Content uploaded by Ana Andruchow Colombo
Author content
All content in this area was uploaded by Ana Andruchow Colombo on Jul 11, 2018
Content may be subject to copyright.
American Journal of Botany 105(6): 1–21, 2018; http://www.wileyonlinelibrary.com/journal/AJB © 2018 Botanical Society of America • 1
e conifer family Araucariaceae has been identied in the fos-
sil record at least since the Jurassic (Stockey and Taylor, 1978b;
Stockey, 1982, 1994; Kershaw and Wagsta, 2001; Panti et al.,
2012). However, remains referred to the family have been reported
since as early as the Late Triassic (Lele, 1956; Axsmith and Ash,
2006), although these may represent an araucariaceous stem group
(Kunzmann, 2007). During the Mesozoic, the family had a world-
wide distribution, but its dominance in paleoecosystems started to
decline during the Cretaceous. By the beginning of the Paleocene,
Araucariaceae became restricted to South America, Australia,
Antarctica, and New Zealand (Berry, 1908; Whitmore and Page,
1980; Dettman and Cliord, 2005). Today, the family comprises
three genera, Araucaria, Agathis, and Wollemia, restricted to
the southwest Asia- Western Pacic regions, and South America
(Seward and Ford, 1906; Berry, 1908; Florin, 1963; Farjon, 2010).
is disjunct distribution of extant Araucariaceae and its present
low species diversity, in contrast with its higher species diversity in
the past, lead to the hypothesis that these extant taxa are relictual
(Stockey, 1982; Kershaw and Wagsta, 2001).
Araucariaceae comprise trees reaching from 10 to 90 m in
height, although the most common mature height is around 50
m (Farjon, 2010). Agathis and Wollemia have been recovered as a
Araucaria lepanensis (Araucariaceae), a new species with
dimorphic leaves from the Late Cretaceous of Patagonia,
Argentina
Ana Andruchow-Colombo1,3 , Ignacio H. Escapa1, N. Rubén Cúneo1, and María A. Gandolfo2
RESEARCH ARTICLE
Manuscript received 27 February 2018; revision accepted 11 April
2018.
1 Consejo Nacional de Investigaciones Cientícas y Técnicas
(CONICET),Museo Paleontológico Egidio Feruglio (MEF), Av.
Fontana 140, 9100 Trelew, Chubut, Argentina
2 L. H. Bailey Hortorium,Plant Biology Section,School of
Integrative Plant Science,Cornell University, 410 Mann Library
Building, Ithaca, NY 14853, USA
3 Author for correspondence (e-mail: aandruchow@mef.org.ar)
Citation: Andruchow-Colombo, A., I. H. Escapa, N. R. Cúneo,
and M. A. Gandolfo. 2018. Araucaria lefipanensis (Araucariaceae),
a new species with dimorphic leaves from the Late Cretaceous of
Patagonia, Argentina. American Journal of Botany 105(6): 1–21.
doi:10.1002/ajb2.1113
PREMISE OF THE STUDY: We describe a new araucarian species, Araucaria lepanensis, from
the Late Cretaceous ora of the Lepán Formation, in Patagonia (Argentina) based on
reproductive and vegetative remains, with a combination of characters that suggest mosaic
evolution in the Araucaria lineage.
METHODS: The studied fossils were found at the Cañadón del Loro locality. Specimens were
separated into two leaf morphotypes, and their morphological dierences were tested with
MANOVA.
KEY RESULTS: The new species Araucaria lepanensis is erected based on the association of
dimorphic leaves with cuticle remains and isolated cone scale complexes. The reproductive
morphology is characteristic of the extant section Eutacta, whereas the vegetative organs
resemble those of the sections Intermedia, Bunya, and Araucaria (the broad- leaved clade).
CONCLUSIONS: The leaf dimorphism of A. lepanensis is similar to that of extant A. bidwillii,
where dimorphism is considered to be related to seasonal growth. The leaf dimorphism in
A. lepanensis is consistent with the paleoclimatic and paleoenvironmental reconstructions
previously suggested for the Lepán Formation, which is thought to have been a seasonal
subtropical forest. The new species shows evidence of mosaic evolution, with cone scale
complexes morphologically similar to section Eutacta and leaves similar to the sections of the
broad- leaved clade, constituting a possible transitional form between these two well- dened
lineages. More complete plant concepts, especially those including both reproductive and
vegetative remains are necessary to understand the evolution of ancient plant lineages.
This work contributes to this aim by documenting a new species that may add to the
understanding of the early evolution of the sections of Araucaria.
KEY WORDS Araucaria; Araucariaceae; Argentina; Cañadón del Loro; Cretaceous; leaf dimor-
phism; Lepán Formation; Maastrichtian; mosaic evolution; Patagonia.
2 • American Journal of Botany
monophyletic group (i.e., ‘Agathioid’ clade, Escapa and Catalano,
2013) in most recent morphological, molecular, and combined phy-
logenetic analyses (Gilmore and Hill, 1997; Kunzmann, 2007; Rai
etal., 2008; Codrington etal., 2009; Liu et al., 2009; Escapa and
Catalano, 2013; contra Setoguchi etal., 1998). e agathioid clade is
morphologically distinctive, with seed cones bearing numerous spi-
rally arranged scales, which are interpreted as the ovuliferous scale
completely fused to the bract (Florin, 1951; Hyland, 1978; Stewart
and Rothwell, 1993; Chambers etal., 1998). Each cone scale bears
one free inverted seed. In Wollemia the seed is circumferentially
winged, whereas in Agathis it has two asymmetrical lateral wings
(Dickson, 1863; Hyland, 1978; Whitmore, 1980; Chambers etal.,
1998; Farjon, 2010). ese two genera are also easily distinguished
from Araucaria by dierences in leaf morphology and anatomy
(Chambers etal., 1998). Wollemia has opposite/decussate, sessile,
linear leaves with slightly revolute margins, whereas Agathis has
subopposite to opposite phyllotaxy and short- petiolate leaves with
broad, at blades (de Laubenfels, 1978, 1979; Page, 1990; Farjon,
2010).
e genus Araucaria includes 20 modern species classied in
four sections, originally erected based solely on morphological
characters of the extant species (Wilde and Eames, 1952). Araucaria
section Araucaria (=Columbea Endlicher emend. Wilde and Eames,
1952) includes the two South American species, A. araucana
(Molina) K.Koch and A. angustifolia (Bertol.) Kuntze. In addition,
there are two monotypic sections: Araucaria section Intermedia
White (1947) that includes Araucaria hunsteinii K.Schum., con-
ned to Papua New Guinea, and Araucaria section Bunya Wilde
and Eames (1952) that contains Araucaria bidwillii Hook., which
is restricted to disjunct locations in southeastern and northeastern
Queensland, Australia. Finally, Araucaria section Eutacta Endlicher
(1842) includes A. cunninghamii Mudie from New Guinea and
Queensland, Australia, A. heterophylla (Salisb.) Franco native to
Norfork Island National Park, Australia, and 14 New Caledonian
endemic species (Florin, 1963; Enright, 1995; Enright etal., 1995;
Farjon, 2010; Mill etal., 2017). e genus Araucaria has two dis-
tinct leaf morphologies: (1) sessile, imbricate, usually erect and rel-
atively small leaves persistent on falling branches that are typical of
the Araucaria section Eutacta; and (2) sessile leaves with broad, at
lamina and acute apices that are characteristic of Araucaria sections
Araucaria, Intermedia, and Bunya (Chambers etal., 1998; Stockey,
1982; Farjon, 2010). All Araucaria species (both extant and fossil)
have ovuliferous cones with spirally arranged seed complexes, each
bearing a single, inverted, central seed embedded in scale tissues
(Eames, 1913; Wilde and Eames, 1948; de Laubenfels, 1972; Page,
1990; Stockey, 1994; Farjon, 2010). Also, they all have a ligule at the
distal portion of the cone scale complex right over the chalazal end
of the seed, which is interpreted to be the free distal end of the ovu-
liferous scale (Eames, 1913; Wilde and Eames, 1948; Florin, 1951;
de Laubenfels, 1988; Stewart and Rothwell, 1993; Stockey, 1994;
Farjon, 2010). However, the morphology of the cone scale complex
is variable among sections. Araucaria section Araucaria has nut-
like diaspores with non- vascularized, extremely reduced lateral ex-
pansions (Carrière, 1855; Seward and Ford, 1906; Wilde and Eames,
1952; Haines, 1983a; Farjon, 2010). Araucaria section Intermedia
produces samara- like complexes that are fan- shaped and have
laterally expanded, vascularized, papery- thin wings (Seward and
Ford, 1906; Wilde and Eames, 1952; Haines, 1983a; Farjon, 2010).
Araucaria section Eutacta has samara- like ovulated complexes with
wings that are well developed, papery thin, and not vascularized
(Carrière, 1855; Seward and Ford, 1906; Wilde and Eames, 1952;
Haines, 1983a; de Laubenfels, 1972, 1988; Farjon, 2010). Araucaria
section Bunya produces cone scale complexes with large, heavy,
vascularized, woody wings (Carrière, 1855; Seward and Ford, 1906;
Wilde and Eames, 1952; Haines, 1983a; Farjon, 2010).
Although there is extensive information on fossil forms within
Araucariaceae, only few fossil species are dened based on associ-
ated vegetative and reproductive organs (e.g., Kendall, 1949; Harris,
1979; Del Fueyo, 1991; Ohsawa etal., 1995; Wilf etal., 2014). Such
organismal concepts are crucial for the development of more stable
phylogenetic studies. Herein, we describe a new species based on
associated reproductive and vegetative araucarian fossil remains col-
lected at the Cañadón del Loro locality from the Upper Cretaceous
Lepán Formation that crops out at the Chubut Province, Patagonia,
Argentina. We also discuss the implications of these new records on
the evolution of the genus during the last part of the Mesozoic Era.
MATERIALS AND METHODS
Geologic setting
e Lepán Formation belongs to the Cañadón Asfalto Basin and
crops out at the Chubut River middle valley, near Paso del Sapo
village, NW Chubut Province, Patagonia, Argentina (Fig. 1A).
e entire unit was deposited during the Maastrichtian (Late
Cretaceous)–Danian (Paleocene) in a tide- dominated deltaic set-
ting (Scasso etal., 2012).
e age of the Lepán Formation is constrained by biostrati-
graphic proxies, i.e., marine faunas, terrestrial palynomorphs and
dinoagellates. In the rst case, bivalves, gastropods, amonoids, de-
capods, and corals initially dened the Maastrichtian- Danian time
span of deposition (Medina etal., 1990; Olivero etal., 1990; Medina
and Olivero, 1994; Kiessling etal., 2005). is age was conrmed by
terrestrial pollen and spore assemblages (Baldoni, 1992), and more
recently and in more detail by Barreda etal. (2012), who showed a
clear Maastrichtian- Danian transition associated to dinoagellates
(see also Vellekoop etal., 2017).
A highly diverse paleoora has been recovered from
Maastrichtian localities of the Lepán Formation located south of
the Chubut River (Fig.1A); the local assemblages are dominated
by angiosperms with lower proportion of gymnosperms and ferns
(Cúneo etal., 2008). From the same Maastrichtian localities, paly-
nological studies have shown a rich fern- angiosperm association,
with gymnosperms (mostly podocarps) as a frequent element
(Barreda etal., 2012).
e material here studied comes from the Cañadón del Loro
locality, located north of the Chubut River (see Fig.1A). e plant-
bearing sediments of Cañadón del Loro locality are stratigraphi-
cally below the localities from the south of the Chubut River. In
this section, the lower part of the Lepán Fm. has more terrestrial
sedimentary features, including well- developed paleosols and asso-
ciated coaly layers, and probably represents a more proximal (fresh
water dominated) location in the regional deltaic system. Based on
the palynological content of nearby and stratigraphic equivalent
sections (Barranca de los Perros locality, Baldoni and Askin, 1993),
the age of the lower Lepán Fm. at the Cañadón del Loro locality is
estimated to be Maastrichtian (Late Cretaceous).
Four fossiliferous horizons were identied at the Cañadón del
Loro locality (Fig.1B), all of them highly prolic in yielding fossil
2018, Volume 105 • Andruchow- Colombo etal.—Late Cretaceous Araucaria lefipanensis from Patagonia • 3
plants. In particular, Level 4 (Fig. 1B) has produced most of the
araucarian remains herein studied. Associated with this level, two
quarries were excavated: 4A and 4B. Level 4A is nearly 1 m thick,
and it is dominated by angiosperms, while Level 4B (La Huella) is
strongly dominated by the araucarian leaves and seed complexes
here described. Level 4B is 15 cm thick with a highest fossil con-
centration layer of 7 cm and underlies a sand level with two types
of dinosaur footprints. Interestingly, the best- preserved specimens
of Level 4B were found immediately below the footprints. Level 4A
yields, in addition to the araucarian material, a diverse angiosperm
assemblage and fern remains, as well as leafy branches and isolated
cone scale complexes of another type of conifer. is second conifer
shows anity to Cupressaceae, comprising multi- seeded cone scale
complexes with seeds positioned distally and needle- like leaves. e
cupressaceous conifer was also found at the other three fossilifer-
ous levels represented by both leafy branches and cone scale com-
plexes in clear association. e levels where the described fossils
come from comprised by clayey siltstones, suggesting a low- energy
depositional environment (N. R. Cúneo, personal observation)
that allowed the preservation of delicate structures such as epider-
mal patterns of the leaves and the papery wings of the cone scale
complexes.
Fossil preparation and illustration
e fossil remains are preserved as impressions and compressions
in clayey siltstones, occasionally with cuticular remains or some
epidermal patterns impressed on the sedimentary surface. Fossils
were prepared using standard mechanical techniques; macroscopic
images of the specimens were taken with a Canon EOS 7D camera
and a Canon EF- S 60 mm macro lens (Canon Corp., Melville, NY,
USA) under halogen lighting projected at dierent angles to max-
imize observation of venation details (Kerp and Bomeur, 2011).
e description of epidermal patterns is based on in situ leaf
cuticlular remains, cuticles extracted by bulk maceration (to ob-
tain additional specimens), and observation of leaf impressions
with no cuticle preserved but with retained impression of cellu-
lar details. Scanning electron microscope images were taken with
a low vacuum scanning electron microscope (LVSEM) at Aluar
Aluminio Argentino (Puerto Madryn, Chubut Province, Patagonia,
Argentina).
Images obtained were processed with Photoshop Lightroom 5
(Adobe, San José, CA, USA) for exposure and white balance and
with Photoshop CS5 (Adobe) for focus stacking (Bercovici etal.,
2009) and plate assemblage. All specimens are housed at the
Paleobotanical Collection of the Museo Paleontológico Egidio
Feruglio, Trelew, Chubut Province, Patagonia, Argentina (hereaer
MPEF- Pb).
Statistical analyses
For testing the signicance of dierences between two morpholog-
ical groups in a set of leaf morphological characters a multivariate
analysis of variance (MANOVA) was applied. Four morphological
variables (leaf length, leaf maximum width, apex angle, and dis-
tance between the leaf base and its maximum width) were selected
as dependent variables and the shape group (ovate- lanceolate or
lanceolate, see Results) was set as main factor.
Univariate normality was tested for each variable with Shapiro–
Wilks tests and with graphic approaches (error frequency histo-
grams and QQ- Plots). Multivariate normality (MVN) was tested
with two analytical methods: Mardias’s and Royston’s MVN
test, according to recommendations of Korkmaz et al. (2014).
Homogeneity of variance–covariance matrices were veried with
Box’s M- test (Box, 1949). e statistic regarded for conrmation
or rejection of the null hypothesis was Pillai’s trace (Pillai, 1955;
FIGURE 1. Geologic map and stratigraphic section. (A) Geologic map of study area (modied from Ruiz, 2007), Cañadón del Loro locality (Chubut
Province, Argentina) marked with black star. (B) Partial stratigraphic section of lower portion of Lepán Formation at Cañadón del Loro locality.
0246
Km
Ruta 13
PrR Nuta o . 12 v
70°O 69°55’O 69°50’O 69°45’O
42°35’S
42°40’S
42°45’S
Settlement
Alluvial fan
Ephemeral river
River
Lonco Trapial
Group
(Alvar Andesites)
Fm
Paso del Sapo
Fm
Lefipán
Fm
Collún Curá
Fluvial
Terrace
deposits
Recent
deposits
Complejo
Volcánico-
Piroclástico
del Río
Chubut Medio
Ju ra s s ic
Maas t ric ht ian /
n nDa ia
te eo n eLa P al ce /
Eoc n ee
o t M o eneP s - i c
Neo ge n e
Mi c eo e n
Pto. Don Manuel
. T mQ de a o al
Pto. San Martín
Est. Don Felix
Ea. Don Manuel
Ex Ea. Cretton Ea. San Ramón
Ea. dePirola Crett
Barda de los Perros
Cañadon del Loro
E l a CQ. C i c i o arrz l h
Stratigraphic Units
Study area
REFERENCES
Mass Wastings
BA
5m
REFERENCES
NF1
Tabular cross-bedding
Through cross-bedding
Swaley cross-bedding
Parallel lamination
Heterolithic bedding
Bioturbation
Coal
NF4
NF3
NF2
4 • American Journal of Botany
Olson, 1974). We considered a level of signicance of 95% (α =
0.05). All analyses were performed in R environment (R Core Team
2016), using stats (R Core Team 2016), biotools (da Silva, 2017),
MNV (Korkmaz etal., 2014), lattice (Sarkar, 2008), psych (Revelle,
2016), Hmisc (Harrell and Dupont, 2016), MASS (Venables and
Ripley, 2002), and mvoutlier (Filzmoser and Gschwandtner, 2018)
packages.
e analyzed data set and the correspondent R script are avail-
able in Appendices S1 and S2 (see the Supplemental Data with this
article).
RESULTS
e results of the MANOVA show signicant dierences between
the ovate- lanceolate and lanceolate leaf shape groups (F4, 9 = 22.08;
P < 0.0005). erefore, subsequently, both leaf types were treated
separately along the study. Nevertheless, these two leaf morphol-
ogies are assumed to belong to a single dimorphic species (see
Discussion).
Systematic palaeontology
Family—Araucariaceae Henkel and Hochst., 1865
Genus—Araucaria de Jussieu, 1789
Type species—Araucaria araucana (Molina) K.Koch, 1873
Species—Araucaria lefipanensis sp. nov. Andruchow Colombo,
Escapa, Cúneo & Gandolfo
(Figs.2–6; Appendices S3 and S4, see Supplemental Data)
Etymology—e specic epithet refers to the Lepán Formation
where the type material of this species was collected.
Holotype—MPEF- Pb 8297 (Fig 2A). Leafy branch. Level 4,
Cañadón del Loro locality, Lepán Formation, Cañadón Asfalto
Basin, Chubut Province, Argentina.
Paratypes—Leafy branches. MPEF- Pb 5799, 5821, 5825, 5827,
8285, 8287- 8288, 8291, 8294- 8300, 8303- 8306, 8311, 8314, 8316-
8318, 8320, 8321, 8323, 8325, 8327, 8328, 8333, 9210- 9213, 9216,
9219, 9221, 9223, and 9229. Isolated leaves. MPEF- Pb 5817, 5818,
8286- 8287, 8289- 8290, 8292- 8294, 8299, 8308, 8310, 8312, 8315,
8319, 8326, 8329- 8330, 8332, 9214- 9215, 9217- 9218, 9220, 9222,
9224- 9228, 9230- 9248, and 9250. Cuticle remains. MPEF- Pb 8331-
8332. Cone scale complexes. MPEF- Pb 5810, 5826, 8299, 8301,
8307, 8309, 8313, 8322, and 9252- 9272.
Geographic occurrence—Cañadón del Loro, Chubut Province,
Argentina
Stratigraphic occurrence—Levels 3 and 4, lower Lepán Formation
(Maastrichtian), Cañadón Asfalto Basin
Diagnosis—Shoots bearing helically arranged, imbricated leaves;
leaves dimorphic, multiveined, sessile, with entire margin and acute
apex, lanceolate to ovate- lanceolate, abaxially keeled, 11.3–35.3 mm
long, 4.7–12.4 mm wide. Stomata arranged in parallel discontinuous
rows aligned with major axis of the leaf; stomatal apparatuses with
ovate contour, four to ve subsidiary cells. Cone scale complexes
heart- shaped, length 14.9–18.3 mm, maximum width 11.5–20.0
mm, ligulate, with a bract tip; central body of complex cuneate in
outline, woody in appearance and with longitudinal striations; lat-
eral wings thin and slightly asymmetric; each complex bearing a
single central inverted seed; seed 8.7–10.9 mm long, 4.2–5.9 mm
wide.
Description—e vegetative remains are represented by impres-
sions and compressions of foliar branches (Figs.2 and 3) and of
isolated leaves (Fig.4). Several specimens are three- dimensionally
preserved, and so the arrangement of the leaves on the branches is
perceivable (Figs.2 and 3).
Leaves—Foliar branches are up to 7.8 cm wide, including leaves
(Fig.2A). Leaves usually cover the entire central axis, although in a
few specimens the leaves are only partially preserved and a portion
of the central axis can be observed (Fig.2D, 2E). Twigs are straight,
up to 3.9 mm wide (mean: 3.0, SD: 0.8 mm, n: 3), and bear spirally
arranged leaves showing helical phyllotaxy (Figs.2A–F, 3A–D). e
leaves are highly imbricated with a degree of superposition varying
between 15–70% (mean: 41%, SD: 20%, n: 9, Figs.2, 3) and show an
insertion angle of 26–63º (mean: 40.8°, SD: 10.2º, n: 12, Fig.2A,E).
At the apical region of the foliar branches, the leaves are densely
packed with small leaf insertion angles, resulting in a drop- like
structure (Fig.2B).
Two slightly dierent leaf morphologies were identied, which
were labeled as “lanceolate” and “ovate- lanceolate” shape groups
(L- shaped and O- shaped groups respectively), there are also leaves
with intermediate morphologies between L- and O- shape groups
(Appendix S4).
e O- shaped group includes, as indicated by its name, ovate-
lanceolate leaves (Figs.2C–E, 3B, C, 4C–E, G, H), with entire mar-
gin and acute apex (its angle varies between 31.3° and 53.4°, mean:
39.6°, SD: 7.7°, n: 9; Fig.4E, F). e leaves are thick in appearance
(Figs.3C, 4G, H). Leaf length is 11.3–22.3 mm (mean: 17.5 mm, SD:
3.9 mm, n: 9), and its maximum width is 4.7–12.7 mm (mean: 8.9
mm, SD: 2.5 mm, n: 9). e width/length ratio is 0.3–0.7 (mean: 0.5,
SD: 0.1, n: 9), and the distance between the leaf base and the max-
imum width represents a 15–33% of the leaf length (mean: 21%,
SD: 5%, n: 9). ese leaves are sessile (Figs.2D, E, 4C, D, G, H),
have 55–68 parallel veins that maintain the same caliber through
all of the length (Figs.3C, 4D, E), and have a central abaxial keel
extended from the base to the apex; the leaves are oen folded over
the keel when found on the branches (Figs.2C, 3C).
e L- shaped group comprises lanceolate leaves (Figs.2A, 2B,
2F, 3A, 3D, 4A, 4B, 4F), which are also thick in appearance (Figs.2A,
2B, 2F, 3A, 3D) and have entire margins and acute apices (apex angle
varies between 19 and 38.9°, mean: 27.7°, SD: 7.2°, n: 8; Fig.4A, 4B).
e leaf length is 19.5–35.3 mm (mean: 28.2 mm, SD: 5.2 mm, n: 8),
although one specimen exhibited one leaf 47.0 mm long; leaf maxi-
mum width is 6.3–12.4 mm (media: 8.6 mm, SD: 2.3 mm, n: 8). e
width/length ratio uctuates between 0.2 and 0.4 (mean: 0.3, SD:
0.1, n: 8), and the distance between the leaf base and its maximum
width represents a 16–35% of the leaf length (mean: 21%, SD: 7%,
n:8). e leaves have a central abaxial keel that extends from the
base to the apex (Fig.3A, D), and when found on the branches, the
leaves are oen folded over the keel (Figs.2A, B, F, 3A, D); 21–46
veins have been counted or estimated (Figs.2A, B, F, 3A, D, 4F).
2018, Volume 105 • Andruchow- Colombo etal.—Late Cretaceous Araucaria lefipanensis from Patagonia • 5
FIGURE 2. Leafy shoot diversity of Araucaria lepanensis sp. nov. (A, B, F) L- shaped group. (C–E) O- shaped group. (A) Holotype MPEF- Pb 8297. (B)
MPEF- Pb 8288 apical zone of a leafy shoot; abaxial keel of lower leaf indicated by arrowhead. (C) MPEF- Pb 8327, abaxial keel of lower leaf indicated
by arrowhead. (D) MPEF- Pb 8316, general view of specimen showing portions of the naked branch. (E) MPEF- Pb 8316, detail of detached leaf base,
indicated by arrowhead. (F) MPEF- Pb 8311. Scale bars A–D, F = 10 mm; E = 5 mm.
6 • American Journal of Botany
Isolated leaves of both morphological groups show several types
of preservation at their bases (Fig.4). Some of these leaves clearly
show the leaf concave base (Fig.4A–D, G), while others appear to
have decorticated their branch when they detached (Fig.4D, F–H).
Cuticular patterns—A few leaves of both morphological groups
preserve epidermal patterns found as impressions on the rock
(Fig.4D,E). Several stomatal rows parallel to the leaf axis and oc-
curring between adjacent veins were found (Fig.4D, E). Stomatal
apparatuses are ovate in outline (Fig.4E). Also a few specimens, of
both shape groups, preserve remains of carbonized cuticle on the
leaves, which show similar features to those described below for
bulk maceration specimens.
Cuticular fragments obtained from bulk maceration (Fig. 5)
show stomata arranged in discontinuous parallel rows (Fig.5A, F),
which are oriented mostly parallel to slightly oblique to the long
axis of the leaf (Fig.5A, B, F), while perpendicular orientations are
rare or absent. On the external cuticle epidermal cells outlines are
FIGURE 3. Leafy shoot diversity of Araucaria lepanensis sp. nov. (A, D) L- shaped group. (B, C) O- shaped group. (A) MPEF- Pb 8296; arrowhead indicates
zone with evident parallel venation. (B) MPEF- Pb 8291; arrowhead indicates abaxial keel. (C) MPEF- Pb 9223, transverse section of a leafy shoot show-
ing the spirally arranged leaves. (D) MPEF- Pb 8328. Scale bars = 10 mm.
2018, Volume 105 • Andruchow- Colombo etal.—Late Cretaceous Araucaria lefipanensis from Patagonia • 7
FIGURE 4. Isolated leaf diversity with varying abscission zones of Araucaria lepanensis sp. nov. (A, B, F) L- shaped group. (C–E, G, H) O- shaped group.
(A) MPEF- Pb 8310. (B) MPEF- Pb 8329. (C) MPEF- Pb 8308. (D) MPEF- Pb 8287, general view. (E) MPEF- Pb 8287, leaf detail showing venation and stomatal
discontinuous rows. (F) MPEF- Pb 8319. (G) MPEF- Pb 9230. (H) MPEF- Pb 9233. Scale bars A–D, F–H = 5 mm; E = 2.5 mm.
8 • American Journal of Botany
FIGURE 5. Cuticles of Araucaria lepanensis sp. nov. under LVSEM, MPEF- Pb 8331 h III and IV; A–E, MPEF- Pb 8331 h III; F, G, MPEF- Pb 8331 h IV. (A)
Middle portion of one cuticular fragment showing several stomatal rows and epidermal cell rows. (B–G) Detail of dierent stomata showing the typical
morphology with four subsidiary cells, two lateral and two polar. (B) Stomata showing polar extensions. (E) Detail of the granulose cuticle that extends
into the stomatal aperture. (F) Detail of a stomatal row and surrounding epidermal cells. (G) Detail of the rst stoma of the previous image, one of the
few stomata showing ve subsidiary cells, three lateral and two polar. Abbreviations: ec, epidermic cell; er, external ridge; fg, anges among guard
cells; fgs, anges between guard and subsidiary cells; gc, guard cell; ls, lateral subsidiary cell; pe, polar extensions; pr, polar ridge; ps, polar subsidiary
cell. Scale bar A = 100 μm; B, C, F = 50 μm; D, E, G = 10 μm.
2018, Volume 105 • Andruchow- Colombo etal.—Late Cretaceous Araucaria lefipanensis from Patagonia • 9
obscure and stomatal plugs were not observed. Internally, cuticles
show from two to ve epidermal cells (Fig.5F) separating adjacent
stomata in a row, and between ve and 11 rows of normal epidermal
cells between stomatal rows (Fig.5A–C, F). Stomatal apparatuses
are rounded to polygonal in outline (Fig.5B–D, F–G), 63.9–90.8μm
long (mean: 77.7 μm, SD: 9.0 μm, n: 12), and 37.0–75.3μm wide
(mean: 55.6 μm, SD: 8.9 μm, n: 12). Stomatal size (only considering
the guard cells) ranged between 26.2–36.8 μm (mean: 32.1 μm, SD:
4.1 μm, n: 6) long and between 14.1–21.4 μm (mean: 18.5 μm, SD:
2.9 μm, n: 6) wide. Four subsidiary cells are common (two lateral
and two polar, Fig.5B–D). One stomatal apparatus with ve sub-
sidiary cells was observed (Fig. 5G), in which the h subsidiary
cell appears to be the consequence of a lateral subsidiary cell divi-
sion, due to its position (Fig.5G). Outer anges of subsidiary cells
are uniformly thickened in both lateral and polar subsidiary cells
(Fig.5B, G). Subsidiary cell cuticle surface appears to be rugose and
sometimes granulose (Fig. 5G). Flanges between guard cells and
subsidiary cells are thick and irregular to smooth in appearance
(Fig.5D, G). Cuticle on guard cells surface appears to be granular
in texture (Fig.5G). e ange between guard cells is also gran-
ular, with—in some cases—pronounced pointed polar extensions
that show a middle polar ridge (Fig.5B, 5E, 5G). Epidermal cells
are generally rectangular, although polygonal cells are common
(Fig.5F). e epidermal cells within stomatal rows measure 8.9–
20.6 μm (mean: 14.9 μm; SD: 4.5 μm; n: 7) wide and 17.4–27.5 μm
(mean: 24.1 μm; SD: 3.5; n: 7) long; while epidermal cells between
stomatal rows measure 11.5–18.0 μm (mean: 14.7 μm, SD: 2.8; n:5)
wide and 23.4–31.0 μm (mean: 26.2 μm; SD: 3.4 μm; n:4) long.
Epidermal cell anges seem to be thick and straight at both LVSEM
and epiuorescence light microscopy (Fig.5F).
Reproductive organs—Isolated cone scale complexes are cuneate to
heartshaped (Fig.6B–F), 14.9–18.3 mm (mean:16.7mm, SD: 1.3,
n:7) long; their minimum width, located at the base of the cone scale
complex, is 2.2–7.2 mm (mean:4.4mm, SD: 1.9 mm, n: 7), and their
maximum width is 11.5–20.0 mm (mean: 15.2 mm, SD: 3.3, n: 8).
e maximum width is localized at the distal zone of the cone scale
complex, approximately at two thirds of its total length (Fig.6B–F).
e apex of the bract is mucronate, and the length of the bract tip is
1.8–2.7 mm (mean: 2.1 mm, SD: 0.5 mm, n: 3; Fig.6B,E). e cen-
tral body of the complex has a cuneate outline, with a distal widen-
ing adjacent to the end of the lateral wings, it is woody in appearance
FIGURE 6. Isolated cone scale complexes of Araucaria lepanensis sp. nov. (A) MPEF- Pb 8307. (B) MPEF- Pb 8322. (C) MPEF- Pb 8313. (D) MPEF- Pb 9252.
(E) MPEF- Pb 5826. Abbreviations: bt, bract tip; l, ligule; mi, micropyle; s, seed; w, cone scale complex wing. Scale bar A = 10 mm; B–F = 5 mm.
10 • American Journal of Botany
and has longitudinal striations (Fig. 6B, 6.4–6). e lateral wings
are slightly asymmetric and thin with a membranous appearance
(Fig.6B, D–F), their maximum width varies between 1.6–3.3 mm
(mean: 2.5 mm, SD: 0.6 mm, n: 8). Each complex bears only one
central, inverted seed that occupies a high proportion of the central
body surface (Fig.6B–F). Seed length varies between 8.7–10.9 mm
(mean: 9.9, SD: 0.8 mm, n: 7), and its maximum width between 4.2–
5.9 mm (mean: 4.9 mm, SD: 0.6 mm, n: 8). At the adaxial surface of
some of the complexes, a ligule can be distinguished immediately
distal the chalazal end of the seed (Fig.6B, C, F).
DISCUSSION
Taxonomic assignment and comparisons
Araucaria lefipanensis is assigned to the genus Araucaria
(Araucariaceae) based on numerous reproductive and vegetative
characters such as single- seeded cone scale complexes with well-
developed wings, and broad, multiveined, ovate- lanceolate to
lanceolate leaves with parallel- oriented stomata arranged in discon-
tinuous rows.
Both leaves and cone scale complexes show enough diagnostic
characters to be independently assigned to Araucaria, and although
these two types of organs were not found in organic connection,
they occur intimately associated at the same level. is close associ-
ation is especially strong in the quarry 4B (La Huella, see Materials
and Methods) where the araucarian reproductive and vegetative
remains—obtained from a 7 cm layer—strongly outnumbered all
other taxa. Furthermore, both organs are characterized by diagnos-
tic araucarian features, while no other remains found at any level
of the Cañadón del Loro locality, nor in any other locality of the
Lepán Formation, show araucarian anities. us, we propose
that both organs were produced by the same plant, and conse-
quently, the denition of Araucaria lefipanesis is based on dimor-
phic leaves and cone scale complexes.
e araucarian anity of the leafy shoots is supported by mac-
romorphological characters such as the helical phyllotaxy and the
presence of sessile, keeled, multiveined leaves with an ovate to
lanceolate outline (Carrière, 1855; Seward and Ford, 1906; Wilde
and Eames, 1952; de Laubenfels, 1988; Page, 1990; Farjon, 2010).
Besides, when leaves are found isolated, their bases are not always
noticeable, since in many specimens leaves appear to have detached
together with part of the branch cortex (Fig.4). ese dierences
in leaf base preservation suggest that A. lefipanensis lacked a mech-
anism of natural dehiscence, in agreement with what is observed
among the extant members of the genus Araucaria (de Laubenfels,
1988; Page, 1990; Farjon, 2010), which retain their leaves even on
old branches and trunks. e placement of these remains within
Araucaria is strongly supported by numerous cuticular features as
well. Among them, the arrangement of the stomata in discontinu-
ous rows, their predominantly parallel orientation respect with the
leaf major axis, the presence of 4–5 subsidiary cells, and the pres-
ence of polar extensions (Stockey and Taylor, 1978a; Stockey and
Ko, 1986).
Other conifer genera that produce leaves comparable to A.
lefipanensis are Nageia (Podocarpaceae), Agathis and Wollemia
(Araucariaceae), as they all produce broad, multiveined leaves
(Seward and Ford, 1906; de Laubenfels, 1969, 1972, 1988;
Page, 1990; Farjon, 2010). Nevertheless, Wollemia possesses
strap- shaped leaves with rounded apices (Chambers etal., 1998;
Farjon, 2010) and has stomata with usually six subsidiary cells and
prominent polar extensions (Chambers etal., 1998). In addition,
although Wollemia nobilis stomata are mostly oriented parallel
to the long axis of the leaf, it has a higher proportion of oblique
and transversal orientations (Chambers etal., 1998). On the other
hand, Agathis and Nageia produce petiolate leaves (Seward and
Ford, 1906; de Laubenfels, 1969, 1972, 1988), whereas leaves of
Araucaria lefipanensis lack a petiole. Furthermore, Agathis species
usually show oblique or transverse stomatal orientations, promi-
nent, bilobed polar extensions, Florin rings (absent in Araucaria
species), and epidermal cells that are quadrangular but not as elon-
gated as those in Araucaria (Stockey and Atkinson, 1993). Another
dierence between Araucaria and Agathis is the range of varia-
tion of the subsidiary cell number. Although four subsidiary cells
is most common among species of both genera, many species of
Agathis have a wider variation in this feature, with three to nine
subsidiary cells sometimes present (Stockey and Atkinson, 1993),
while in Araucaria species the natural variation ranges between
four and six (Stockey and Ko, 1986). Nageia species dierentiate
from A. lefipanensis in having decussate phyllotaxy, stomata with
Florin rings, usually two to four subsidiary cells that show a nar-
row rectangular outline, and guard cells with prominent polar ex-
tensions (de Laubenfels, 1969, 1988; Hill and Pole, 1992; Stockey,
1994; Sun, 2008; Jin etal., 2010).
e vegetative remains assigned to Araucaria lefipanensis show
robust morphological similarities with the broad- leaved araucari-
ans (Araucaria sections Araucaria, Intermedia, and Bunya), which
have been recurrently found as forming a monophyletic group in
both DNA and combined phylogenetic analyses (Setoguchi etal.,
1998; Liu etal., 2009; Escapa and Catalano, 2013). ese similari-
ties between A. lefipanensis and the members of the broad- leaved
clade include the presence of multiple veins, the leaf shape, and the
stomatal morphology and organization (Seward and Ford, 1906;
Wilde and Eames, 1952; Stockey and Ko, 1986; de Laubenfels,
1988; Farjon, 2010). Among the broad- leaved sections, the one that
shows the strongest similarities with the Lepán vegetative organs
is the Australian species A. bidwillii (section Bunya). Araucaria
lefipanensis and A. bidwillii have similar leaf dimorphism, with
some leaves ovate- lanceolate in outline and others lanceolate
(Table1, Fig.7; Seward and Ford, 1906; Oer, 1984; Stockey and
Ko, 1986; Farjon, 2010). Leaves of A. lefipanensis are also simi-
lar to those of the South American section Araucaria. e South
American section contains two species: the Brazilian- Argentinian-
Paraguayan A. angustifolia, whose narrow lanceolate leaves resem-
ble those of the L- shaped morphology of A. lefipanensis; and the
Patagonian A. araucana, which bears ovate- lanceolate leaves that
are more similar to the O- shaped morphology of A. lefipanensis
(Table1; Carrière, 1855; Seward and Ford, 1906; Farjon, 2010).
Araucaria section Intermedia has leaves that are more triangular-
lanceolate than those of A. lefipanensis (Table1; Seward and Ford,
1906; Oer, 1984; Farjon, 2010). All the members of the sections
Araucaria, Intermedia, and Bunya show a similar cuticular micro-
morphology with stomata oriented parallel to the long axis of the
leaf, organized in discontinuous rows having 4–6 subsidiary cells
(Stockey and Ko, 1986), features that A. lefipanensis share with
members of these sections.
Species of section Eutacta produce leaves that dier greatly
from those described here in both macro and micromorphological
features. Araucaria section Eutacta species show relatively small,
2018, Volume 105 • Andruchow- Colombo etal.—Late Cretaceous Araucaria lefipanensis from Patagonia • 11
single- veined leaves and stomata arranged in rows within two lat-
eral bands located at both sides of the central vein (Carrière, 1855;
Wilde and Eames, 1952; de Laubenfels, 1972; Oer, 1984; Stockey
and Ko, 1986; Farjon, 2010). Also, the species within this section
exhibit stomata oblique or perpendicularly oriented in relation to
the leaf major axis (Stockey and Ko, 1986).
In terms of the reproductive organs, the species from Lepán
has ligulate, winged cone scale complexes with a single, unwinged
central seed, which are diagnostic of the genus Araucaria (Seward
and Ford, 1906; Wilde and Eames, 1952; de Laubenfels, 1972, 1988).
ese cone scales are also comparable to those of the genera Agathis
and Wollemia. However, both Agathis and Wollemia produce sin-
gle, winged seeds that are adaxially positioned on the cone scale
complexes, and which are not embedded in the ovuliferous scale
tissues (Seward and Ford, 1906; Florin, 1951; de Laubenfels, 1988;
Chambers etal., 1998; Page, 1990; Owens etal., 1997; Farjon, 2010).
Also they lack the characteristic Araucaria distal ligule (Seward and
Ford, 1906; Florin, 1951; Whitmore, 1980; Chambers etal., 1998;
Farjon, 2010).
e cone scale complexes of A. lefipanensis are more similar to
those of extant species of Araucaria section Eutacta in their gen-
eral outline as well as in the thin, papery appearance of the wings
of the complex (Table 2; Dickson, 1863; Carrière, 1855; Seward
and Ford, 1906; Wilde and Eames, 1952; de Laubenfels, 1972).
Interestingly, the members of the broad- leaved clade (Araucaria
sections Intermedia, Bunya, and Araucaria) produce variable
cone scale complexes (Table2; Seward and Ford, 1906; Wilde and
Eames, 1952; Farjon, 2010). Araucaria section Intermedia has
cone scale complexes with papery- thin, well- developed wings.
However, the cone scale complexes of this section are fan- shaped,
diering from the more cuneate complexes of A. lefipanensis and
Eutacta species (Table2; Wilde and Eames, 1952; de Laubenfels,
1988; Farjon, 2010). Furthermore, the wings of the cone scale com-
plexes of Araucaria section Intermedia, contrary to what happens
in at least some species of the section Eutacta (e.g., A. cunning-
hamii), are vascularized (Haines, 1983b). Species of the section
Araucaria have cone scale complexes with extremely reduced
wings and a prominent rounded ligule (Table 2; Carrière, 1855;
Dickson, 1863; Seward and Ford, 1906; Wilde and Eames, 1952).
Cone scale complexes of Araucaria section Bunya have woody,
vascularized wings and seeds that can be shed at maturity, neither
of which was observed in the cone scale complexes of A. lefipan-
ensis (Table2; Wilde and Eames, 1948, 1952; Florin, 1951). e
cone scale complexes of A. lefipanensis are generally smaller than
in extant species (Table2).
ere are also major dierences between Araucaria lefipan-
ensis and other fossil species previously described within the ge-
nus Araucaria and the fossil genus Araucarites for the mid- late
Mesozoic and Cenozoic (Tables3–6). Several of these species have
similar leaf morphology to A. lefipanensis (Tables3, 4), but only a
few of them have reported dimorphism (Table4; see also section
Leaf morphological variation and seasonality). Among previously
described dimorphic species only Araucaria alexandrensis Cantrill
and Falcon- Lang (2001) from the late Albian of Alexander Island
(Antarctica) shows a similar size to the Lepán species’. It has long,
leafy branches that bear two dierent leaf sizes, but unfortunately
TABLE 1. Comparisons of leaf morphology and cuticle among Araucaria lepanensis and adult morphology of extant Araucaria species.
Character
Section Araucaria Section Bunya
Section
Intermedia
Section EutactaA. lepanenis A. araucana A. angustifolia A. bidwillii A. hunsteinii
Shape Ov. lanc.- Lanc. Ov. lanc. Lanc. Ov. lanc.- Lanc. Tr. lanc. Squamiform
Length (mm) 11.3–35.3 25–60 15–50 10–50 50–100 Up to 20
Width (mm) 4.7–12.7 15–30 3–20 3–15 12–20 Up to 12
Width/Length 0.2–0.7 0.2–0.4 0.2–0.4 0.3 0.1–0.3 Varying
Maximum width position Varying Almost at the leaf base Near the middle Near the middle Near the middle Varying
Type II leaf dimorphismaPresent Absent Absent Present Absent Present
Stomatal orientationb Mostly parallel Mostly parallel Mostly parallel Mostly parallel Mostly parallel Oblique or perpendicular
Epidermal cell outlines Straight Straight More or less straight More or less
sinuous
More or less
sinuous
Varying
Notes: Lanc. = lanceolate; Ov. = ovate; Ov. lanc. = ovate- lanceolate; Tr. lanc. = triangular- lanceolate.
aLeaf dimorphism characterized by two distinct leaf shapes that do not necessarily dier in size.
bStomatal orientation is considered with respect to the major axis of the leaf. Data from Farjon (2010) and Stockey and Ko (1986).
FIGURE 7. Dimorphism comparison between Araucaria bidwillii Hook.
and Araucaria lepanensis sp. nov. (A) Araucaria bidwillii. Leaf silhouettes
of two specimens from the Kew Royal Botanical Gardens Herbarium.
Left, a lanceolate, elongated leaf (L- shaped morphology, specimen
K000961232); right, a shorter, ovate- lanceolate leaf (O- shaped morphol-
ogy, specimen K000961233). (B) Araucaria lepanensis sp. nov. leaf sil-
houettes. Left, L- shaped leaf morphology (MPEF- Pb 8310; Fig. 3.1); right,
O- shaped leaf morphology (MPEF- Pb 8308; Fig. 3.3). Scale bar = 10 mm.
AB
12 • American Journal of Botany
cuticular characters were not preserved (Tables3, 4). e Antarctic
species has been found in association with cone scale complexes re-
ferred to the fossil species Araucarites wollemiaformis that has a cu-
neate outline, a much more prominent bract tip, and is signicantly
larger than the cone scale complexes described here (Tables5, 6).
Araucaria bladenensis Berry (Berry, 1908; Stults etal., 2012) from
the middle and late Cretaceous of North America shows also di-
morphic leaves of a similar length but generally wider than those
of A. lefipanensis (Tables3, 4). e disposition and orientation of
the stomata, and the number and disposition of subsidiary cells are
TABLE 2. Comparisons of cone scale complexes among Araucaria lepanensis and extant Araucaria species.
Character
Section Araucaria Section Bunya Section Intermedia
Section EutactaA. lepanensis A. araucana A. angustifolia A. bidwillii A. hunsteinii
Shape (Not to scale)
OC maximum width (mm) 14.9–18.3 15–20 20 60–80 70–90 From 15 to 90
OC total length (mm) 11.5–20 40–50 50 80–100 50–60 From 15 to 60
Seed length (mm) 9.9 35–50 40 Up to 50 30 15–30
Seed width (mm) 4.9 10–15 15 Up to 35 8 5–15
Wings Well- dev. Ext. red. Ext. red. Well- dev. Well- dev. Well- dev.
Wing appearance Thin Thin Thin Woody Papery- thin Papery- thin
Notes: Well- dev. = well developed; Ext. red. = extremely reduced. Data from Farjon (2010).
TABLE 3. List of fossil species compared with Araucaria lepanensis (Leaves)
Species Age Formation Locality Reference
Aa. cartellei Duarte Aptian Santana Fm. Crato, Ceará, BR Duarte 1993
Aa. grandifolia Feruglio Early Albian Punta del Barco Fm. Ea. El Verano, Santa Cruz, AR Feruglio, 1951; Del Fueyo and
Archangelsky, 2002
Aa. seorsum Cantrill Mid to Late Albian Unnamed a Southern Victoria, AU Cantrill, 1992
Aa. lanceolatus Cantrill Mid to Late Albian Unnamed aSouthern Victoria, AU Cantrill, 1992
Aa. acutifoliatus Cantrill Mid to Late Albian Unnamed aSouthern Victoria, AU Cantrill, 1992
Aa. carinatus Cantrill Mid to Late Albian Otway Fm. Southern Victoria, AU Cantrill, 1992
Aa. otwayensis Cantrill Mid to Late Albian Otway Fm. Southern Victoria, AU Cantrill, 1992
Aa. alexandrensis Cantrill &
Falcon- Lang
Late Albian Neptune Glacier Fm. Triton Point Member, AN Cantrill and Falcon- Lang, 2001
Aa. chambersii Cantrill & Falcon- Lang Late Albian Neptune Glacier Fm. Triton Point Member, AN Cantrill and Falcon- Lang, 2001
Aa. bladenensis Berry Mid and
Late- Cretaceous
Black Creek and Eutaw Fm. Alabama, N and S Carolina, US Berry, 1908; Stults et al., 2012
At. ovatus Hollick Cenomanian Magothy Fm. Cliwood, NJ, US Hollick, 1897
Aa. desmondii Pole Cenomanian Horse Range Fm. Horse Range, NZ Pole, 1995
At. marshalli Edwards Campanian Unnamed Bull’s Point and Batley, NZ Edwards, 1926
Aa. haastii Ettingshausen Late Cretaceous Taratu Fm. Shag Point and Malvern Hills,
NZ
Bose, 1975
Aa. oweni (Ettingsh.) Pole Campanian Taratu Fm. Shag Point, NZ Pole, 1995
Aa. lepanensis Maastrichtian Lepán Fm. Cañadón del Loro, Chubut,
AR
This publication
Aa. taierensis Pole Maastrichtian Taratu Fm. Kai Point Mine, NZ Pole, 1995
Aa. brosa Césari Maastrichtian Snow Hill Island Fm. Cape Lamb, AN Césari et al., 2001; Césari et al., 2009
Aa. hastiensis Hill & Bigwood Mid- Late Eocene Unnamed Hasties, North- East TA Hill and Bigwood, 1987
Aa. pararaucana Panti Late Eocene- Early
Oligocene
Sloggett Fm. Slogget Bay, Tierra del Fuego,
AR
Panti et al., 2007
Aa. mbriatus Hill Late Oligocene Unnamed Little Rapid River, North-
Western TA
Hill, 1990
Aa. nathorsti Dusén Late
Oligocene- Miocene
Ñirihuau Fm. Pico Quemado, Río Negro,
Argentina
Dusén, 1899; Berry, 1928; Menéndez
and Caccavari, 1966; Falaschi et al.,
2012; Ohsawa et al., 2016
Notes: Aa. = Araucaria; At. = Araucarites; AN = Antarctica; AU = Australia; AR = Argentina; BR = Brasil; NJ = New Jersey; NZ = New Zealand; TA = Tasmania; US = United States.
aOtway Group, Zone D (Cantrill and Webb, 1987; Cantrill, 1992).
2018, Volume 105 • Andruchow- Colombo etal.—Late Cretaceous Araucaria lefipanensis from Patagonia • 13
TABLE 4. Comparisons of leaf morphology and cuticle among A. lepanensis and extinct Araucaria species.
Species Shape
Length
(mm)
Width
(mm) Width/Length
Maximum width
position
Foliar
dimorphism Stomatal orientation
Aa. cartellei Lanc. 48 10 0.2 Near basal third of leaf ? —
Aa. grandifolia Tr. lanc. 70–80 10–20 0.2 Near basal third of leaf Absent Mostly parallel
Aa. seorsum Lanc. 54–72 7–11 ≅0.14 Near middle Absent Mostly parallel
Aa. lanceolatus Lanc. 40–52 7–9 0.17 Near basal third of leaf Absent Mostly parallel
Aa. acutifoliatus Lanc. 47–52 6–7 0.13 Near basal third of leaf Absent Parallel to oblique
Aa. carinatus Lanc. to Ov. 4–17 2–12 0.7 Near basal third of leaf Absent Oblique or perpendicular
Aa. otwayensis Lanc. to Ov. 20 — — Near middle ? Mostly oblique
Aa. alexandrensis Lanc. to Ov. 20–30 8–12 0.4 Near basal third of leaf Present ?
Aa. chambersii Lanc. or Ov. lanc. 45–105 8–15 0.15 Near middle Present ?
Aa. bladenensis Ov. lanc. 10–30 8–20 0.7 Near middle Present ?
At. ovatus Ov. lanc. Up to 38 Up to 12.7 0.3 Near middle? ? ?
Aa. desmondii Ov. to lanc. 14–20 10–11 1.4–1.8 Near middle ? Mostly perpendicular
At. marshalli Ov. to lanc. Near basal third of leaf Present ?
Aa. haastii Lanc. 25–75 10–18 0.3 Near basal third of leaf ? Mostly parallel
Aa. oweni Ov. lanc. 20–35 9–16 2.2 Near middle ? ?
Aa. lepanensis Present Mostly parallel
O-shaped group Ov. lanc. 17.49 8.92 0.5 Almost at leaf base
L-shaped group Lanc. 28.37 8.51 0.3 Near middle
Aa. taierensis Ov. lanc. 9–12 5–8 0.6–0.7 Near third of leaf Absent Mostly parallel
Aa. brosa Lanc. to Ov. 55–40 25 0.5 Near basal third of leaf? ? Mostly parallel
Aa. hastiensis Ov. lanc. 19 9 0.5 Almost at leaf base ? Mostly parallel
Aa. pararaucana Ov. lanc. 57 22.5 0.4 Near basal third of leaf ? Mostly parallel
Aa. mbriatus Lanc. 19–23 6–8 0.3 Near middle ? Mostly parallel
Aa. nathorsti Ov. to Lanc. 43 20 0.5 Near basal third of leaf Present Mostly parallel
Notes: Aa. = Araucaria; At. = Araucarites; Lanc. = Lanceolate; Ov. = ovate; Ov. lanc. = ovate- lanceolate; Tr. lanc. = triangular- lanceolate.
TABLE 5. List of fossil species compared with Araucaria lepanensis (reproductive)
Species Age Formation Locality Reference
Aa. cutchensis Feistmantel Jurassic and Early
Cretaceous
Mount Flora Fm.,
Cañadón Asfalto, and
Jabalpur Series
Hope Bay, AN; Chubut, AR; SE of
Chandia, IN; Makoia and Mount
Potts, NZ
Halle, 1913; Arber, 1917; Frenguelli,
1949; Pant and Srivastava, 1968;
Escapa et al., 2008
At. sehoraensis Bose & Maheshwari Mid- Late Jurassic? Parsora Fm. Sher River, Madhya Pradesh, IN Bose and Maheshwari, 1973
At. minutus Bose & Maheshwari Mid- Late Jurassic? Parsora Fm. Sher River, Madhya Pradesh, IN Bose and Maheshwari, 1973
Aa. indica (Sahni) Sukh- Dev &
Zeba- Bano
Late Jurassic- Early
Cretaceous
Jabalpur Fm. Madhya Pradesh, IN Sukh- Dev and Zeba- Bano, 1976
Aa. minimus Archangelsky Early Cretaceous Anteatro de Ticó Fm. Bajo Grande, Santa Cruz, AR Archangelsky, 1966
At. baqueroensis Archangelsky Early Cretaceous Anteatro de Ticó Fm. C. Testigo and other loc., Santa
Cruz, AR
Archangelsky, 1966
At. chilensis Baldoni Early Cretaceous Springhill Fm. El Cóndor, Santa Cruz, AR Baldoni, 1979
At. vulcanoi Duarte Early Cretaceous Santana Fm. Crato, Ceará, BR Duarte, 1993
Araucarites sp. Archangelsky Early Cretaceous Springhill Fm. Pozo El Dorado, XI Región, CH Archangelsky, 1976
At. citadelbastionensis Cantrill &
Falcon- Lang
Early Cretaceous Neptune Glacier Fm. Citadel Bastion, Alexander Island,
AN
Cantrill and Falcon Lang, 2001
At. rogersii Seward Early Cretaceous Kirkwood Fm. Cape Province, SA Seward, 1903; Brown, 1977
Aa. jereyi Berry Mid- Cretaceous Black Creek and Eutaw
Fm.
North Carolina, US Berry, 1908
Araucarian ovulate cone scales Cenomanian Winton Fm. Queensland, AU Dettman et al., 1992; McLoughlin
et al., 1995
Aa. scale type B Pole Cenomanian and
Campanian
Horse Range Fm. Horse Range and Clutha Mouth,
NZ
Pole, 1995
Aa. lepanensis Maastrichtian Lepán Fm. Cañadón del Loro, Chubut, AR This publication
Aa. bladenensis asociated cone
scales
Late Cretaceous Eutaw Fm. Ingersol Shale, Alabama, US Stults et al., 2012
At. pichileufensis Berry Early Eocene La Huitrera Fm. Río Pichileufú, Chubut, AR Berry, 1938
Aa. cf. Araucarites pichileufensis
Berry
Early Eocene Huitrera Fm. Pampa de Jones, Neuquén, AR Wilf et al., 2010
Araucaria sp. Wilf Early Eocene Ventana Fm. Laguna del Hunco, Chubut, AR Wilf et al., 2003
Aa. nathorsti Dusén Late Oligocene- Miocene Ñirihuau Fm. Pico Quemado, Río Negro, AR Falaschi et al., 2012; Ohsawa, 2016
Notes: Aa. = Araucaria; At. = Araucarites; AN = Antarctica; AR = Argentina; AU = Australia; BR = Brasil; CH = Chile; IN = India; NZ = New Zealand; SA = South Africa; US = United States.
14 • American Journal of Botany
similar in both A. bladenensis and A. lefipanensis; however, these
particular cuticular characters tend to be stable through the broad-
leaved araucarian clade. Cone scale complexes associated with A.
bladenensis were also described by Berry (1908) under the name
Araucaria jeffreyi Berry (Tables5, 6), which have a dierent general
outline of those described for the new species. Araucarites mar-
shalli Edwards (1926), from the Campanian of New Zealand also
shows leaf dimorphism. It has leaves with slightly rounded apices
that dier from the sharply acute apices of A. lefipanensis (Tables3,
4). However, A. marshalli cone scale complexes are unknown.
Araucaria hastiensis Hill and Bigwood (Hill and Bigwood, 1987;
Hill, 1990) from the mid- late Eocene of Tasmania and A. fimbria-
tus Hill (1990) from the late Oligocene of Tasmania (Table3) have
some similarities with A. lefipanensis. Both Tasmanian species show
leaf size and shape similar to O- and L- shape groups of A. lefipanen-
sis, respectively (Table4). ey also share with the Patagonian new
species the presence of stomata oriented parallel to the major axis of
the leaf, arranged in rows, with four subsidiary cells. Nevertheless,
both A. hastiensis and A. fimbriatus show stomata with rectangular
outlines, and elongated stomatal apparatuses (Hill and Bigwood,
1987; Hill, 1990) that dier from those observed in A. lefipanensis.
Leaves of A. lefipanensis also dier markedly from those of the
previously known Patagonian fossil species A. grandifolia Feruglio,
A. pararaucana Panti, and A. nathorsti Dusén (Table3; Dusén, 1899;
Berry, 1928; Feruglio, 1951; Menéndez and Caccavari, 1966; Del
Fueyo and Archangelsky, 2002; Panti etal., 2007; Falaschi etal., 2012;
Ohsawa etal., 2016). e Early Cretaceous A. grandifolia Feruglio
has triangular- lanceolate leaves similar to those found in Araucaria
section Intermedia, although Del Fueyo and Archangelsky (2002)
classied this species as part of the section Araucaria because its
leaves are more imbricated than those of the extant species of sec-
tion Intermedia. Araucaria lefipanensis has ovate- lanceolate leaves
that are smaller than those of A. grandifolia (Table 4; Feruglio,
1951; Del Fueyo and Archangelsky, 2002). e Eocene- Oligocene
species, A. pararaucana Panti, has a leaf morphology similar to that
of the O- shaped morphology of A. lefipanensis, but dier in size,
and stomatal orientation (Table 4, Panti etal., 2007). Finally, the
Oligocene- Miocene A. nathorstii Dusén has leaves that are similar
to the new species in shape and stomatal morphology, but that are
larger, and associated cone scale complexes with a dierent gen-
eral outline and degree of wing development (Table4; Dusén, 1899;
Berry, 1928; Menéndez and Caccavari, 1966; Falaschi etal., 2012;
Ohsawa etal., 2016).
e cone scale complexes of Araucaria lefipanensis are unu-
sual in comparison with other fossil cone scales of Araucaria and
Araucarites (Tables5, 6); they have a more heart- shaped outline
than previously described species. Among the most similar cone
scales in shape and size are Araucarites cutchensis Feistmantel
(Feistmantel, 1876; Halle, 1913; Arber, 1917; Frenguelli, 1949;
Pant and Srivastava, 1968) from the Jurassic and Cretaceous of
Gondwana, Araucarites baqueroensis Archangelsky (1966) from
the Early Cretaceous of Patagonia, Araucaria scale type B (Pole,
1995) from the Late Cretaceous of New Zealand, and Araucaria cf.
Araucarites pichileufensis Berry (Wilf et al., 2010) from the early
Eocene of Patagonia (Table5). However, these species dier signi-
cantly in outline from A. lefipanensis cone scale complexes.
Leaf morphological variation and seasonality
Among the vegetative specimens, two morphological groups were
distinguished based on leaf shape and found to be signicantly dif-
ferent in the statistical analyses performed (O and L groups, see
Materials and Methods and Results). However, from a biological
view, they may correspond either to a single taxon or to dierent
natural taxa. Here we propose that both leaf morphologies belong
to a single species with broad, multiveined, sessile leaves based
on the fact that most of the leaf specimens were concentrated in a
single fossiliferous layer (see geologic settings and comparisons),
TABLE 6. Comparisons of Araucaria lepanensis and extinct Araucaria and Araucarites species (reproductive)
Species
Maximum
width
(mm)
Total
length
(mm)
Bract tip
length
(mm)
Seed length
(mm)
Seed
width
(mm) Wings
Wing
appearance Leaf association
At. cutchensis 12.7–20.7 10–22.8 3.5–6.5 5.7–13.8 3.6–7.9 Well- dev. Thin Linear squam.
At. sehoraensis 11–13 13–20 1.2 10–12 6–9 Well- dev. ? Not reported
At. minutus 8–11 10–15 1 - 2 8–10 3–6 Well- dev. ? Not reported
Aa. indica 9–15 23–40 15 - 25 7–17 4–10 Well- dev. ? Podozamites
At. minimus 8 At least 7 3 3.5–5 2–2.5 Well- dev. Thin ?
At. baqueroensis 20 20–30 3 10–15 4–5 Well- dev. Thin ?
At. chilensis 8 11 1 7 3.5 Well- dev. ?Brach.
At. vulcanoi 0.8 12.5 8.4 3.6 Well- dev. ? Broad and Brach.
Araucarites sp. 8 11 1.89 7 3.5 Well- dev. ?Brach.
At. citadelbastionensis 11–15 7–12 2 - - Well- dev. Thin Broad
At. rogersii 25–30 20–30 Not pres. 23.9 8.6 Well- dev. Thin Brach.
Aa. jereyi ? ? ? ? ? Well- dev. Thin Broad
Araucarian ovulate cone scales 7–26 10–37 <1–5 ? ? Well- dev. ? Broad
Aa. scale type B 15–22 17–22 2–5 14 4.7 Well- dev. Thin Broad
Aa. lepanensis 15.2 16.7 2.1 9.9 4.9 Well-dev. Thin Broad
Aa. bladenensis asociated cone scales 6.4 (inc.) 8.9 (inc.) Not pres. 5.3 2.2 Well- dev. Thick Broad
At. pichileufensis 30 27.5 3.19 15.76 7.08 Well- dev. Thin Linear squam.
Aa. cf. Araucarites pichileufensis 15.03 16.9 2.05 10.81 4.5 Well- dev. Thin Without assoc. fol.
Araucaria sp. 12.84 14.83 Not pres. 8.29 5.5 Well dev. Thin ?
Aa. nathorsti Up to 30 15 Not pres. ? 9 Reduced ? Broad
Notes: Aa. = Araucaria; At. = Araucarites; Brach. = Brachyphyllum; Inc. = incomplete; Linear squam. = linear squamiform; Not pres. = not preserved; Well- dev. = well developed; Without assoc.
fol. = without associated foliage.
2018, Volume 105 • Andruchow- Colombo etal.—Late Cretaceous Araucaria lefipanensis from Patagonia • 15
which, in addition to the leaves, yielded a single morphotype of
araucarian cone scale complexes. Furthermore, specimens with in-
termediate morphologies were also found, although in smaller pro-
portion (Appendix S4). Only one type of Araucaria- like epidermal
morphology was recorded in the macerated specimens, which show
the same micromorphology than the (more poorly preserved) cuti-
cles found in connection with both types of leaves of A. lefipanensis.
is nding suggests that both groups also share cuticular char-
acters, including the presence of 4–5 subsidiary cells, polar exten-
sions, and quadrangular, elongated epidermal cells. Nevertheless,
cuticular features in extant species of the broad- leaved clade (sec-
tions Araucaria, Intermedia, and Bunya) are conservative, sharing
most of the gross micromorphological characters (Stockey and Ko,
1986). Additional information supporting the hypothesis of a single
species are the continuous characters, like the sizes of the dierent
epidermal structures, that vary in narrow ranges. In this respect, it
is important to remark that continuous characters are potentially
more informative than discrete features for resolving phylogenetic
relationships among terminal nodes (Escapa and Pol, 2011) since
they capture slighter variations, which are those that can be ex-
pected among closely related organisms.
e leaf shape dierences described for A. lefipanensis are in-
terpreted here as dimorphism. e presence of dimorphic leaves
is a common feature in broad- leaved extant and extinct members
of Araucaria (Seward and Ford, 1906; Berry, 1908; Cantrill and
Falcon- Lang, 2001; Farjon, 2010). e araucarian broad- leaved
clade has two kinds of leaf dimorphism. One consisting of only a
change in leaf size (hereaer type I dimorphism), similarly to what
occurs in the extant South American species Araucaria angustifolia
(Bertol.) Kuntze, and in the extinct species Araucaria bladenensis
Berry, A. alexandrensis Cantrill and Falcon- Lang, Araucarites mar-
shalli Edwards, and A. nathorstii Dusén (Tables3, 4; Dusén, 1899;
Berry, 1908; Edwards, 1926; Berry, 1928; Menéndez and Caccavari,
1966; Cantrill and Falcon- Lang, 2001; Falaschi etal., 2012; Stults
etal., 2012). e second type of dimorphism is characterized by two
distinct leaf shapes (hereaer, type II dimorphism). is is found
in the Australian Araucaria bidwillii, (Fig.7; Stockey and Taylor,
1978a; Farjon, 2010; see the isolectotype of A. bidwillii K000961233
and the specimen K0009612332 from the herbarium of Kew Royal
Botanical Gardens) and in the fossil species A. chambersii Cantrill
and Falcon- Lang (2001) from the Late Cretaceous of Antarctica.
e signicant dierences found between A. lefipanensis O- and L-
shaped groups might indicate that the new species has the second
type of dimorphism described above, with a similar morphological
variation to A. bidwillii (Fig.7). Furthermore, both O- and L- leaf
morphologies have a wide range of sizes, suggesting that several
stages of development were preserved at the Lepán sediments.
erefore, we assume that the dimorphism here reported cannot be
explained as dierent stages of a unique ontogenetic series.
Dimorphic leaves in the broad- leaved sections of Araucaria
have been linked to seasonal variation (Cantrill and Falcon- Lang,
2001), and even though this has been proposed for variation in size
(type I dimorphism), it is possible that changes in shape (type II
dimorphism) are also developed as a response to seasonality. Both
the paleoenvironment and paleoclimate have been reconstructed
for the lower Lepán Formation (Baldoni and Askin, 1993; Cúneo
et al., 2008). ese reconstructions suggest that during the Late
Cretaceous the area was a warm to subtropical patchy forest, prob-
ably more open, warmer, and drier than the cool wet Weddellian
forests of the more southern latitudes (Baldoni and Askin, 1993).
Based on angiosperm mean leaf area analysis (Wilf etal., 1998) and
leaf margin analysis (Wolfe, 1993; Wilf, 1997), Cúneo etal. (2008)
estimated for the latest Cretaceous Lepán Fm., a mean annual
precipitation of around 950 mm and mean annual temperature of
18.2 ± 1.5°C. Since the Late Cretaceous paleolatitude for Lepán
Fm. would have been somewhere near 45° S (Baldoni and Askin,
1993), both temperature and precipitation seasonality could be
expected. e paleoclimate and paleoenvironment of the Lepán
Formation are comparable with that of nowadays natural niche of
Araucaria bidwilli (Enright, 1995; Smith and Butler, 2002; Farjon,
2010), which grows in areas with a mean annual temperature of
18.5°C (Smith and Butler, 2002) and a mean annual rainfall—of the
southern distribution areas of the species—that ranges from 900 to
1400 mm, with a dry season from April/May to September (Farjon,
2010).
Mosaic evolution in araucarian conifers: the case for Araucaria
lepanensis?
Modern conifer systematics is dominated by molecular studies
that do not include fossil species or that use them for node dat-
ing only, without their previous incorporation in the data matrix
(e.g., Bin etal., 2010; Lin etal., 2010; Mao etal., 2010; Crisp and
Cook, 2011; Leslie et al., 2012; Yang etal., 2012). Because whole
plant reconstructions are rare (e.g., Dilcher, 1991; Gee and Tidwell,
2010; Klymiuk etal., 2011; Bomeur et al., 2013), conifer evolu-
tionary studies based on morphology, or both morphology and
molecular evidence, that include fossils are mostly based on an-
atomically preserved seed cones (Miller, 1976, 1988; Smith and
Stockey, 2001; Gernandt etal., 2011; Rothwell etal., 2011; Escapa
and Catalano, 2013; Smith etal., 2017). e use of this particular
organ is understandable if we take into account that seed cones,
among all the organs that conform the conifer bauplan, are oen
considered to have the highest number of characters retaining phy-
logenetic information (Miller, 1988; Rothwell etal., 2009; Spencer
etal., 2015). Furthermore, most modern conifer families are char-
acterized by unique sets of seed cone character states, whereas
other organs, although better represented in the fossil record, tend
to show higher levels of homoplasy (Kendall, 1947; de Laubenfels,
1953; Archangelsky, 1963; Harris, 1979; Miller, 1988). Because of
their apparently less homoplastic nature in comparison with other
organs, in absence of whole- plant reconstructions, seed cones are
currently thought to be the most valuable single- organ substitute
of the whole- plant concept when dealing with extinct conifers
(Spencer etal., 2015).
Fossils with character state combinations not found in extant
species may represent transitional stages in the evolution of a clade.
Studying these is critical in order to understand cryptic homologies
(Florin, 1951; Miller, 1988; Spencer etal., 2015) and to provide ev-
idence for the assessment of whether hypothetical character state
transitions are compatible or incompatible with the fossil record
(Miller, 1988). When fossils with novel character state combinations
are multiple- organ remains or, better still, whole- plant reconstruc-
tions, they are more relevant to evolutionary studies, since they might
reveal changes occurring asynchronously in dierent organs (i.e.,
mosaic evolution). Evidences of mosaic evolution in the fossil record
can help to elucidate the evolutionary history of a given plant group
(e.g., Florin, 1951; Escapa etal., 2010; Bomeur etal., 2013), since
they may be providing information in areas of the phylogeny that
are poorly sampled in terms of extant taxa (Donoghue etal., 1989;
16 • American Journal of Botany
Nixon, 1996; Spencer etal., 2015). Increased taxon sampling based
on fossils, especially on those that show evidence of mosaic evolu-
tion, is particularly important in ancient lineages such as the conifers,
whose evolutionary history goes back in time to the upper Paleozoic,
and, consequently, whose extant families and genera are separated
by long branches (Florin, 1951, 1963; Stockey, 1982; Kunzmann,
2007; Taylor etal., 2009; Leslie etal., 2012). In such cases, the taxon
sampling automatically becomes extremely poor when only extant
species are included in evolutionary studies, since there are extensive
portions of the phylogenetic history of the group that are not sam-
pled at all (Donoghue etal., 1989, Nixon, 1996). erefore, the incor-
poration of fossil species with novel combinations of characters that
occupy a transitional position within these large and poorly sampled
areas, where a large number of changes may have occurred, provides
information not only on the sequential order in which those changes
arose, but also about the timing of these changes.
FIGURE 8. Character evolution of leaves and cone scale complexes of Araucaria. Phylogenetic hypothesis from Escapa and Catalano (2013); Broad-
leaved clade (in pink) includes sections Araucaria, Intermedia, and Bunya; Eutacta clade (in lilac) includes species of section Eutacta. Reconstructed
plesiomorphic features for both leaves and cone scale complexes specied at the nodes that dene each of these clades; above the tree tips, diagrams
of the mean features analyzed are presented. At bottom left, diagrams of the same features specied for the tree tips are shown for Araucaria lepan-
ensis. At bottom right are the character state changes expected for the Eutacta lineage if A. lepanensis were positioned at its base. Finally, the grey
arrows on the tree show a plausible evolutionary scheme for the cone scale complex wings of the broad- leaved clade.
Section Bunya Section Intermedia Section Araucaria Section Eutacta
multiveined uni-veined
A
. lefipanensis
Wing
Reduction
Wing
Vascularization
Wing
Lignification
OC with papery-like wings
+
Scaly-like leaves
Broad Leaved Clade
OC with papery-like wings
+
Broad leaves
Eutacta Clade
2018, Volume 105 • Andruchow- Colombo etal.—Late Cretaceous Araucaria lefipanensis from Patagonia • 17
e material here described—if as we hypothesize, belongs to
the same biological species—provides evidence of mosaic evolution
in Araucaria. Broad, sessile, multiveined leaves, characteristic of
the clade formed by Araucaria sections Araucaria, Intermedia, and
Bunya, are found together with cone scale complexes that are sim-
ilar to those of extant species of Araucaria section Eutacta in both
their general outline and the thin appearance of their wings. Hence,
if they were not found associated, each organ would probably have
been related with dierent sections of the genus.
According to the combined phylogenetic analysis of Escapa and
Catalano (2013), when only considering extant species, the plesio-
morphic conguration of the crown group of the genus Araucaria
seems to be the papery- thin wing morphology for the cone scale
complexes and a broad multiveined morphology for the leaves
(Fig.8). However, a rhomboidal (scale- like) morphology appears
to be a more plausible basal leaf morphology when taking into ac-
count the oldest fossil record assigned to the genus or associated
with it, as it is the case of several Brachyphyllum species (Kendall,
1949; Calder, 1953; Townrow, 1967; Harris, 1979; Gee and Tidwell,
2010; Falaschi etal., 2011; Sender etal., 2015). e reconstructed
basal conguration for the crown group of the clade comprised
by the species of section Eutacta would be thin- winged cone scale
complexes and single- veined scale- like leaves (Fig. 8). Finally, for
the crown group of the broad- leaved clade (sections Araucaria,
Intermedia, and Bunya) the basal conguration for the leaves would
be broad and multiveined (Fig.8), especially if its fossil record is
considered (e.g., Berry, 1908; Bose, 1975; Cantrill, 1992; Duarte,
1993; Cantrill and Falcon- Lang, 2001; Del Fueyo and Archangelsky,
2002). e basal conguration of the cone scale complex wings for
this clade is papery- thin when considering only extant species, but
when the fossil record is taken into account, the optimization of this
character is ambiguous (Escapa and Catalano, 2013).
Regarding the previously discussed possible plesiomorphic con-
gurations of the broad- leaved and Eutacta clades of the phylog-
eny recovered by Escapa and Catalano (2013), the new Patagonian
species has two putative places within Araucaria. One would be
at the base of the Eutacta clade. If this is the case, A. lefipanensis
would be an autapomorphic basal species or, alternatively, broad
leaves would be the basal conguration for the Eutacta clade, and
they would go through a reduction in the evolution of the group
to scaly, single- veined leaves, with oblique or transverse- oriented
stomata, organized in parallel rows, arranged at both sides of the
leaf mid- vein in two stomatal bands (Fig.8). In this scenario, cone
scale complexes would suer virtually no change in the evolution of
the clade (Fig.8). In the second evolutionary scenario, Araucaria
lefipanensis would be part of the broad- leaved clade. is scenario
is supported by the high amount of features shared by leaves of the
new Patagonian species and extant species of the genus, which in-
clude shape and attachment of leaves, presence of multiple veins,
and cuticle morphology. Additionally, as mentioned above, the ple-
siomorphic conguration of the cone scale complex wing morphol-
ogy for the broad- leaved clade is optimized as ambiguous, being
compatible with a thin- winged basal species. e second scenario
is also more compatible than the rst one when taking into account
the consistent evidence provided by the leaf morphology of the
Cretaceous and Cenozoic fossil species assigned to both Eutacta
and broad- leaved clades (e.g., Hill and Bigwood, 1987; Del Fueyo
and Archangelsky, 2002; Panti etal., 2007).
Traditionally, the ancestral conguration of the seed cones of
Araucaria was interpreted as showing heavy, woody- winged cone
scale complexes (Wilde and Eames, 1948) because Jurassic mem-
bers assigned to the genus show cone scale complexes with well-
developed, woody wings (Kendall, 1949; Calder, 1953; Stockey,
1975, 1980; Axsmith etal., 2008). However, it is yet to be determined
whether these species belong to the crown or stem group of the ge-
nus or even to the stem group of the family (Kunzmann, 2007). On
the light of the total evidence analyses performed by Escapa and
Catalano (2013), section Bunya is reconstructed to have the most
derived cone scale complex morphology, including the woody, well-
developed wings and seeds that shed at maturity (Wilde and Eames,
1952), which might have evolved sequentially in the broad- leaved
clade, by an initial vascularization of the cone scale complex wings,
as seen in section Intermedia (Haines, 1983b), and by further ligni-
cation (Fig.8). In this context, Araucaria lefipanensis can be in-
terpreted as having a derived conguration of leaf characters and a
plesiomorphic conguration of cone scale complexes features (thin,
well- developed wings), suggesting mosaic evolution.
CONCLUSIONS
Remains of leaves and cone scale complexes from the Late
Cretaceous of Patagonia were described and interpreted as belong-
ing to a single new species, Araucaria lefipanensis. e leaf shape
dimorphism in A. lefipanensis is consistent with the presence of
this type of dimorphic leaves in the extant Australian A. bidwillii
(section Bunya), which is native to subtropical forest with markedly
seasonality and mean annual temperature and precipitation values
similar to those reconstructed by Cúneo etal. (2008) for the Late
Cretaceous portion of the Lepán Formation.
e new Patagonian species shows a mosaic of character states,
with broad, multiveined, sessile leaves typical of the broad- leaved
clade (sections Araucaria, Intermedia, and Bunya; see Fig.8), and
cone scale complexes similar to those found in the Eutacta clade
in both general outline and thin appearance of its wings (Fig.8).
Because of this mosaic of features, A. lefipanensis constitutes an in-
teresting species to analyze in a phylogenetic context since it might
provide information about the early evolution of either the broad-
leaved or the Eutacta clades according to its phylogenetic position.
Moreover, phylogenetic analyses including this and other fossil spe-
cies based on compressions and impressions are necessary steps to
better understand the evolution of the Araucariaceae. Denitely, in-
cluding this kind of fossils implies the circumscription and discus-
sion of systematically informative characters that can be identied
in these preservation types, since previous studies that included fos-
sils were based mostly in permineralized material (see discussion),
and the inclusion of other types of preservations may give comple-
mentary information (e.g., Escapa and Leslie, 2017).
ACKNOWLEDGEMENTS
e authors thank F. De Benedetti, M. Caa, L. Canessa, E. Currano,
A. Elgorriaga, E. J. Hermsen, A. Iglesias, K. Johnson, N. A. Jud, P.
Puerta, R. Scasso, and P. Wilf for their assistance during numerous
eld seasons, L. Reiner and E. Ruigomez for helping with the cura-
tion of the specimens, R. Carpenter and I. Davie for help in cuticle
preparation, M. Pole for kindly providing images of New Zealand
fossil material;, Aluar Aluminio Argentino SAIC for access to the
SEM; J. Groizard and M. Luquet for technical support, and to the
18 • American Journal of Botany
Secretaría de Cultura de la Provincia del Chubut for land access.
Special thanks to P. Milla Carmona and I. M. Soto for their valuable
assistance on the statistical analyses, to D. Pol, A. Elgorriaga, and
M.C. Madozzo Jaén for their valuable insights, and to L. Aagesen
and N. A. Jud for English improvement. Financial support has
been provided by the Agencia Nacional de Promoción Cientíca
y Tecnológica (PICT 2014- 2433 to N.R.C.) and the National
Science Foundation (NSF- DEB- 1556666 and NSF- DEB- 0919071
to N.R.C.; NSF- DEB- 09118932 and NSF- DEB- 1556136 to M.A.G.).
is research was partially funded by the Consejo Nacional de
Investigaciones Cientícas y Técnicas (CONICET). We are in-
debted to two anonymous reviewers that greatly helped to improve
the manuscript.
SUPPORTING INFORMATION
Additional Supporting Information may be found online in the
supporting information tab for this article.
LITERATURE CITED
Arber, E. A. N. 1917. e earlier Mesozoic oras of New Zealand. New Zealand
Geological Survey Bulletin 6: 1–80.
Archangelsky, S. 1963. A new Mesozoic ora from Ticó, Santa Cruz Province,
Argentina. Bulletin of the British Museum (Natural History) Geology 8: 4–92.
Archangelsky, S. 1966. New gymnosperms from the Tico ora, Santa Cruz prov-
ince, Argentina. Bulletin of the British Museum (Natural History). Geology
13: 201–295.
Archangelsky, S. 1976. Vegetales fósiles de la Formación Springhill, Cretácico,
en el subsuelo de la Cuenca Magallánica, Chile. Ameghiniana 13: 141–158.
Axsmith, B. J., and S. R. Ash. 2006. Two rare fossil cones from the Upper Triassic
Chinle Formation in Petried Forest National Park, Arizona, and New
Mexico. Museum of Northern Arizona Bulletin 62: 82–94.
Axsmith, B. J., I. H. Escapa, and P. Huber. 2008. An araucarian conifer bract-
scale complex from the Lower Jurassic of Massachusetts: implications for
estimating phylogenetic and stratigraphic congruence in the Araucariaceae.
Palaeontologia Electronica 11: 1–7.
Baldoni, A. M. 1979. Nuevos elementos paleoorísticos de la tafoora de la
Formación Springhill, límite Jurásico- Cretácico subsuelo de Argentina y
Chile Austral. Ameghiniana 16: 103–119.
Baldoni, A. M. 1992. Palynology of the lower Lepán Formation (Upper
Cretaceous) of Barranca de los Perros, Chubut province, Argentina. Part I.
Cryptogam spores and gymnosperm pollen. Palynology 16: 117–136.
Baldoni, A. M., and R. A. Askin. 1993. Palynology of the lower Lepán formation
(Upper Cretaceous) of Barranca de los Perros, Chubut Province, Argentina
part l—angiosperm pollen and discussion. Palynology 17: 241–264.
Barreda, V. D., N. R. Cúneo, P. Wilf, E. D. Currano, R. A. Scasso, and H.
Brinkhuis. 2012. Cretaceous/Paleogene oral turnover in Patagonia: drop in
diversity, low extinction, and a Classopollis spike. PLoS ONE 7: e52455.
Bercovici, A., A. Hadley, and U. Villanueva-Amadoz. 2009. Improving depth
of eld resolution for palynological photomicrography. Palaeontologia
Electronica 12: 1–12.
Berry, E. W. 1908. Some araucarian remains from the Atlantic Coastal Plain.
Bulletin of the Torrey Botanical Club 35: 249–260.
Berry, E. W. 1928. Tertiary fossil plants from the Argentine Republic. Proceedings
of the US Natural History Museum 73: 1–27.
Berry, E. W. 1938. Tertiary ora from the Río Pichileufú, Argentina. Geological
Society of America, Special Papers 12: 1–149.
Bin, E., R. S. Hill, and A. J. Lowe. 2010. Did Kauri (Agathis: Araucariaceae)
really survive the Oligocene drowning of New Zealand? Systematic Biology
59: 594–602.
Bomeur, B., A. L. Decombeix, I. H. Escapa, A. B. Schwendemann, and B.
Axsmith. 2013. Whole- plant concept and environment reconstruction of a
Telemachus conifer (Voltziales) from the Triassic of Antarctica. International
Journal of Plant Sciences 174: 425–444.
Bose, M. N. 1975. Araucaria hastii Ettingshausen from Shag Point, New Zealand.
Palaeobotanist 22: 76–80.
Bose, M. N., and H. K. Maheshwari. 1973. Some detached seeds belonging to
Araucariaceae from the Mesozoic rocks of India. Geophytology 3: 205–214.
Box, G. E. P. 1949. A general distribution theory for a class of likelihood criteria.
Biometrika 36: 317–346.
Brown, J. T. 1977. On Araucarites rogersii Seward from the Lower Cretaceous
Kirkwood Formation of the Algoa Basin, Cape Province, South Africa.
Palaeontologia Africana 20: 47–51.
Calder, M. G. 1953. A coniferous petried forest in Patagonia. Bulletin of the
British Museum (Natural History) Geology 2: 99–138.
Cantrill, D. J. 1992. Araucarian foliage from the Lower Cretaceous of Southern
Victoria, Australia. International Journal of Plant Sciences 153: 622–645.
Cantrill, D. J., and H. J. Falcon-Lang. 2001. Cretaceous (late Albian) coniferales
of Alexander Island, Antarctica. 2. Leaves, reproductive structures and roots.
Review of Palaeobotany and Palynology 115: 119–145.
Cantrill, D. J., and J. A. Webb. 1987. A reappraisal of Phyllopteroides Medwell
(Osmundaceae) and its stratigraphic signicance in the Lower Cretaceous of
eastern Australia. Alcheringa 11: 59–85.
Carrière, E. A. 1855. Traité général des Conifères. Chez l’auteur, Paris, France.
Césari, S. N., S. A. Marenssi, and S. N. Santillana. 2001. Conifers from the Upper
Cretaceous of Cape Lamb, Vega Island, Antarctica. Cretaceous Research 22:
309–319.
Césari, S. N., S. A. Marenssi, and S. N. Santillana. 2009. Araucaria fibrosa, a new
name to replace the illegitimate name Araucaria antarctica Césari, Marenssi
and Santillana, 2001. Cretaceous Research 30: 1169.
Chambers, T. C., A. N. Drinnan, and S. McLoughlin. 1998. Some morphological
features of Wollemi pine (Wollemia nobilis: Araucariaceae) and their com-
parison to Cretaceous plant fossils. International Journal of Plant Sciences
159: 160–171.
Codrington T. A., L. J. Scott, K. D. Scott, G. C. Graham, M. Rossetto, M.
Ryan, T. Whin, et al. 2009. Unresolved phylogenetic position of
Wollemia, Araucaria and Agathis. In R. L. Bieleski and M. D. Wilcox
[eds.], Araucariaceae, Proceedings of the 2002 Araucariaceae Symposium,
Araucaria-Agathis-Wollemia, 69–73. International Dendrology Society,
Dunedin, New Zealand.
Crisp, M. D., and L. G. Cook. 2011. Cenozoic extinctions account for the low di-
versity of extant gymnosperms compared with angiosperms. New Phytologist
192: 997–1009.
Cúneo, N. R., K. Johnson, R. Scasso, V. Barreda, H. Brinkhuis, W. Clyde, M.
A. Gandolfo, and P. Wilf. 2008. e K-T boundary and the associated o-
ral event in South America. e case for Patagonia. VII International
Organization of Palaeobotany Conference, Bonn, Germany, abstract 126.
da Silva, A. R. 2017. Tools for biometry and applied statistics in agricultural sci-
ence. In R Core Team [eds.], e comprehensive R archive network. Website
https://CRAN.R-project.org/package=psych.
de Laubenfels, D. J. 1953. e external morphology of coniferous leaves.
Phytomorphology 3: 1–20.
de Laubenfels, D. J. 1969. A revision of Malesian and Pacic rainforest conifers,
I. Podocarpaceae, in part. Journal of the Arnold Arboretum 50: 274–369.
de Laubenfels, D. J. 1972. Araucariaceae. In A. Aubréville and J.-F. Leroy [eds.],
Flore de la Nouvelle-Calédonie et dépendances: Gymnospermes, 80–143.
Muséum National d’Histoire Naturelle, Laboratoire de Phanérogamie, Paris,
France.
de Laubenfels, D. J. 1978. e Moluccan dammars (Agathis, Araucariaceae).
Blumea 24: 499–504.
de Laubenfels, D. J. 1979. e species of Agathis (Araucariaceae) of Borneo.
Blumea 25: 531–541.
de Laubenfels, D. J. 1988. Coniferales. In W.J.J.O. de Wilde [ed.], Flora Malesiana,
series 1, Spermatophyta, 419–442. Kluwer, Dordrecht, Netherlands.
Del Fueyo, G. M. 1991. Una nueva Araucariaceae Cretácica de Patagonia,
Argentina. Ameghiniana 28: 149–161.
2018, Volume 105 • Andruchow- Colombo etal.—Late Cretaceous Araucaria lefipanensis from Patagonia • 19
Del Fueyo, G. M., and A. Archangelsky. 2002. Araucaria grandifolia Feruglio
from the Lower Cretaceous of Patagonia, Argentina. Cretaceous Research 23:
265–277.
Dettmann, M. E., and H. T. Cliord. 2005. Biogeography of Araucariaceae.
Australia and New Zealand forest histories: araucarian forests. Australian
Forest History Society Inc. Occasional Publication 2: 1–9.
Dettmann, M. E., R. E. Molnar, J. G. Douglas, D. Burger, C. Fielding, H. T.
Cliord, J. Francis, et al. 1992. Australian Cretaceous terrestrial faunas and
oras: biostratigraphic and biogeographic implications. Cretaceous Research
13: 207–262.
Dickson, A. 1863. II. On some of the stages of development in the female ower
of Dammara australis. Transactions of the Botanical Society of Edinburgh 7:
207–215.
Dilcher, D. L. 1991. e importance of anatomy and whole plant reconstructions
in palaeobotany. Current Science 61: 627–629.
Donoghue, M. J., J. A. Doyle, J. Gauthier, A. G. Kluge, and T. Rowe. 1989. e im-
portance of fossils in phylogeny reconstruction. Annual Review of Ecology,
Evolution and Systematics 20: 431–460.
Duarte, L. 1993. Restos de Araucariáceas da Formação Santana – Membro
Crato (Aptiano), NE do Brasil. Anais da Academia Brasileira de Ciências
65: 357–362.
Dusén, P. 1899. Über die tertiäre Flora der Magellansländer. Wissenschaliche
Ergebnisse der Schwedischen Expedition nach der Magellansländern, 1895–
1897. Band 1: 84–107.
Eames, A. J. 1913. e morphology of Agathis australis. Annals of Botany 27:
1–38.
Edwards, B. A. 1926. Cretaceous plants from Kaipara, New Zealand. Transactions
and Proceedings of the New Zealand Institute 56: 121–128.
Endlicher, S. 1842.Mantissa botanica sistens generum plantarum, supplemen-
tum secundum. Apud Fridericum Beck, Universitatis Bibliopolam, Vienna,
Austria.
Enright, N. J. 1995. Conifers of tropical Australasia. In N. J. Enright and R. S. Hill
[eds.], Ecology of the southern conifers, 197–222. Smithsonian Institution
Press, Washington, D.C., USA.
Enright, N. J., R. S. Hill, and T. T. Veblen. 1995. e southern conifers—an in-
troduction. In N. J. Enright and R. S. Hill [eds.], Ecology of the southern
conifers, 1–9. Smithsonian Institution Press, Washington, D.C., USA.
Escapa, I. H., and S. A. Catalano. 2013. Phylogenetic analysis of Araucariaceae:
integrating molecules, morphology and fossils. International Journal of
Plant Sciences 174: 1153–1170.
Escapa, I. H., and A. Leslie. 2017. A new Cheirolepidaceae (Coniferales) from the
Early Jurassic of Patagonia (Argentina): reconciling the records of impres-
sion and permineralized fossils. American Journal of Botany 104: 322–334.
Escapa, I. H., and D. Pol. 2011. Dealing with incompleteness: new advances for
the use of fossils in phylogenetic analysis. Palaios 26: 121–124.
Escapa, I. H., J. Sterli, D. Pol, and L. Nicoli. 2008. Jurassic tetrapods and ora
of Cañadón Asfalto Formation in Cerro Cóndor Area, Chubut Province.
Revista de la Asociación Geológica Argentina 63: 613–624.
Escapa, I. H., A. L. Decombeix, E. L. Taylor, and T. N. Taylor. 2010. Evolution
and relationships of the conifer seed cone Telemachus: Evidence from the
Triassic of Antarctica. International Journal of Plant Sciences 171: 560–573.
Falaschi, P., J. Grosfeld, A. B. Zamuner, N. Foix, and S. M. Rivera. 2011. Growth
architecture and silhouette of Jurassic conifers from La Matilde Formation,
Patagonia, Argentina. Palaeogeography, Palaeoclimatology, Palaeoecology
302: 122–141.
Falaschi, P., M. C. Zamaloa, N. Caviglia, and E. J. Romero. 2012. Flora
Gimnospérmica de la Formación Ñirihuau (Oligoceno Tardío- Mioceno
temprano), Provincia de Río Negro, Argentina. Ameghiniana 49: 525–551.
Farjon, A. 2010. A handbook of the world’s conifers. Brill, Leiden, Netherlands.
Feistmantel, O. 1876. e fossil ora of the Gondwana system. Jurassic (Oolitic)
Flora of Kach. Memoirs of the Geological Society of India, Palaeontologia
Indica, series II 2: 1–80.
Feruglio, E. 1951. Piante del mesozoico della Patagonia. Pubblicazioni dell’Isti-
tuto Geologico della Università di Torino 1: 35–80.
Filzmoser, P., and M. Gschwandtner. 2018. mvoutlier: multivariate outlier de-
tection based on robust methods. R package version 2.0.9. In R Core Team
[eds.], e comprehensive R archive network. Website https://CRAN.
Rproject.org/package=mvoutlier.
Florin, R. 1951. Evolution in cordaites and conifers. Acta Horticulturae Bergiani
15: 285–388.
Florin, R. 1963. e distribution of conifer and taxad genera in time and space.
Acta Horticulturae Bergiani 20: 121–312.
Frenguelli, J. 1949. Los estratos con ‘Estheria’ en el Chubut. Revista de la
Asociación Geológica Argentina 4: 11–24.
Gee, C. T., and D. Tidwell. 2010. A mosaic of characters in a new whole-plant
Araucaria, A. delevoryasii Gee sp. nov., from the late Jurassic Morrison
Formation of Wyoming, U.S.A. In C. T. Gee [ed.], Plants in Mesozoic time,
67–94. Indiana University Press, Bloomington, IN, USA.
Gernandt, D. S., C. León-Gómez, S. Hernández-León, and M. E. Olson. 2011.
Pinus nelsonii and a cladistic analysis of Pinaceae ovulate cone characters.
Systematic Botany 36: 583–594.
Gilmore, S., and K. D. Hill. 1997. Relationships of the Wollemi pine (Wollemia
nobilis) and a molecular phylogeny of the Araucariaceae. Telopea 7: 275–291.
Haines, R. J. 1983a. Embryo development and anatomy in Araucaria Juss.
Australian Journal of Botany 31: 125–140.
Haines, R. J. 1983b. Seed development in Araucaria Juss. Australian Journal of
Botany 31: 255–267.
Halle, T. G. 1913. e mesozoic ora of Graham Land. Lithographisches Institut
des Generalstabs, Stockholm, Sweden.
Harrell, F. E. Jr., and C. Dupont. 2016. Hmisc: Harrell miscellaneous. In R
Core Team [eds.], e comprehensive R archive network. Website https://
CRAN.R-project.org/package=Hmisc.
Harris, T. M. 1979. e Yorkshire Jurassic ora, V: Coniferales. British Museum
(Natural History), London, UK.
Henkel, J. B., and W. Hochstetter. 1865. Synopsis der Nadelhölzer, deren charak-
teristischen Merkmale nebst Andeutungen über ihre Cultur und Ausdauer in
Deutschlands Klima. Verlag der J. G. Cotta’schen Buchhandlung, Stuttgart,
Ge r many.
Hill, R. S. 1990. Araucaria (Araucariaceae) species from Australian Tertiary sedi-
ments—a micromorphological study. Australian Systematic Botany 3: 203–220.
Hill, R. S., and A. J. Bigwood. 1987. Tertiary gymnosperms from Tasmania:
Araucariaceae. Alcheringa 11: 325–335.
Hill, R. S., and M. S. Pole. 1992. Leaf and shoot morphology of extant Afrocarpus,
Nageia and Retrophyllum (Podocarpaceae) species, and species with sim-
ilar leaf arrangement, from Tertiary sediments in Australasia. Australian
Systematic Botany 5: 337–358.
Hollick, A. 1897. e Cretaceous Clay Marl exposure at Cliwood, N.J.
Transactions of the New York Academy of Sciences 16: 124–138.
Hyland, B. P. M. 1978. A revision of the genus Agathis (Araucariaceae) in
Australia. Australian Systematic Botany 1: 103–115.
Jin, J., J. Qiu, Y. Zhu, and T. M. Kodrul. 2010. First fossil record of the genus
Nageia (Podocarpaceae) in South China and its phytogeographic implica-
tions. Plant Systematics and Evolution 285: 159–163.
de Jussieu, A. L. 1789. Genera plantarum secundum ordines naturales dispos-
ita juxta methodum in horto regio parisiensi exaratam, anno 1774. Apud
Viduam Herissant, typographum, Paris, France.
Kendall, M. W. 1947. On ve species of Brachyphyllum from the Jurassic of
Yorkshire and Wiltshire. Annals and Magazine of Natural History, series 11
14: 225–251.
Kendall, M. W. 1949. A Jurassic member of the Araucariaceae. Annals of Botany
13: 151–161.
Kerp, H., and B. Bomeur. 2011. Photography of plant fossils—New techniques,
old tricks. Review of Palaeobotany and Palynology 166: 117–151.
Kershaw, P., and B. Wagsta. 2001. e southern conifer family Araucariaceae:
history, status, and value for paleoenvironmental reconstruction. Annual
Review of Ecology and Systematics 32: 397–414.
Kiessling, W., E. Aragón, R. Scasso, M. Aberhan, J. Kriwet, F. Medina, and D.
Fracchia. 2005. Massive corals in Paleocene siliciclastic sediments of Chubut
(Argentina). Facies 51: 223–241.
Klymiuk, A. A., R. A. Stockey, and G. W. Rothwell. 2011. e rst organ-
ismal concept for an extinct species of Pinaceae: Pinus arnoldii Miller.
International Journal of Plant Sciences 172: 294–313.
20 • American Journal of Botany
Koch, K. 1873. Pinus araucana Molina. Dendrochronology 2: 206.
Korkmaz, S., D. Goksuluk, and G. Zararsiz. 2014. MVN: An R package for as-
sessing multivariate normality. R Journal 6: 151–162.
Kunzmann, L. 2007. Araucariaceae (Pinopsida): Aspects in palaeobiogeog-
raphy and palaeobiodiversity in the Mesozoic. Zoologischer Anzeiger 246:
257–277.
Lele, K. M. 1956. Plant fossils from Parsora in the South Rewa Gondwana Basin,
India. Palaeobotanist 4: 23–34.
Leslie, A. B., J. M. Beaulieu, H. S. Rai, P. R. Crane, M. J. Donoghue, and S.
Mathews. 2012. Hemisphere- scale dierences in conifer evolutionary
dynamics. Proceedings of the National Academy of Sciences, USA 109:
16217–16221.
Lin, C. P., J. P. Huang, C. S. Wu, C. Y. Hsu, and S. M. Chaw. 2010. Comparative
chloroplast genomics reveals the evolution of Pinaceae genera and subfami-
lies. Genome Biology and Evolution 2: 504–517.
Liu, N., Y. Zhu, Z. X. Wei, J. Chen, Q. B. Wang, S. G. Jian, D. W. Zhou, et al. 2009.
Phylogenetic relationships and divergence times of the family Araucariaceae
based on the DNA sequences of eight genes. Chinese Science Bulletin 54:
2648–2655.
Mao, K., G. Hao, J. Liu, R. P. Adams, and R. I. Milne. 2010. Diversication and
biogeography of Juniperus (Cupressaceae): variable diversication rates and
multiple intercontinental dispersals. New Phytologist 188: 254–272.
McLoughlin, S., A. N. Drinnan, and A. C. Rozefelds. 1995. A Cenomanian
ora from the Winton Formation, Eromanga Basin, Queensland, Australia.
Memoirs of the Queensland Museum 92: 207–227.
Medina, F. A., and E. Olivero. 1994. Paleontología de la Formación Lepán
(Cretácico- Terciario) en el valle medio del río Chubut. Revista de la
Asociación Geológica Argentina 48: 105–106.
Medina, F. A., H. H. Camacho, and E. C. Malagnino. 1990. Bioestratigrafía del
Cretácico Superior- Paleoceno marino de la Formación Lepán, Barranca de
los Perros, Río Chubut, Chubut. V Congreso Argentino de Paleontología y
Bioestratigrafía, San Miguel de Tucumán, Tucumán. Actas 1: 137–141.
Menéndez, C. A., and M. A. Caccavari. 1966. Estructura epidérmica de Araucaria
nathorsti Dus. del Terciario de Pico Quemado, Río Negro. Ameghiniana 4:
195–199.
Mill, R., M. Ruhsam, P. omas, M. Gardner, and P. Hollingsworth. 2017.
Araucaria goroensis (Araucariaceae), a new monkey puzzle from New
Caledonia, and nomenclatural notes on Araucaria muelleri. Edinburgh
Journal of Botany 74: 123–139.
Miller, C. N. Jr. 1976. Early evolution in the Pinaceae. Review of Palaeobotany
and Palynology 21: 101–117.
Miller, C. N. Jr. 1988. e origin of modern conifer families. In C.B. Beck [ed.],
Origin and evolution of gymnosperms, 448–486. Columbia University Press,
NY, NY, USA.
Nixon, K. C. 1996. Paleobotany in cladistics and cladistics in paleobotany: en-
lightenment and uncertainty. Review of Paleaobotany and Palynology 90:
361–373.
Oer, C. E. 1984. Extant and fossil Coniferales of Australia and New Guinea.
Part 1: A study of the external morphology of the vegetative shoots of the
extant species. Palaeontographica, Abteilung B 193: 18–120.
Ohsawa, T., H. Nishida, and M. Nishida. 1995. Yezonia, a new section of
Araucaria (Araucariaceae) based on permineralized vegetative and repro-
ductive organs of A. vulgaris comb. nov. from the Upper Cretaceous of
Hokkaido, Japan. Journal of Plant Research 108: 25–39.
Ohsawa, T. A., A. Yabe, T. Yamada, K. Uemura, K. Terada, M. Leppe, L. F.
Hinojosa, and H. Nishida. 2016. Araucarian leaves and cone scales from the
Loreto Formation of Río de Las Minas, Magellan Region, Chile. Botany 94:
805–815.
Olivero, E. B., F. A. Medina, and H. H. Camacho. 1990. Nuevos hallazgos de
moluscos con anidades australes en la Formación Lepán (Cretácico
Superior, Chubut): signicado paleogeográco. V Congreso Argentino de
Paleontología y Bioestratigrafía, San Miguel de Tucumán, Tucumán. Actas
1: 129–135.
Owens, J. N., G. L. Catalano, and J. Aitken-Christie. 1997. e reproductive bi-
ology of Kauri (Agathis australis). IV. Late embryogeny, histochemistry, cone
and seed morphology. International Journal of Plant Sciences 158: 395–407.
Olson, C. L. 1974. Comparative robustness of six tests in multivariate analysis of
variance. Journal of the American Statistical Association 69: 894–908.
Page, C. N. 1990. Araucariaceae. In K. Kubitzki, K. U. Kramer, and P. S. Green
[eds.], e families and genera of vascular plants, vol. I, Pteridophytes and
gymnosperms, 294–299. Springer-Verlag, NY, NY, USA.
Pant, D. D., and G. K. Srivastava. 1968. On the cuticular studies of Araucaria
(Araucarites) cutchensis (Feistmantel) comb. nov. from the Jabalpur series,
India. Botanical Journal of the Linnean Society 61: 201–206.
Panti, C., S. N. Césari, S. A. Marenssi, and E. B. Olivero. 2007. A new araucarian
fossil species from the Paleogene of southern Argentina. Ameghiniana 44:
215–222.
Panti, C., R. R. Pujana, M. C. Zamaloa, and E. J. Romero. 2012. Araucariaceae
macrofossil record from South America and Antarctica. Alcheringa 36: 1–22.
Pillai, K. C. S. 1955. Some new test criteria in multivariate analysis. Annals of
Mathematical Statistics 26: 117–121.
Pole, M. 1995. Late Cretaceous macrooras of eastern Otago, New Zealand:
gymnosperms. Australian Systematic Botany 8: 1067–1106.
R Core Team. 2016. R: A language and environment for statistical computing.
R Foundation for Statistical Computing, Vienna, Austria. Website https://
www.R-project.org/.
Rai, H. S., P. A. Reeves, R. Peakall, R. G. Olmstead, and S. W. Graham. 2008.
Inference of higher- order conifer relationships from a multi- locus plastid
data set. Botany 86: 658–669.
Revelle, W. 2016. psych: Procedures for personality and psychological research.
In R Core Team [eds.], e comprehensive R archive network. Website
https://CRAN.R-project.org/package=psych.
Rothwell, G. W., G. Mapes, R. A. Stockey, J. Hilton, and R. M. Bateman. 2009.
“Descent with modication”, transformational series, and phylogenetic anal-
yses to infer the evolution of modern conifer families. Geological Society of
America Annual Conference Abstracts and Programs, Portland, OR, USA,
vol. 41: 563.
Rothwell, G. W., R. A. Stockey, G. Mapes, and J. Hilton. 2011. Structure and rela-
tionships of the Jurassic conifer seed cone Hughmillerites juddii gen. et comb.
nov.: Implications for the origin and evolution of Cupressaceae. Review of
Palaeobotany and Palynology 164: 45–59.
Ruiz, L. E. 2007. Estudio sedimentológico y estratigráco de las formaciones
Paso del Sapo y Lepán en el Valle Medio del Río Chubut. B.S. dissertation,
Universidad de Buenos Aires, Buenos Aires, Argentina.
Sarkar, D. 2008. Lattice: multivariate data visualization with R. Springer, NY, NY,
USA.
Scasso, R. A., M. Aberhan, L. Ruiz, S. Weidemeyer, F. A. Medina, and W.
Kiessling. 2012. Integrated bio- and lithofacies analysis of coarse- grained,
tide- dominated deltaic environments across the Cretaceous/Paleogene
boundary in Patagonia, Argentina. Cretaceous Research 36: 37–57.
Sender, L. M., I. H. Escapa, and N. R. Cúneo. 2015. Diversidad de coníferas de
la Formación Cañadón Asfalto (Jurásico Inferior- Medio) en la Patagonia
central Argentina: aplicación de nuevas técnicas en el estudio de cutículas
fósiles. XVI Simposio Argentino de Paleobotánica y Palinología, La Plata,
Buenos Aires, Argentina. Ameghiniana, Abstract Supplement 52: 4R.
Setoguchi, H., T. A. Osawa, J. C. Pintaud, T. Jaré, and J. M. Veillon. 1998.
Phylogenetic relationships within Araucariaceae based on rbcL gene se-
quences. American Journal of Botany 85: 1507–1516.
Seward, A. C. 1903. Fossil ora of Cape Colony. Annals of the South African
Museum 4: 1–122.
Seward, A. C., and S. O. Ford. 1906. e Araucarieae, recent and extinct.
Philosophical Transactions of the Royal Society, B, Biological Sciences 98:
305–411.
Smith, I. R., and D. Butler. 2002. e bunya pine— the ecology of Australia’s
other “living fossil” araucarian: Dandabah area— Bunya Mountains,
southeast Queensland, Australia. In R. L. Bieleski and M. D. Wilcox
[eds.], Araucariaceae, Proceedings of the 2002 Araucariaceae Symposium,
287–296. Araucaria-Agathis-Wollemia. International Dendrology Society,
Dunedin, New Zealand.
Smith, S. Y., and R. A. Stockey. 2001. A new species of Pityostrobus from the
Lower Cretaceous of California and its bearing on the evolution of Pinaceae.
International Journal of Plant Sciences 162: 669–681.
2018, Volume 105 • Andruchow- Colombo etal.—Late Cretaceous Araucaria lefipanensis from Patagonia • 21
Smith, S. Y., R. A. Stockey, G. W. Rothwell, and S. A. Little. 2017. A new spe-
cies of Pityostrobus (Pinaceae) from the Cretaceous of California: moving
towards understanding the Cretaceous radiation of Pinaceae. Journal of
Systematic Palaeontology 15: 69–81.
Spencer, A. R. T., G. Mapes, R. M. Bateman, J. Hilton, and G. W. Rothwell. 2015.
Middle Jurassic evidence for the origin of Cupressaceae: a paleobotanical
context for the roles of regulatory genetics and development in the evolution
of conifer seed cones. American Journal of Botany 102: 1–20.
Stewart, W. N., and G. W. Rothwell. 1993. Paleobotany and the evolution of
plants. Cambridge University Press, Cambridge, UK.
Stockey, R. A. 1975. Seeds and embryos of Araucaria mirabilis. American
Journal of Botany 62: 856–868.
Stockey, R. A. 1980. Anatomy and morphology of Araucaria sphaerocarpa
Carruthers from the Jurassic Inferior Oolite of Bruton, Somerset. Botanical
Gazette 141: 116–124.
Stockey, R. A. 1982. e Araucariaceae: an evolutionary perspective. Review of
Palaeobotany and Palynology 37: 133–154.
Stockey, R. A. 1994. Mesozoic Araucariaceae: morphology and systematic rela-
tionships. Journal of Plant Research 107: 493–502.
Stockey, R. A., and I. J. Atkinson. 1993. Cuticle micromorphology of Agathis
Salisbury. International Journal of Plant Sciences 154: 187–224.
Stockey, R. A., and H. Ko. 1986. Cuticle micromorphology of Araucaria de
Jussieu. Botanical Gazette 147: 508–548.
Stockey, R. A., and T. N. Taylor. 1978a. Cuticular features and epidermal patterns
in the genus Araucaria de Jussieu. Botanical Gazette 139: 490–498.
Stockey, R. A., and T. N. Taylor. 1978b. On the structure and evolutionary rela-
tionships of Cerro Cuadrado fossil conifer seedlings. Botanical Journal of the
Linnean Society 76: 161–176.
Stults, D. Z., B. J. Axsmith, T. K. Knight, and P. S. Bingham. 2012. e coni-
fer Araucaria bladenensis and associated large pollen and ovulate cones
from the Upper Cretaceous Ingersoll shale (Eutaw Formation) of Alabama.
Cretaceous Research 34: 142–148.
Sukh-Dev and Zeba-Bano. 1976. Araucaria indica and two other conifers from
the Jurassic- Cretaceous rocks of Madhya Pradesh, India. Palaeobotanist 25:
496–508.
Sun, T. X. 2008. Cuticle micromorphology of Nageia. Journal of Wuhan
Botanical Research 26: 554–560.
Taylor, T. M., E. L. Taylor, and M. Krings. 2009. Paleobotany, the biology and evo-
lution of fossil plants. Second Edition. Academic Press, Burlington, MA, USA.
Townrow, J. A. 1967. The Brachyphyllum crassum complex of fossil conifers.
Papers and Proceedings of the Royal Society of Tasmania 101: 149–172.
Vellekoop, J., F. Holwerda, M. B. Prámparo, V. Willmott, S. Schouten, N. R.
Cúneo, R. A. Scasso, and H. Brinkhuis. 2017. Climate and sea- level changes
across a shallow marine Cretaceous- Paleogene boundary succession in
Patagonia, Argentina. Palaeontology 60: 519–534.
Venables, W. N., and B. D. Ripley. 2002. Modern applied statistics with S. 4th ed.
Springer, NY, NY, USA.
White, C. T. 1947. Notes on two species of Araucaria in New Guinea and a
proposed new section of the genus. Journal of the Arnold Arboretum 28:
259–260.
Whitmore, T. C., and C. N. Page. 1980. Evolutionary implications of the dis-
tribution and ecology of the tropical conifer Agathis. New Phytologist 84:
407–416.
Whitmore, T. C. 1980. A monograph of Agathis. Plant Systematics and Evolution
135: 41–69.
Wilde, M. H., and A. J. Eames. 1948. e ovule and ‘seed’ of Araucaria bid-
willii with discussion of the taxonomy of the genus I. Morphology. Annals
of Botany 12: 311–327.
Wilde, M. H., and A. J. Eames. 1952. e ovule and seed of Araucaria bidwilli
with discussion of the taxonomy of the genus II. Taxonomy. Annals of
Botany 16: 28–49.
Wilf, P. 1997. When are leaves good thermometers? A new case for leaf margin
analysis. Paleobiology 23: 373–390.
Wilf, P., N. R. Cúneo, K. R. Johnson, J. F. Hicks, J. F. Wing, and J. D. Obradovich.
2003. High plant diversity in Eocene South America: evidence from
Patagonia. Science 300: 122–125.
Wilf, P., I. H. Escapa, N. R. Cúneo, R. M. Kooyman, K. R. Johnson, and A.
Iglesias. 2014. First South American Agathis (Araucariaceae), Eocene of
Patagonia. American Journal of Botany 101: 156–179.
Wilf, P., B. S. Singer, M. C. Zamaloa, K. R. Johnson, and N. R. Cúneo. 2010.
Early Eocene 40Ar/39Ar age for the Pampa de Jones plant, frog, and in-
sect biota (Huitrera Formation, Neuquén Province, Patagonia, Argentina).
Ameghiniana 47: 207–216.
Wilf, P., S. L. Wing, D. R. Greenwood, and C. L. Greenwood. 1998. Using fos-
sil leaves as paleoprecipitation indicators: an Eocene example. Geology 26:
203–206.
Wolfe, J. A. 1993. A method of obtaining climatic parameters from leaf assem-
blages. U.S. Geological Survey Bulletin 2040: 1–71.
Yang, Z. Y., J. H. Ran, and X. Q. Wang. 2012. ree genome- based phylogeny of
Cupressaceae s.l.: further evidence for the evolution of gymnosperms and
Southern Hemisphere biogeography. Molecular Phylogenetics and Evolution
64: 452–470.
