3.30.4 cm

rounded acute

41–60 30–48
m 40–50 per cm 35–40 per cm

papillae (Figure 6c). The hairs are hollow, 25.5
m in height and with a basal diameter of 20.3
m (Figure 6d). The stomata are regularly disposed between the veins of the abaxial epidermis. Each subsidiary cell has compound papillae closing the stoma (Figure 6e). The guard cells are sunken and strongly thickened dorsally (Figure 6f).

50–90 27–45
m

59–68 41–54
m

simple compound

globose X — X X

Genus Cycadolepis Saporta, 1875 Type species. Cycadolepis villosa Saporta, 1875 Cycadolepis coriacea Mene´ ndez, 1966 Figures 7e–g, 8 Material studied. BA Pb 11667; BA Pb Pm 410, 411, 412, 413, 414; BA Pb MEB 70; and BA Pb MET 172.

Figure 7. a–d, Ptilophyllum valvatum (Villar de Seoane) emend. a, section of the external wall of the stoma with a longitudinal section of the papilla, BA Pb MET 170. b, detail of the TS section of the anticlinal wall, BA Pb MET 170. c, detail of the TS section of the epidermal wall, BA Pb MET 170. d, detail of the granular upper layer, BA Pb MET 170. e–g, Cycadolepis coriacea (Mene´ ndez) emend. e, transverse (TS) section of the external wall of the epidermis, BA Pb MET 172. f, detail of the TS section of the anticlinal wall, BA Pb MET 172. g, detail of the TS section of a subsidiary cell wall, BA Pb MET 172. P, papilla; GC, guard cells; UL, upper layer; ML, middle layer; LL, lower layer. Scale bar represents 5
m in a, b, e and f, 0.5
m in c, d and g.

Cuticular study of Bennettitales from Argentina

Emended diagnosis. Simple scale-leaf oblong or ovallanceolate 2.8 cm long and 2.0 cm wide. Abaxial side convex, with incurved margins, acute apex and wide base. Veins parallel in lower part, dichotomizing and anastomosing with a concentration of 12 per cm, terminating at the margins. Adaxial epidermis with rectangular, occasionally isodiametric cells 57
m long and 25
m wide. Surface smooth. Abaxial epidermis with rectangular, occasionally isodiametric cells 70
m long and 31
m wide. Surface with trichome bases. Scale-leaf amphistomatic. Paracytic stomatal apparatus 91
m long and 41
m wide. Subsidiary cells with transverse striae. Hypodermis present. Ultrastructurally, epidermal external wall with an upper layer 0.60
m thick; a middle layer 3.10
m thick; and a lower layer 0.80
m thick. Description. The scale-leaf has an acute apex, the base wide but incomplete and the abaxial side strongly convex (Figure 8a). The adaxial epidermal cells are regularly disposed, and maintain a longitudinal orientation. The cells have oblique end walls (Figure 8b). They are thick (2.8
m) and slightly sinuous (Figure 8d). The abaxial epidermal cells have thicker walls than the adaxial cells (Figure 8c) with a few irregularly disposed trichome bases. The trichome bases are 20
m in diameter and may be solitary or grouped in transverse rows of 3–6 cells. The stomata are scattered on both sides, but they are more frequent in the abaxial epidermis. The orientation of the stomata is transverse to the veins. The subsidiary cells bear transverse striae but do not have papillae (Figure 8c). They overlap the guard cells forming a cuticular ridge (Figure 8f). The guard cells are sunken and strongly cutinized (Figure 8e). There is a slightly cutinized hypodermis with cells similar to the epidermis. Ultrastructurally, the external wall of the epidermis consists of three layers (Figure 7e). The upper layer is dark and composed of granules that are uniformly disposed and without any definite structure (Figure 7g); the middle layer is light and the structure is ill-defined, apparently being composed of more dispersed granules than either the upper or the lower layers (Figure 7e, g); the lower layer is dark and shows a similar structure to the upper layer although the granules appear to form a fine stratum that is horizontally disposed, similar to lamellae separated by translucent channels (Figure 7g). At high magnification (125 k) the lower layer does not show the presence of lamellae or microchannels, only an amorphous structure. The anticlinal walls have the same structure in the three layers, but thicknesses differ in that the

473

upper and lower layers are more developed (Figure 7f). Comparison. The material analysed is anatomically similar to the bracts described by Mene´ ndez (1966) and Baldoni (1974) from the Baquero´ Group, but the scale studied is smaller. The diagnosis is emended by inclusion of the ultrastructural features that are evident in the new specimen described here. Cycadolepis involuta Mene´ ndez, 1966 Figure 9 Material studied. BA Pb 11668; BA Pb Pm 415, 416; and BA Pb MEB 71, 72. Description. Simple scale-leaf 3.0 cm long and 1.4 cm wide. The outline is oblong but more or less oval and its margins are incurved with an acute apex and a wide, partially incomplete, base. The abaxial side is convex (Figure 9a). The veins radiate from the base, curving, dichotomizing and anastomosing near the margins, with a concentration of 10 per cm (Figure 9a). The adaxial epidermis has rectangular cells up to 56
m long and 25
m wide, with thick (4.0
m), straight walls. They form regular rows and their surface is smooth (Figure 9b). Some cells are elongate-rhomboid with acute longitudinal termini (Figure 9d). The abaxial epidermis consists of rectangular cells up to 109
m long and 56
m wide, with walls that are thinner than those of the adaxial cells, and straight or slightly sinuous. The surface has trichome bases in some regions (Figure 9c). These are irregularly disposed, solitary and 33.6
m in diameter (Figure 9c). The scale-leaf is amphistomatic, with the stomata scattered on both sides, but more numerous in the abaxial epidermis. The orientation of the stomata is transverse to the veins. The stomatal apparatus is up to 90
m long and 53
m wide (Figure 9e, f). The subsidiary cells lack papillae, but form a cuticular ridge surrounding the pit (Figure 9f) above the sunken and strongly cutinized guard cells (Figure 9e). The hypodermis is slightly cutinized and has rectangular cells similar to those of the epidermis. Comparison. The material studied has the same anatomical characters as the specimens described by Mene´ ndez (1966) and Baldoni (1974) from the Baquero´ Group, and by Baldoni (1979) from the Springhill Formation, but in all cases the new specimens are smaller. All the species belonging to the genus Cycadolepis found in the Baquero´ Group

474

L. Villar de Seoane

Figure 8. Cycadolepis coriacea (Mene´ ndez) emend. a, general view of specimen, BA Pb 11667. b, detail of the adaxial epidermal cells, BA Pb MEB 70. c, striate subsidiary cells of a stoma in the abaxial epidermis, BA Pb Pm 410. d, detail of the adaxial cellular walls, BA Pb MEB 70. e, inner detail of a stomatal apparatus, BA Pb MEB 70. f, external view of a stoma showing rim of pit, BA Pb MEB 70. Scale bar represents 0.5 cm in a, 10
m in d–f, and 20
m in b and c.

Figure 9. Cycadolepis involuta Mene´ ndez 1966. a, general view of specimen, BA Pb 11668. b, detail of the adaxial epidermal cells, BA Pb Pm 415. c, external view of trichome base (arrow) in the abaxial epidermis, BA Pb Pm 415. d, detail of the adaxial cellular walls, BA Pb MEB 71. e, detail of the guard cells, BA Pb MEB 71. f, external view of a stoma (arrow), BA Pb MEB 71. Scale bar represents 0.5 cm in a, 10
m in d–f, and 20
m in b and c.

476

L. Villar de Seoane

and the Springhill Formation are compared in the following table:

Species

increased by cooling of the leaf surfaces; with a temperature of 15C and a humidity of 80% the

Locality

Scale: Size

Outline

Apex

Veins

Ep. Cells

Stomata

Papillae

Hairs

C. baqueroensis C. coriacea C. involuta C. jenkinsiana C. lanceolata C. menendezii C. oblonga

Baquero´

lanceolate

acute

25 per cm

4020
m

solitary

X

oblong or oval-lanc. oblong or oval ovatespatulate lanceolate

acute

12 per cm 10 per cm

78–109 34–53
m 59–90 48–53
m

solitary or grouped solitary

—

acute

40–50 20–24
m 39–101 20–39
m 31–109 14–56
m

rounded

8 per cm

—

acute

10 per cm

solitary or grouped solitary

rounded

5–6 per cm

C. petriellai

Baquero´

2–2.5 1–1.5 cm 2.8 2.0 cm 3.0 1.4 cm 14.5 6 cm 4.0 1.3 cm 10–12 3.5–5 cm 4.0 0.8 cm ?2.5 cm

C. sp.

Springhill

7.0 3.0 cm

oval

C. sp. 1

Baquero´

C. sp. 2

Baquero´

Baquero´ Springhill Baquero´ Springhill Baquero´ Baquero´ Baquero´ Baquero´

6.5 2.0 cm

ovalspatulate oblonglanceolate oblong

lanceolate

4. Discussion Spicer et al. (1994) suggested that during the Cretaceous, the vegetation below palaeolatitudes 40 North or South was predominantly xeric with: (1) reduced leaves, (2) sculptured surfaces, (3) specialized sunken stomata, and (4) thick cuticles which may have induced the absorption of water from a humid atmosphere. Furthermore, mid and low latitude plants exhibit xeromorphic characters and are often preserved charcoalified. Enlarging on these four points in turn: 1. Reduced leaves are a defense strategy for xerophytic plants. When the leaf surface is small, the possibilities of water loss are diminished, reducing the daily cuticular transpiration rate. The Bennettitales are characterized by having large leaves divided into small pinnae, thereby diminishing the extent of the evaporative surface. 2. Sculptured surfaces are directly or indirectly involved in plant-water relations. Barthlott & Wollenweber (1981) suggested that epidermal elevations and papillae increase air turbulence over leaf surfaces, reducing the heat stress of the leaves during the day. During the night, atmospheric water is

20–40 14–18
m 30–40 10–16
m 24–45 12–20
m 20–30 12–16
m

26–33 10–16
m 120 60
m

—

marginal

solitary or grouped solitary or grouped solitary or grouped

mammillate marginal

solitary

X

strong

15 per cm

16–20 per cm

26 10–16
m 20–30 10–16
m

26 16–26
m 40 20–26
m

X

sculpture retains water drops, thus forming a positive vapour gradient from the outside to the inside of the leaf, allowing the entrance of CO2 through the stomatal aperture. The Bennettitales are characterized by having leaves with a smooth adaxial epidermis and a strongly ornamented abaxial epidermis; in contrast the scale-leaves are ornamented on both surfaces. The ornamented abaxial surface of the bennettitalean leaves studied have different types of trichomes. Otozamites archangelskyi has simple papillae and globose hairs; Otozamites patagonicus has compound and simple papillae; Pterophyllum trichomatosum has simple papillae and hairs; Ptilophyllum valvatum has compound papillae and hairs; and Ptilophyllum antarcticum has both simple and compound papillae and hairs. On the other hand, the scale-leaves have irregular elevations on the epidermal surfaces associated with different types of hairs. Cycadolepis coriacea has solitary or grouped hairs; and Cycadolepis involuta has only solitary hairs. 3. Sunken stomata with protected papillae and epistomatal chambers reduce water loss even when they are open by reducing air circulation. Cutler (1982) suggested that the disposition and protection

Cuticular study of Bennettitales from Argentina

of the stomata is another important factor for determining environmental conditions, and Raven (1977) has emphasized the role of the stomata in regulating water loss especially during stress conditions. Generally, plants that live in dry habitats have sunken stomata. The bennettitalean leaves belonging to the genera Otozamites, Pterophyllum and Ptilophyllum have sunken stomata protected by two or four papillae. The species of Cycadolepis have sunken stomata protected by a cuticular ridge that forms an epistomatal chamber above the guard cells. 4. Lyshede (1982) suggested that the external wall of the epidermis is divided into five main layers: (i) epicuticular wax, which covers the surface of most higher land plants and appears as crystalline bodies or amorphous layers in a great diversity of form and thickness; (ii) the cuticle proper consisting almost exclusively of cutin, perhaps with wax incrustations; (iii) the cutinized layer usually consisting of a cellulose skeleton encrusted with cutin, wax and pectin; (iv) the pectin layer; and (v) the cellulose layer. The cutinized layer is normally the thickest part of the epidermal wall. In xerophytic plants it is divided into an outer layer without cellulose and an inner layer with cellulose and pectinaceous microchannels. Barale & Baldoni (1993) analysed the ultrastructure of five Bennettitalean species from the Anfiteatro de Tico´ Formation (Baquero´ Group, Lower Cretaceous): Zamites decurrens Mene´ ndez; Dictyozamites areolatus Archangelsky & Baldoni; Ptilophyllum antarcticum (Halle) Archangelsky & Baldoni; Otozamites waltonii Archangelsky & Baldoni; and Cycadolepis oblonga Mene´ ndez. For all of these they described a homogeneous outer multilamellate or monolamellate layer. They suggested that the ultrastructure of transverse sections of these cuticles are very near type I of Holloway (1982), in which the outer zone is multilamellate, but monolamellate in places (Otozamites waltonii) and of varying thickness, and the internal zone may be amorphous, reticulate, fibrillar or a combination of the latter two. I have studied the ultrastructure of the epidermal wall in Otozamites ornatus from the Bajo Tigre Formation (Baquero´ Group) and this consists of a compact and uniform upper layer, and a thick lower layer that may be divided into two sub-layers: a lamellate upper sub-layer with superposed lamellae separated by translucent channels, and an alveolate lower sub-layer with small lacunae and a strong net (Villar de Seoane, 1999). The specimens analysed for this paper do not show the structures described by Barale & Baldoni (1993) or Villar de Seoane (1999) in the cuticular membrane,

477

except for the net and channel arrangement of structural elements in the papillate walls of Otozamites patagonicus. According to Lyshede (1982, p. 95), who remarked that ‘‘these microchannels are stable wall structures in the inner cutinized sublayer containing pectin’’, a lack of such microchannels is not possible in any foliaceous structure. The Springhill Formation is characterized by carbonized fossil material. The charcoal fragments are present on the cuticular surface, especially between the cellular wall and the papillae of the stomata (e.g., in Pterophyllum trichomatosum; Figure 4d) and within the layers of the external wall of the epidermis (e.g., in Otozamites patagonicus; Figure 4b). High temperatures may have altered the ultrastructure of the epidermal wall and transformed the multilamellate and reticulate-alveolate layers to amorphous layers. These high temperatures may have resulted from forest fires possibly initiated by volcanoes in the region (Cortin˜ as & Arbe, 1981). During the Cretaceous, plant life was strongly influenced by volcanic activity in a vast area of Patagonia. The source area of the persistently falling ash was located to the west along the Andean orogenic belt where volcanoes occur today (Archangelsky et al., 1995). In the platform area of the northeastern part of the basin, between 44 and 53S, the weathering and erosion of the volcanic rocks resulted in transport and deposition of the oil-bearing continental to marine sandstones of the Springhill Formation which disconformably overlie the Jurassic El Quemado Volcanic Complex (Riccardi, 1988). 5. Conclusions New morphological and structural characters are described and illustrated using LM, SEM and TEM for seven species (Otozamites patagonicus sp. nov., Otozamites archangelskyi, Pterophyllum trichomatosum, Ptilophyllum valvatum, Ptilophyllum antarcticum, Cycadolepis coriacea and Cycadolepis involuta) belonging to four genera of bennettitalean structures. The LM and SEM studies show that the seven species have similar xeromorphic epidermal characters. All have an epidermis sculptured with granules, hairs and papillae, and sunken stomata with papillate subsidiary cells or a cuticular ridge protecting the mouth. The TEM studies have revealed that the external wall of the epidermis has a similar thickness in Otozamites, Pterophyllum and Ptilophyllum, but is notably thicker in Cycadolepis. The ultrastructure is similar in all species; each has three amorphous layers, the upper and lower layers being darker than the middle layer. All layers

478

L. Villar de Seoane

have a granulate ultrastructure of variable electron density at high magnification (125 k). These xeromorphic characters probably indicate high temperatures, low humidity and arid soils. Such palaeoenvironmental conditions may have been produced by volcanic activity, as reflected by the types of sediments found in this formation. Finally, the presence of carbonized specimens is likely to have been a consequence of forest fires initiated during dry seasons or regional volcanic activity. Acknowledgements Thanks are due to Dr Sergio Archangelsky for critical comments on the manuscript and for providing the material; Prof. David J. Batten and the anonymous reviewers for linguistic corrections and valuable suggestions for improving the paper; Dr Rube´ n Cu´ neo for fieldwork in connection with the fossil collection; Isabel Farías for technical assistance in the preparation of cuticles for TEM; La Plata Natural History Museum for use of the SEM and the Cellular Biology Department (Medicine, Buenos Aires University) for access to their TEM. This research has been supported by the National Research Council (CONICET), grant PICT 99 07-06044. References Archangelsky, A., Andreis, R., Archangelsky, S. & Artabe, A. 1995. Cuticular characters adapted to volcanic stress in a new Cretaceous cycad leaf from Patagonia, Argentina. Considerations on the stratigraphy and depositional history of the Baquero´ Formation. Review of Palaeobotany and Palynology 89, 213–233. Archangelsky, S. 1976. Vegetales fo´ siles de la Formacio´ n Springhill, Creta´ cico, en el Subsuelo de la Cuenca Magalla´ nica, Chile. Ameghiniana 13, 141–158. Archangelsky, S. & Baldoni, A. 1972. Revisio´ n de las Bennettitales de la Formacio´ n Baquero´ (Creta´ cico Inferior), provincia de Santa Cruz. I. Hojas. Revista del Museo de La Plata (Nueva Serie) Paleontologı´a 7 (44), 195–265. Baldoni, A. 1974. Revisio´ n de las Bennettitales de la Formacio´ n Baquero´ (Creta´ cico Inferior), Pcia. de Santa Cruz. II. Bra´ cteas. Ameghiniana 11, 328–356. Baldoni, A. 1977. Ptilophyllum ghiense n. sp., una nueva Bennettital de Paso Roballos, Provincia de Santa Cruz. Ameghiniana 14, 53–58. Baldoni, A. 1979. Nuevos elementos paleoflorı´sticos de la Tafoflora de la Formacio´ n Springhill, lı´mite Jura´ sico-Creta´ cico, subsuelo de Argentina y Chile Austral. Ameghiniana 16, 103–119. Baldoni, A. & Taylor, T. N. 1983. Plant remains from a new Cretaceous site in Santa Cruz, Argentina. Review of Palaeobotany and Palynology 39, 301–311. Barale, G. & Baldoni, A. 1993. L’ultrastructure de la cuticule de quelques Bennettitales du Cre´ tace´ infe´ rieur d’Argentine. Comptes Rendues de l’Acade´mie des Sciences de Paris 316, 1171–1177. Barthlott, W. & Wollenweber, E. 1981. Zur Feinstruktur, Chemie und taxonomischen Signifikanz epicuticularer Wachse und ahnlicher Sekrete. Tropische und Subtropische Pflanzenwelt 32, 1–67. Boyd, A. 1998. Bennettitales from the Early Cretaceous floras of West Greenland: Pseudocycas Nathorst. Palaeontographica B 247, 123–155.

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