Submitted: January 13th, 2020 – Accepted: June 23th, 2020 – Published online: June 28th, 2020
To link and cite this article:
doi: 10.5710/AMGH.23.06.2020.3333
1 A NEW SPECIES OF BRACHYPHYLLUM FROM THE CRATO FORMATION
2 (LOWER CRETACEOUS), ARARIPE BASIN, BRAZIL
3
4 MARIA EDENILCE P. BATISTA1,2*, LUTZ KUNZMANN3, ARTUR A.A. SÁ4,5,
5 ANTÔNIO ÁLAMO F. SARAIVA2, MARIA IRACEMA B. LOIOLA6
6 1Programa de Pós-Graduação em Ecologia e Recursos Naturais, Departamento de Biologia,
7 Universidade Federal do Ceará, Av. Mister Hull, CEP 60455-900, Fortaleza, Brazil.
8 2Departamento de Ciências Biológicas, Universidade Regional do Cariri, R. Cel. Antônio
9 Luis, CEP 63105-000, Crato, Brazil. 3Senckenberg Natural History Collections,
10 Königsbrücker Landstr. 159, 01109 Dresden, Germany. 4Departamento de Geologia,
11 Universidade de Trás-os-Montes e Alto Douro, Quinta de Prados, 5000-801 Vila Real,
12 Portugal. 5Centro de Geociências, Universidade de Coimbra-Polo II, 3030-790 Coimbra,
13 Portugal. 6Departamento de Biologia, Universidade Federal do Ceará, Av. Mister Hull, CEP
14 60455-900, Fortaleza, Brazil.
15 20 pag. (text+references); 5 figs. 2 tables
16 BATISTA ET AL.: NEW BRACHYPHYLLUM FROM THE ARARIPE BASIN, BRAZIL
17 permineralized
18 Running Header: We describe a new species of the fossil genus Brachyphyllum from the
19 Crato Formation, Araripe Basin, Brazil.
20
21 Corresponding author: Maria Edenilce Peixoto Batista, e-mail [email protected]
22
23
24
25 26
27 Abstract. The Araripe Basin, located on the Northeast of Brazil, contains many fossils.
28 Among these, the gymnosperms stand out, especially species of the fossil taxon
29 Brachyphyllum. It encompasses conifer shoots with helically arranged scale-like, adpressed
30 leaves whose length does not exceed the width. This foliage morphotype was widely
31 distributed during the Mesozoic and species accommodated in this genus can be attributed to
32 different families if their anatomical characters are taken into consideration. In the Araripe
33 basin, specifically in the Crato and Romualdo formations, B. obesum is frequently found and
34 was attributed to the family Araucariaceae based on leaf epidermal and xylem characters. In
35 this work, we describe the new species from the Crato Formation (Lower Cretaceous),
36 Brachyphyllum sattlerae sp. nov., based on the following morphological and anatomical
37 features: submain shoots with lateral branches oppositely disposed and almost exclusively
38 decussately arranged leaves; scarious leaf margins; rugose abaxial leaf surfaces; non-papillate
39 epidermal cells; stomata distributed in longitudinal rows except close to the leaf margins and
40 scarce at the leaf base; stomatal openings obliquely oriented; and hypodermis with a sinuous
41 pattern around the substomatal chamber. Some of these features are distinctive of
42 Araucariaceae, which indicates that B. sattlerae sp. nov. also belongs to this family.
43
44
45 Key words. Araucariaceae. Cretaceous. Conifer. Epidermal micromorphology.
46
47 Resumen. UNA NUEVA ESPECIE DE BRACHYPHYLLUM DE LA FORMACIÓN CRATO
48 (CRETÁCICO INFERIOR), CUENCA ARARIPE, BRASIL. La cuenca de Araripe, ubicada
49 en el noreste de Brasil, contiene mumerosos registros fósiles. Entre estos, se destacan las
50 gimnospermas, especialmente las especies del género fósil Brachyphyllum. Se registran ramas 51 de coníferas con hojas dispuestas helicoidalmente en forma de escamas, adheridas, cuya
52 longitud no excede el ancho. Este tipo foliar se distribuyó ampliamente durante el Mesozoico
53 y las especies asignadas en este género pueden atribuirse a diferentes familias si se tienen en
54 cuenta sus caracteres anatómicos. En la cuenca de Araripe, específicamente en las
55 Formaciones Crato y Romualdo, B. obesum se encuentra con frecuencia y fue atribuida a la
56 Familia Araucariaceae por sus caracteres epidérmicos y el xilema de las hojas. En este
57 trabajo, describimos una nueva especie recuperada en la Formación Crato (Cretácico Inferior),
58 Brachyphyllum sattlerae sp. nov., basada en las siguientes características morfológicas y
59 anatómicas: brote subprincipal con ramas laterales con disposición opuesta y hojas casi
60 exclusivamente dispuestas de forma decusada; márgenes de las hojas escariosas; las
61 superficies abaxiales de las hojas son rugosas; las células epidérmicas sin papiladas; estomas
62 distribuidos en hileras longitudinales excepto cerca de los márgenes de las hojas siendo
63 escasos en la base de la hoja; aberturas estomáticas orientadas oblicuamente; e hipodermis
64 con un patrón sinuoso alrededor de la cámara subestomática. Algunas de estas características
65 son distintivas de Araucariaceae, lo que indica que B. sattlerae sp. nov. pertenece a esta
66 familia.
67
68
69 Palabras clave. Araucariaceae. Cretácico. Coníferas. Micromorfología epidérmica.
70
71
72
73
74
75 76
77 THE Araripe Basin in northeastern Brasil has been known for a long time for its exquisitely
78 preserved fossils recovered from several formations. The basin has already been included
79 among the top ten of the fossil lagerstätten in the world (Maisey, 1991; Martill, 1990). One of
80 its units, the Lower Cretaceous Crato Formation, is considered one of the best windows to a
81 northern Gondwanan Cretaceous ecosystem (Martill et al., 2007). The Crato fossil beds are a
82 classical konservat lagerstätte containing excellently preserved vertebrates, invertebrates and
83 plants. The Crato taphoflora is rather diverse and includes charophytes, sphenophytes,
84 lycophytes, monilophytes, gnetaleans, conifers, pteridospermophytes, cycadophytes, and
85 angiosperms, (Bernardes-de-Oliveira et al., 2007; Fanton, 2007; Martill et al., 2007; Mohr et
86 al., 2000; Mohr et al., 2007). As low latitude fossil flora, it lacks typical mid to high latitude
87 groups such as gingkoaleans.
88 Conifers have been described from megafossil remains and pollen assemblages.
89 Among megafossils, representatives of the families Araucariaceae, Cheirolepidiaceae, and
90 Podozamitaceae were determined (Duarte, 1985, 1993; Kunzmann et al., 2004, 2006; Mohr et
91 al., 2007, 2012; Sucerquia et al., 2015; Batista et al., 2017), while Cupressecae and Pinaceae
92 were reported from pollen assemblages (Lima, 1979; Batten, 2007; Portela et al., 2014).
93 Species of Araucariaceae and a considerable number of species of Cheirolepidiaceae are
94 characterized as large canopy-forming trees (Bernardes-de-Oliveira et al., 2007; Martill et al.,
95 2007; Barral et al., 2016). Foliage shoots of the taxon Brachyphyllum Lindl. et Hutton ex
96 Brongn. emend. T.M.Harris are the most frequent plant fossils of the Crato flora (Duarte,
97 1985; Kunzmann et al., 2004; Batista et al., 2017). However, in contrast to the number of
98 specimens reported, the diversity of fossil species determined from the Crato flora is
99 comparatively low. Only two species B. obesum Heer and B. castilhoi L.Duarte have been
100 described to date (Batista et al., 2017). While the majority of the Brachyphyllum shoots are 101 ascribed to Among B. obesum, the latter species is quite rare (Duarte, 1985, 1993; Martill et
102 al., 2007).
103 Representatives of the fossil genus Brachyphyllum have been reported from all
104 continents during the Mesozoic Era (Traverso, 1968; Ash, 1973; Raab et al., 1986; Yabe &
105 Kubota, 2004; Barale & Appert, 2007; Du et al., 2013; Karakitsios et al., 2015). It is
106 characterized by helically arranged,scale-like adpressed leaves, whose total length (length of
107 the free part and length of the cushion) is the same or less than the width of the leaf cushion
108 (Kendall, 1947; Harris, 1979). According to the concept of Harris (1979), who gave an
109 emended diagnosis, Brachyphyllum is an artificial morphotype. If anatomical characters, such
110 as leaf epidermis and wood structure, are preserved and taken into consideration for
111 taxonomic purposes individual species show clear affinities to different families. To date,
112 Brachyphyllum species are affiliated to Araucariaceae, Cheirolepidiaceae, Podocarpaceae,
113 and Cupressaceae (Hollick & Jeffrey, 1906; Kendalll, 1947; Harris, 1979; van der Ham et al.
114 2003; Kunzmann et al., 2004; Batista et al., 2017). For instance, the aforementioned B.
115 obesum was repeatedly assigned to Araucariaceae (Kunzmann et al., 2004; Batista et al.,
116 2017), whereas the systematic relationships of B. castilhoi are still indefinite. This taxonomic
117 question can only be resolved if appropriately preserved fossil material will be available for
118 micro- and ultrastructural studies.
119 In this paper, we analyze the morphology and epidermal structure of peculiar
120 Brachyphyllum specimens from the Crato Formation whose features exclude an attribution to
121 both B. obesum and B. castilhoi. Based on a distinct set of characters we propose the new
122 species of Brachyphyllum sattlerae sp. nov., which most likely belongs to the Araucariaceae.
123 Therefore, our result contributes to better understand the diversity and frequency of conifers
124 in a paleo-equatorial environment of Gondwana.
125 126 GEOLOGICAL SETTING
127 The Araripe Basin is located upon the central part of a continental collision belt called
128 the Proterozoic Borborema Tectonic Province (Assine, 1992, 2007; Valença et al., 2003).
129 Geographically, this Mesozoic basin is situated in the border areas of Ceará, Pernambuco and
130 Piauí states. It is the most extensive intracratonic basin of northeastern Brazil, covering an
131 area of about 9,000 km2. Its depositional history ranges at least from the Upper Jurassic to the
132 Upper Cretaceous. The origin of this basin was related to the reactivation of continental-
133 scaled basement faults, which was caused by tectonic movements during the opening of the
134 South Atlantic and the subsequent separation of South America and Africa (Assine, 1992,
135 2007; Carvalho et al., 1995; Valença et al., 2003).
136 The limestone slabs containing the fossil study specimens come from the Crato
137 Formation, Santana Group (Fig. 1 and 2). This formation was deposited during the post-rift
138 tectonic phase and mainly comprises light-coloured to greyish laminated micritic limestones,
139 intercalated by darker and calciferous shales and sandstones. The lithology of the limestones
140 is indicative of a lacustrine environment that was characterized by the low terrigenous influx
141 and that was deposited under a seasonal climate with high temperatures and longer dry and
142 shorter wet seasons (Beurlen, 1971; Assine, 1992, 2007; Valença et al., 2003; Martill et al.,
143 2007). There are, however, claims for a partly and/or temporarily hypersaline water body or
144 even first marine ingressions from an early Proto-South Atlantic. Shallo and hypersaline
145 water conditions are evidenced by halit pseudomorphs and stromatolithic microbialites in the
146 limestone sections (Santos et al., 2017; Warren et al., 2017).
147 Based on its palynological assemblages, the Crato Formation is considered to be late
148 Aptian to probably early Albian in age (Viana & Neumann, 2002; Batten, 2007).
149 [Figure 1 here]
150 151 [Figure 2 here]
152
153
154 MATERIAL AND METHODS
155 All studied fossil specimens were collected at the flagstone-producing quarries known
156 as Mina Pedra Branca, near the town Nova Olinda, Ceará State, Brazil. Due to the common
157 excavation and sampling approaches, it is unknown from with subunit of the limestone
158 section our study specimens are coming from.
159 Branched shoots are preserved as compressions and have been replaced by iron oxide.
160 The specimens MPSC PL 561 and MPSC PL 804 are deposited in the Paleontological
161 Museum Plácido Cidade Nuvens, Santana do Cariri, Ceará State, Brazil. The specimen SAK -
162 6 is kept in the paleobotanical collection of Senckenberg Natural History Collections Dresden,
163 Germany. Small samples of the best-preserved specimen, MPSC PL 561, were subject to
164 scanning electron microscope (SEM) analyses in order to observe anatomical features of the
165 leaf surface. First, they were mounted to aluminium stubs using carbon tape and then
166 sputtered with a 20-nm-thick gold layer. The analyses were conducted at the Central Analítica
167 of the Universidade Federal do Ceará (UFC), Fortaleza, Ceará State, Brazil, with the SEM
168 Inspect S50 and Quanta 450 FEG, FEI Company.
169
170 SYSTEMATIC DESCRIPTION
171 PINIDAE Cronquist, Takht. et W.Zimm., 1966
172 Brachyphyllum Lindl. et Hutton ex Brongniart, 1828 emend. T.M.Harris, 1979
173 Type species Brachyphyllum mamillare Lindl. et Hutton 1836.
174 Brachyphyllum sattlerae Batista, L.Kunzmann, Sá, Saraiva et Loiola sp. nov. 175 Etymology. The specific epithet is after Ellie Sattler, the fictional character of the Jurassic
176 Park novel and film who contributed to popularize the role and importance of both
177 palaeobotanists and women for science in general.
178 Holotype. MPSC PL 561, selected herein, (Fig. 3, 4 and 5).
179 Referred specimens. MMG PB SAK 6 and MPSC PL 804, (Fig. 3).
180 Type horizon and locality. Lower Cretaceous (upper Aptian) Crato Formation, Santana
181 Group of the Araripe Basin; flagstone quarry near Nova Olinda, Ceará State, northeastern
182 Brazil (Figs 1 and 2).
183 Diagnosis. Penultimate branches opposite; on ultimate branches scale leaves arranged
184 decussately or almost decussately, on wider branches helically in a very low spiral; leaf
185 margin scarious; abaxial leaf surface rugose and bearing stomatal apparatuses arranged in
186 longitudinal rows separated by rows of elongate ordinary epidermal cells; stomatal
187 apparatuses monocyclic, with four to six non-papillate subsidiary cells; stomatal apertures
188 mainly obliquely oriented; ordinary epidermal cells non-papillate; hypodermal bundles of
189 sclerenchyma heavily lignified and with sinuous patterns around the uppermost portions of
190 the substomatal chamber; tracheids of the primary xylem with scalariform thickenings.
191
192 Description. Brachyphyllum sattlerae sp. nov. is known from penultimate and ultimate
193 foliage shoot fragments. The leafy shoots branch regularly branched with both main and
194 lateral branches being straight (Fig. 3). The analyzed specimens show only two orders of
195 branching, in which the ultimate branches are oppositely arranged and diverge from the main
196 axis at angles of 37°–65º. The distance between successive lateral branches ranges from 1.0 to
197 5.6 mm. The main axes of the specimens are ca. 6–8 mm in width and ca. 40–100 mm in
198 length, whereas the short lateral branches are ca. 4–6 mm in width and ca. 15 mm in
199 maximum length. 200
201 [Figure 3 here]
202
203 All branches are densely covered with coriaceous or ‘fleshy’ leaves, which are
204 arranged in a very low spiral at main axes but appear to be occasionally almost decussately or
205 decussately arranged at ultimate lateral branches. (Fig. 4.1). They do not differ significantly in
206 their shape from each other. The leaves are scale-like, rhomboidal, adpressed to the stem and
207 imbricated to various extents , reaching with their apices the bases of the following leaves.
208 The abaxial leaf surface is rugose, which is expressed by the presence of three to four
209 keels that become less marked towards the leaf apex (Fig. 4.2). The free apical leaf portions
210 are rather short. Particularly, the apex is acute, somewhat bulge-shaped and slightly curved
211 towards the axis. Leaf margins are scarious, with a single thin layer of elongated cells
212 building a frill-like fringe which adheres to the neighbouring leaf (Fig. 4.4). These cells are
213 ca. 98 µm in length and 30 µm in base width. In general, leaves are wider (5.9–6.9 mm) than
214 long (4–5.1 mm). Leaf size varies, i.e. those at the main axis are larger than those at the lateral
215 branches. Leaves of lateral branches are 5–5.1 mm in width and 3–3.9 mm in length.
216
217 [Figure 4 here]
218
219 Stomata are visible in low magnification, which is a matter of their sizes and the fact,
220 that their apertures are frequently filled with withish-yellow sediment that underlines with its
221 distinct colour the visibility of stomata on the brownish leaf surfaces (Fig. 4.2). Stomata are
222 present on almost the entire abaxial leaf surface except for narrow areas adjacent to the leaf
223 margin (Fig. 4.3). They gradually become less numerous towards the leaf base. They are
224 arranged in longitudinal rows that converge towards the leaf apex separated by a variable 225 number of rows of elongate ordinary epidermal cells. The stomatal apparatus is monocyclic,
226 with four to six subsidiary cells that vary in shape from oval to roundish (Figs. 5.1 and 5.2).
227 and Subsidiary cells are never shared between adjacent stomata. Guard cells are kidney-
228 shaped and sunken and form stomatal apertures that are obliquely oriented in relation to the
229 longitudinal leaf axis (Figs. 5.1 and 5.2). These stomatal apparatuses are ca. 77–105 µm in
230 diameter, whereas the rounded ones are ca. 71–85 µm in diameter.
231 Ordinary epidermal cells are longitudinally arranged in rows in relation to the leaf
232 margin and they can be either square-shaped or polygonal to rectangular in outline (Figs. 5.3
233 and 5.4). Those at the leaf base are wider (ca. 30–40 µm) but shorter (ca. 23–35 µm) than the
234 others (ca. 16–23 µm in width and 46–92 µm in length). All epidermal cells, including the
235 subsidiaries, have thickened (ca. 4 µm) cell walls and lack papillae and hairs. The cuticle is
236 relatively thin (ca. 3 µm). Sinuous bundles of sclerenchyma, heavily lignified, occur in the
237 hypodermis around the uppermost portions of the substomatal chambers (Fig. 5.5). The
238 primary xylem has tracheids with scalariform thickenings (Fig. 5.6).
239
240 [Figure 5 here]
241
242 COMPARISONS AND DISCUSSION
243 Based in the dimensions of the scale leaves and other morphological features such as
244 leaf lamina adpressed, small free apical leaf portion and phyllotaxis, the study material is
245 clearly assigned to Brachyphyllum. This fossil genus is solely defined on gross-morphological
246 features, i.e. helically arranged, adpressed scale leaves that are shorter than wide or as long as
247 wide (Harris, 1979). Its leaves could be also slightly imbricated. Anatomical characters were
248 excluded from the emended generic diagnosis (Harris, 1979) which is commonly accepted to
249 date. 250 Observing most of the lateral branches, the phyllotaxis of B. sattlerae sp. nov. is
251 almost exclusively decussate, which is a common character in several Cupressaceae genera,
252 such as Thuja, Thujopsis, Calocedrus, and Chamaecyparis, as well as in non-frenelopsid
253 Cheirolepidiaceae (Alvin, 1982). An overall decussate phyllotaxis would exclude an
254 affiliation of our study material to Brachyphyllum. However, in some main branches, the
255 phyllotaxy of B. sattlerae sp. nov. is also helical to a certain extent. This condition resembles
256 that of B. elegans from the Jurassic of England, whose submain branches have a decussate
257 phyllotaxis, whereas on larger branches it becomes partly spiral (Karakitsios et al., 2015). To
258 our opinion, in B. sattlerae sp. nov. The marked variations of phyllotaxis may have occurred
259 in a similar way, but it is not possible to definitely state this for the entire plant because only
260 submain branches are available so far. Decussate phyllotaxis on smallest branches could be a
261 consequence of the dimensions of leaves and axes. The thick coriaceous leaves are born in
262 comparatively thin axes which is why space for leaves is limited. If more material would be
263 available, a statistical analysis would be feasible in order to clarify if the decussate phyllotaxis
264 is a specific “space phenomenon” or not. However, as the thicker axes display also helical
265 phyllotaxis we have no doubt to accomodate our species into Brachyphyllum, adopting the
266 concept of B. elegans to our material.
267 Brachyphyllum elegans differs from B. sattlerae by its non-scarious leaf margins and
268 smooth abaxial surfaces, along with the remarkable size difference, in which the former has
269 branches with a maximum width of 2.5 mm and the latter has branches with width ranging
270 from 4 to 8 mm (Karakitsios et al., 2015).
271 Interpreting the generic diagnosis, Brachyphyllum cannot be affiliated with a family.
272 Moreover, species lacking anatomical characters, e.g., epidermal or vascular, also cannot be
273 assigned to a family. As the diagnosis encompasses only very few characters, it is rather
274 difficult to distinguish Brachyphyllum species only based on their morphological and 275 morphometric features. However, if epidermal features are available from the fossils they can
276 vary significantly between species making distinction of species significantly and affiliations
277 of species to different families obvious (Tables 1, 2) (Du et al., 2013).
278
279 [Table 1 here]
280
281 Brachyphyllum sattlerae sp. nov. shares with B. obesum, the most frequent plant fossil
282 and species in the Crato flora, the monocyclic stomata apparatuses and their arrangement of in
283 longitudinal rows on the abaxial leaf surface. However, these species are distinct by specific
284 epidermal and morphological characters. Leaves of B. obesum from Brazil, as well as from its
285 type horizon in Portugal, are arranged in well-marked spirals (Heer, 1881; Saporta, 1894;
286 Duarte, 1985; Kunzmann et al., 2004; Yabe & Kubota, 2004; Batista et al., 2017). Another
287 character, the striated abaxial surfaces, which is an original diagnostic feature, is repeatedly
288 identified as preservational phenomenon. Kunzmann et al. (2004) and Batista et al. (2017)
289 showed that the abaxial striations of B. obesum are actually well-defined, prominent stomatal
290 rows longitudinally oriented. In contrast, the abaxial surface of B. sattlerae is rugose and its
291 stomatal apparatuses are in less prominent and less well-defined rows. Additionally, the
292 distances between adjacent stomata in a row and between neighbouring stomatal rows are
293 greater in B. sattlerae than in B. obesum. Another difference between the two species is that
294 the orientation of the stomatal apertures is alomost exclusively oblique in B. sattlerae,
295 whereas these structures are more perpendicularly or randomly oriented in B. obesum
296 (Kunzmann et al., 2004; Batista et al., 2017). Moreover, stomatal apparatuses are evenly
297 distributed throughout the whole leaf surface of B. obesum (Kunzmann et al., 2004), whereas
298 in B. sattlerae sp. nov. they are scarce at the leaf base and absent close to the leaf margins. 299 Another species from the Araripe Basin is B. castilhoi (Duarte, 1985; Kunzmann et
300 al., 2004), whose coniferous nature has not been unambiguously shown to date. The axes
301 display helically arranged ?leaf scares but leaves were never preserved. However, the most
302 distinctive character, which is the claviform-shaped lateral shoots, has not been observed from
303 any other Brachyphyllum species.
304 Actually, the scarious leaf margins seen in B. sattlerae sp. nov. are quite common in
305 many Brachyphyllum species and help to distinguish these taxa from those lacking this
306 feature. Among the species with scarious margins are B. castatum, B. comancheanum, B.
307 crucis, B. expansum, B. irregulare, B. kachaikensis, B. mamillare, B. mirandai, B.
308 mucronatum, B. obesum, B. pulcher, B. scalbiensis, B. squamosum, B. tigrense and B.
309 baqueroense (Bancroft, 1913; Kendall, 1947, 1949; Archangelsky, 1963; Traverso, 1966,
310 1968; Lorch, 1968; Harris, 1979; Givulescu & Bucur, 1985; Watson et al., 1987; Raubeson &
311 Gensel, 1991; Ash, 1999; Kunzmann et al., 2004; Kvaĉek, 2007; Passalia, 2007; Carrizo et
312 al., 2019). On the other hand, theses species can also be set appart from B. sattlerae sp. nov.
313 based on various differences which are listed in detail in Tables 1 and 2. For instance, B.
314 castatum has stomata distributed in a scattered way, with 5–12 subsidiary cells and their
315 leaves are exclusively spirally arranged (Watson et al., 1987). B. kachaikensis exhibits
316 stomatal openings that are randomly oriented, and its phyllotaxis is also helically (Passalia,
317 2007). B. expansum shows obtuse leaf apices and falciform abaxial surfaces, although its
318 helical phyllotaxis is not very clear (Kendall, 1949; Givulescu & Bucur, 1985). B. tigrense
319 has a helical phyllotaxis too, and stomata are arranged in well-defined rows, but leaves exhibit
320 smooth abaxial surfaces (Traverso, 1966).
321 As reported by Kunzmann et al. (2004), no hypodermis of B. obesum is known, but in
322 B. sattlerae sp. nov. it is easily observed, being sinuous and heavily lignified. Actually, the
323 presence of a hypodermis is also a common feature of several species of Brachyphyllum 324 (Table 2) (Bancroft, 1913; Kendall, 1947, 1949; Archangelsky, 1963; Traverso, 1966; Lorch,
325 1968; Harris, 1979; Givulescu & Bucur, 1985; Watson et al., 1987; Ohana & Kimura, 1993;
326 van der Ham et al., 2003; Passalia, 2007; Barale & Appert, 2007; Carrizo et al., 2019). In B.
327 kachaikensis, for instance, hypodermal cells are heavily lignified and form a ring around the
328 substomatal chamber (Passalia, 2007). In B. patens, these cells present a sinuous pattern
329 around the substomatal chambers (van der Ham et al., 2003), as in B. sattlerae sp. nov. too.
330 However, the former species differs from the latter in having the stomatal apparatuses
331 scatterly arranged on the abaxial surface (van der Ham et al., 2003).
332
333 [Table 2 here]
334
335 In short, none of the previously described Brachyphyllum species is characterized by
336 the same combination of features that we have observed in our study material. The definition
337 of a new fossil species within the genus Brachyphyllum is justified. The characters of the leaf
338 epidermis, i.e. all cells non-papillate and stomata arranged in longitudinal rows which are
339 distributed over alomost the complete abaxial surface, are meaningful for an affiliation of the
340 new species to Araucariaceae. This has been demonstrated for instance for Brachyphyllum
341 mamillare from the Yorkshire Jurassic flora of UK (Harris, 1979), for Brachyphyllum
342 (Araucaria) vulgaris from the Upper Cretaceous of Hokkaido, Japan (Ohsawa et al., 1995),
343 and for Brachyphyllum obesum from the Crato flora (Kunzmann et al., 2004; Batista et al.,
344 2017). Non-frenelopsid taxa of the familiy Cheirolepidiaceae are distinguished by
345 prominently papillate epidermal cells and by scatterly arranged stomata. In species of
346 Cupressaceae, stomata are arranged in two bands or in two triagular patches on the abaxial
347 surface. Within band and patches, stomata could be ordered randomly or in rows. In scaled-
348 leaved taxa of Podocarpaceae, stomata are either arranged in bands, patches or scatterly on 349 abaxial surface, never in longitidinal rows covering the complete abaxial side. Their stomata
350 apertures are strictly longitidinally oriented. For more detailed data in epidermal cell structure
351 on Araucariaceae, Cupressaceae and Podocarpaceae see Florin (1931).
352 CONCLUSION
353 The study material shows a specific combination of morphological and anatomical
354 features which has not been described from any other Brachyphyllum species. Brachyphyllum
355 sattlerae sp. nov. is distinct by the presence of (1) rugose abaxial leaf surfaces, (2) an opposite
356 arrangement of lateral branches at least in submain shoots, (3) almost exclusively decussately
357 arranged leaves, (4) stomata distributed in longitudinal rows except close to the leaf margins
358 and scarce at the leaf base, (5) obliquely oriented stomatal openings, (6) scarious leaf margins,
359 and (7) hypodermis with a sinuous pattern around the substomatal chambers. indicate that B.
360 sattlerae is indeed a new conifer species as The description of this new species from the Crato
361 Formation indicates more diversity among araucarian conifers in the paleo-equatorial
362 Gondwanan Araripe Basin.
363
364 ACKNOWLEDGMENTS
365 We thank the staff of the Paleontological Museum Plácido Cidade Nuvens and Institute
366 Senckenberg for providing specimens for this study. Central Analítica (UFC) for the technical
367 assistance during the SEM analysis. Marcos Sales for giving important contributions to early
368 drafts of this manuscript. Islandia Silva for helping with the figures. Manuel Robledo
369 (Universidad Nacional del Nordeste, Corrientes, Argentina) for sharing important references.
370 Edson J. C. Amaro (UFC) kindly helped with the methods and early drafts of the manuscript.
371 We would like also to express our gratitude to anonymous reviewers, whose suggestions
372 considerably improved this paper. This work was supported by the Coordenação de
373 Aperfeiçoamento de Pessoal de Nível Superior (CAPES, Finance Code 001) under a PhD 374 grant to M.E.P.B., Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq)
375 under a productivity grant to M.I.B.L and Fundação Cearense de Apoio ao Desenvolvimento
376 Científico e Tecnológico (FUNCAP) under a productivity grant to A.A.F.S. Authors MEPB
377 and LK are members of the Crato Fossil Lagerstätte Project Group which received funding in
378 the bilateral PROBRAL program by Brazilian CAPES (project ID 2018915170P) and German
379 DAAD (project ID 57446885).
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545 Figure captions
546 Figure 1. Map showing the provenance of studied specimens. 1, Location of the Araripe
547 Basin, northeastern Brazil. Scale bar 40 km. 2, Simplified geological map of the area
548 indicated by the rectangle in 1. Scale bar 6 km. Abbreviation: Fm, formation. Modified from
549 Batista et al. (2017) after Martill et al. (2007).
550
551 Figure 2. Stratigraphy of the Araripe Basin, northeastern Brazil. 1, Generalized
552 lithostratigraphic log for the northern central region of the Araripe Basin. 2,
553 Chronostratigraphic scheme of the basin. Modified from Batista et al. (2017) after Martill et
554 al. 2007).
555
556 Figure 3. Brachyphyllum sattlerae sp. nov. 1, Specimen MPSC PL 561, holotype. 2,
557 Specimen SAK-6. 3, Specimen MPSC PL 804. Scale bars 1 cm
558
559 Figure 4. Detail of Brachyphyllum sattlerae sp. nov. 1, Detail of a leaf of MPSC PL 561
560 showing the branches with opposite leaves. Scale bar 0,5 cm. 2, Detail of a leaf of MPSC PL
561 561 showing the rugose abaxial surface and the acute leaf apex. Scale bar 2 mm. 3, Margin of
562 another leaf (arrowhead) lacking stomata. Scale bar 1 mm. 4, Detail of the scarious condition
563 of the leaf margin shown in 3 (arrowhead) Scale bar 100 µm.
564 565 Figure 5. Anatomic details of Brachyphyllum sattlerae sp. nov (MPSC PL 561.) 1, Stomatal
566 aparatus of B. sattlerae, showing the guard cells (arrowhead). Scale bar 50 µm. 2, Stomatal
567 aparatus of B. sattlerae, showing the guard cells (black arrowhead) and subsidiary cells (white
568 arrowhead). Scale bar 50 µm. 3, Epidermal cells (arrowhead) arranged longitudinally with
569 varied shapes. Scale bar 100 µm. 4, Epidermal cells (black arrowhead) arranged
570 longitudinally with rectangular shapes and Stomatal apparatus (white arrowhead). Scale bar
571 100 µm. 5, Sinuous hypodermis (arrowhead) around the substomatal chambers of B. sattlerae.
572 Scale bar 200 µm. 6, Tracheids of B. sattlerae with scalariform thickenings (arrowhead) Scale
573 bar 50 µm.
TABLE 1. Macromorphological comparisons of Brachyphyllum species. Species Branch Leaf shape and phyllotaxy Abaxial surface Leaf apex Geological epoch Locality Reference arrangement B. ardenicum Unknown Rhomboidal and spirally No data Acute Middle Jurassic England Harris 1979 B. castatum Unknown Scale-like and spirally Unkeeled Acute, obtuse Lower Cretaceous England Watson et al. 1987 or rounded B. baqueroense In different planes Scale-like and spirally No venation Acute, slightly Lower Cretaceous Argentina Traverso 1968 rounded B. brettii In one or more Rhomboidal and spirally No venation Rounded or Lower Cretaceous Argentina Archangelsky 1963 planes acute B. comancheanum Opposite or helical Scale-like, rhomboidal or oval, Keeled Acute Upper Triassic United States Ash 1999 helically arranged in a low spiral B. crassifolium Not informed Multiveined and spirally Keeled Acute Upper Cretaceous Netherlands Bosma et al. 2009 B. crucis Not informed Heteromorphic and spirally Convex Obtuse in Middle Jurassic England Kendal 1947; Harris 1979 general B. desnoyersii Not informed Pyamid-like and spirally Many keels Not informed Middle Jurassic England Kendal 1947 B. elegans Sub-opposite or Scale-like, decussately or Smooth Rounded to Lower Jurassic Greece Karakitsios et al. 2015 alternate almost decussately in a very slightly bluntly low spiral apiculate B. expansum Alternate Rhomboidal, inconspicuously Falciform Obtuse Middle Jurassic England Kendal 1949; Givulescu & Bucur spirally 1985 B. garciarum Not informed Scale-like, rhomboidal to Keeled and striated Mostly rounded Lower Cretaceous Argentina Carrizo et al. 2019 pyramidal and spirally B. hegewaldia Not informed Triangular and spirally Striated Sharp, Upper Triassic United States Ash 1973 acuminate B. irregulare Not informed Spirally No venation Rounded Lower Cretaceous Argentina Archangelsky 1963 B. kachaikensis Not informed Scale-like, rhomboidal or Not informed Acute Lower Cretaceous Argentina Passalia 2007 elogante and spirally B. lorchii Not informed Rhomboidal and spirally Keeled and striated Rounded, Upper Jurassic Israel Raab et al. 1986 typically aquiliform B. madagascariense Unbranched Rhomboidal and spirally Striated Acute Upper Jurassic Madagascar Barale & Appert 2007 B. mamillare Pinnate Rhomboidal and spirally Keeled and striated Obtuse or Middle Jurassic England Bancroft 1913; Kendal 1947; rounded Harris 1979 B. mirandai Not informed Spirally No venation, but Rounded or Lower Cretaceous Argentina Archangelsky 1963 keeled acute B. mucronatum In one Spirally No venation Acute Lower Cretaceous Argentina Archangelsky 1963 or more planes B. negevensis Not informed Rhomboidal and spirally Apparantly keeled Obtuse Lower Jurassic Israel Lorch 1968 B. ningshiaense Unbranched Scale-like and spirally Convex, keeled and Acute Lower Cretaceous China Du et al. 2013 striated B. obesum Opposite or sub- Scale-like with a rounded Convex and striated Acute with Lower Cretaceous Brazil and Japan Heer 1881; Saporta 1894; opposite base and spirally rounded tip Duarte 1985; Kunzmann et al. 2004; Batista et al. 2017 B. obtusum Unbranched Rhomboidal and scale-like Striated Obtuse Lower Cretaceous China Du et al. 2013 imbricate, spirally loosely arranged B. patens Unbranched Rhomboidal, multiveined and Convex, with some Obtuse Upper Cretaceous Netherlands van der Ham et al. 2003 spirally folds at the base and keeled at the apex B. porrigente Not informed Rhomboidal and spirally Not informed Rounded Lower Jurassic Israel Lorch 1968 B. pulcher Not informed Scale-like and spirally Striated Acute Lower Jurassic Israel Lorch 1968 B. tigrense In different planes Scale-like and spirally No venation Acute Lower Cretaceous Argentina Traverso 1966 B. scalbiensis Not informed Rhomboidal and spirally Keeled Acute Middle Jurassic England Kendal 1947 B. squamosum Regular branching Scale-like or rhomboidal and Striated Obtuse Upper Cretaceous Czech Republic and Raubeson & Gensel 1991; spirally southeastern United Kvaĉek 2007 States B. stemonium Irregular branching Spirally Not informed Rounded Middle Jurassic England Kendal 1947 B. vulgare Pinnate and sub- Rhomboidal and phyllotaxy Striated Mucronate Upper Cretaceous Japan Ohana & Kimura 1993 opposite or difficult to be determined alternate, B. sattlerae Opposite or rarely Rhomboidal or scale-like and Rugous Acute Lower Cretaceous Brazil This paper alternate almost decussately in a very low spiral Modified from Du et al. (2013).
TABLE 2. Micromorphological comparisons of Brachyphyllum species. See Table 1 for references. Species Leaf margins Stomatal arrangement Stomatal apparatus Guard cells Subsidiary Stomatal aperture Epidermal cells Hypoderm cells orientation B. ardenicum Not scarious, Longitudinal rows, except Monocyclic Sunken 4-6 Random Rectangular in longitudinal rows Present but with for the leaf margins and projections middle region of the surface B. castatum Scarious Scattered Monocyclic or dicyclic Sunken 5-12 Longitudinal or Square-shaped, rectangular or Present and oblique rounded, arranged randomly irregularly developed B. baqueroense Scarious Tending to form rows Monocyclic and imperfectly Not informed 4-6 Random, tending to Rectangular, isodiametric and Not informed dicyclic oblique polyhedral B. brettii Entire with Longitudinal rows Oval but occasionally Slightly 4-5 Random, tending Isodiametric Present distinct circular sunken to transverse projection of marginal cells B. comancheanum Scarious Longitudinal rows Monocyclic Sunken 6-8 Longitudinal rows Rectangular in leaf margins and Not informed polygonal or square-shaped in other areas B. crassifolium Entire Longitudinal rows Not informed Sunken 4-5 Random Elongate or isodiametric, Not informed between the stomatal rows B. crucis Scarious Scattered except for the Not informed Sunken 4-6 Random Rectangular in longitudinal rows Present middle region of the surface B. desnoyersii Not informed Somehow in rows Not informed Sunken 4-6 Random Rectangular with rounded Unknown corners in longitudinal rows B. elegans Almost Scattered along the leaf Monocyclic or almost Not informed 4-6 Not informed Isodiametric or elongate in leaf Not informed smooth margins amphycyclic margins B. expansum Scarious Spaced longitudinal rows Amphycyclic or haplocheilic Sunken 4-7 Unknown Isodiametric or elongate Present B. garciarum Entire longitudinal bands Monocyclic Sunken 4-8 Parallel to oblique Quadrangular Present to rectangular B. hegewaldia Not informed Scattered, except for leaf Not informed Sunken 4-6 Longitudinal Square-shaped or elongate, Not informed margins and base randomly arranged B. irregulare Microscopicall Irregularly Monocyclic or imperfectly Sunken 4-5 Random, tending to isodiametric, often somewhat Present y serrate dicyclic longitudinal rectangular, longitudinally elongated B. kachaikensis Scarious Scattered or in poorly Monocyclic Sunken 4-6 Random Isodiametric or rectangular in Present defined rows longitudinal rows B. lorchii Entire Well defined longitudinal Not informed Sunken 4-5 Not informed Isodiametric in longitudinal rows Not informed rows B. madagascariense Entire Well defined longitudinal Haplocheilic or monocyclic Slightly 4-6 Not informed Square-shaped, elongate or Present rows, except for leaf apex sunken diamond-shaped and margins B. mamillare Scarious close Longitudinal rows Amphycyclic or incompletely Sunken 2-4 Random Rectangular in longitudinal rows Present to the apex amphycyclic B. mirandai Microscopicall Scattered but sometimes Typically monocyclic or Sunken 4-5 Usually Slightly elongated, rectangular, Present y serrate forming short ill-defined imperfectly dicyclic longitudinally, but polygonal, sometimes longitudinal rows occasionally obliquely square and transversely B. mucronatum Microscopicall Rows ill-defined but more Typically monocyclic, Slightly 4-5 Frequently Isodiametric, transversely Present y serrate definite near midline of sometimes imperfectly sunken longitudinal elongated and rectangular lamina dicyclic B. negevensis Not informed Longitudinal rows Dicyclic Sunken 4-5 Not informed Rectangular or isodiametric Not informed B. ningshiaense Entire Longitudinal rows, except Haplocheilic, round, elliptic Sunken 6-9 Longitudinal to Rectangular, pentagonal or Not informed for leaf margins or narrowly elliptic oblique rhomboidal, isodiametric B. obesum Scarious Longitudinal rows on the Monocyclic or incompletely Sunken 4-6 Mainly transversal, Isodiametric in longitudinal rows Not informed whole leaf surface amphycyclic but occasionally oblique or longitudinal B. obtusum Not informed Longitudinal rows, except Round or elliptical Sunken 7-11 Random Obliquely rectangular, Not informed for leaf margins pentagonal or rhomboidal; longitudinal and isodiametric B. patens Not informed Scattered, except for leaf Dicyclic Sunken 4-6 Longitudinal to Isodiametric Present margins oblique B. porrigente Smooth Well marked longitudinal Monocyclic or rarely Sunken 4-5 Oblique Often wider than long, arranged Present rows amphycyclic in rows B. pulcher Scarious Poorly defined longitudinal Elliptical Sunken 5-6 Random Rectangular or square-shaped, Present rows in rows B. tigrense Sometimes Scattered, except for leaf Monocyclic and imperfeictly Slightly 4-6 Random, tending to Isodiametric or rectangular Present scarious margins and base dicyclico sunken oblique B. scalbiensis Scarious Very spaced longitudinal Monocyclic Sunken 4-5 Random or Rectangular or irregular, in Present, rows longitudinal longitudinal rows sclerified B. squamosum Scarious Longitudinal rows Monocyclic or incompletely Slightly 4-6 Random or Square-shaped or polygonal, in Not informed dicyclic sunken perpendicular rows B. stemonium Smooth Spaced longitudinal rows Not informed Sunken 4-6 Unknown Almost square-shaped in Present longitudinal rows B. vulgare Entire Longitudinal rows haplocheilic or monocyclic Sunken 4-6 Random or Isodiametric or rectangular in Present, but longitudinal longitudinal rows sparce B. sattlerae Scarious Longitudinalrows on the Monocyclic Sunken 4-6 Oblique Elongated rectangular or Present and leaf surface, but scarce at square-shaped at the leaf base heavily lignified the leaf base and absent or near the margins close to the leaf margins Modified from Du et al. (2013).