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Stockeystrobus gen. nov. (Cupressaceae), and the
evolutionary diversification of sequoioid conifer seed cones
Journal: Botany
Manuscript ID cjb-2016-0025.R1
Manuscript Type: Article
Date Submitted by the Author: 06-Apr-2016
Complete List of Authors: Rothwell, Gar; Ohio University, Department of of Enironmental and Plant Biology; Oregon State University, Department of Botany and Plant Pathology Ohana, Tamiko; National Museum of Nature and Science, Department of Geology and Paleontology
Keyword: conifer, Cupressaceae, pollination biology, Sequoioideae, seed cone
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Stockeystrobus gen. nov. (Cupressaceae),
and the evolutionary diversification of sequoioid conifer seed cones
Gar W. Rothwell a, b, *
and Tamiko Ohana c
aDepartment of Botany and Plant Pathology, Oregon State University, 2082 Cordley Hall,
Corvallis, OR 97330 USA; E-mail address: [email protected]
bDepartment of Botany, Ohio University, Athens, OH 45701 USA, E-mail address:
cDepartment of Geology and Paleontology, National Museum of Nature and Science, Tsukuba,
Ibaraki 305-0005, Japan; E-mail: [email protected]
* Corresponding author. Gar W. Rothwell, Department of Botany and Plant Pathology, Oregon
State University, 2082 Cordley Hall, Corvallis, OR, 97331, USA; [email protected]
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Abstract: An anatomically preserved seed cone from Late Cretaceous (Santonian-Coniacian)
sediments of the Yezo Group on the Japanese Island of Hokkaido documents additional diversity
among sequoioid conifers, and reveals previously unknown mechanisms for pollination and post-
pollination seed enclosure in the conifer family Cupressaceae. The cylindrical seed cone of
Stockeystrobus interdigitata gen. et sp. nov. consists of a central axis bearing helically arranged
bract-scale complexes. Individual complexes are tightly packed and peltate in form, with
completely fused bracts and scales. Peltate heads of adjacent complexes are attached to each
other by elongated interdigitating epidermal trichomes. Each complex bears 6 – 8 inverted seeds
on the adaxial surface of the inside of the peltate bract/scale complex head. Seeds occur in a
single row, are roughly disk shaped, with broad wings in the major plane of symmetry. The
nucellus is attached to the seed integument at the chalaza and free distally, with a convoluted
apex. This cone reveals greater diversity of sequoioid reproductive biology than is represented
among living species, and demonstrates that completely enclosed cones with well protected
seeds were produced by Late Cretaceous fossil conifers of the Cupressaceae.
Key Words: conifer, Cupressaceae, pollination biology, Sequoioideae, seed cone
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Introduction
The origin, evolution, and paleontological history of cupressaceous conifers have been
augmented substantially in the past few years by the discovery of new genera and species among
fossils of the Jurassic, Cretaceous, and Paleogene. Species of particularly informative systematic
significance are represented by reproductive organs (e.g., Florin 1938-45; Clement-Westerhof
and van Konijenberg-van Cittert 1991; Hernandez-Castillo et al. 2001; Hernandez-Castillo et al.
2005; Escapa et al. 2008; Rothwell et al. 2011; Bosma et al. 2012; Leslie et al. 2012). These
include the most ancient representatives of the family Cupressaceae (Escapa et al. 2008) and
specimens that display apparently pleisomorphic seed cone morphologies within the family
(Spencer et al. 2015). Anatomically preserved fossil seed cones serve as important intermediates
for a transformational series from Voltziaceae to Cupressaceae (Rothwell et al. 2011). The
largest number of such fossils either are assignable to, or have a great similarity to seed cones of
the subfamily Cunninghamioideae (e.g., Rothwell et al. 2011; Atkinson et al. 2014a, 2014b).
Fossil seed cones that conform to the cupressaceous subfamily Sequoioideae also are
commonly preserved in sediments that range from the Upper Cretaceous through the Neogene
(Ohsawa 1994; Stockey et al. 2005; Table 1), revealing that the clade previously was more
diverse and widespread in the Northern Hemisphere (Farjon, 2005; Stockey et al. 2005). There
is even evidence for the presence of the subfamily in the paleontological record of the Southern
Hemisphere (i.e., Australia; Peters and Christophel; (1978; Table 1). By contrast to the rich
fossil record, the subfamily Sequoioideae is currently represented by only three monotypic
genera (i.e., Sequoia sempervirens [D. Don] Endl., Sequoiadendron giganteum [Lindl.] J.
Buchholz, and Metasequoia glyptostroboides Hu and W.C. Cheng), each with an extremely
limited and apparently relictual geographical distribution (Farjon, 2005). Therefore, specimens
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of extinct species play an important role in revealing the patterns of sequoioid evolution and
phylogeny by documenting varying ranges of structural diversity within the subfamily through
time, by establishing patterns of species richness through time, and by highlighting a wider range
of morphology and reproductive biology than are represented by living species.
Carbonate marine concretions from several Late Cretaceous deposits on the northern
Japanese island of Hokkaido are one of the most valuable sources of fossils for characterizing
diverse assemblages of anatomically preserved, Upper Cretaceous plant remains. Since their
original discovery (Reiss 1907) and initial description by Stopes and Fujii (1910), specimens
from Hokkaido concretions have contributed important information for characterizing the
internal anatomy of late Mesozoic plants. These impressive permineralized assemblages from
Hokkaido were reviewed and summarized by Nishida (1991), but numerous additional plants
have been described subsequently.
The Hokkaido permineralized plant fossils include several species of seed cones assignable
to the Pinaceae, Cupressaceae, and Sciadopityaceae, which provide valuable information for
interpreting structural variation and evolution among conifers (Ohsawa 1994). While the largest
number of such seed cones is assignable to the cunninghamioid Cupressaceae, there are several
species of permineralized seed cones from Hokkaido and elsewhere that represent the subfamily
Sequoioideae (Table 1). In the current paper we describe a previously unknown type of
permineralized sequoioid seed cone from the Upper Cretaceous of Hokkaido, and interpret
several aspects of its relationships and reproductive biology. Interestingly, this species shows a
convoluted apex of the nucellus that reveals a specialized mode of pollination which is similar to
that which has been documented for some living and extinct species of Araucariaceae and
Podocarpaceae, but previously has not been found within the family Cupressaceae. This new
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conifer also has a distinctive mechanism for post-pollination sealing of the cone that may be a
novel specialization for species that are intermediate between the essentially open seed cones of
cunninghamioid Cupressaceae and the “juniper berries” that characterize some of the most
highly derived seed cones of cupressoid Cupressaceae (Lemoine-Sebastian 1969; Farjon 2005).
Occurrence, materials and methods
The anatomically preserved seed cone that forms the basis for this study was collected from
the Upper Cretaceous Yezo Group by Mr. Hiroshi Takahashi in a streambed near Tappu, Obira-
cho, Rumoi-gun on the Japanese Island of Hokkaido. Based upon the most recent stratigraphic
work for this area, sediments from which the fossil was collected are most likely part of the
Hoborogawa Formation (Yezo Group), which is considered to be Coniacian – Santonian in age
(Takashima et al. 2004). The cone was labeled “inflorescence?” among specimens of the
Kimura collection of anatomically preserved plants from marine nodules that are housed in the
Department of Geology and Paleontology, National Museum of Nature and Science, Tsukuba,
Japan. The specimen was prepared many years ago by the junior author. It is represented by 30
microscope slides of mounted cellulose acetate peel sections prepared from a single seed cone, as
well as three unprepared segments of the cone. All of these cone segments and microscope
slides, as well as eight additional segments of the concretion (that do not contain parts of the
cone), are identified as National Museum of Nature and Science specimen number NSM PP-
9373.
The cone was exposed in oblique section by the original saw cut. The segments were glued
back together, leaving a space of the appropriate thickness to accommodate the saw kerf (see
Fig. 3C), and then recut into six segments (shown in Fig. 1A) to expose the specimen in cross
section. A small number of anatomical sections (i.e., peel preparations) were prepared from
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several of the exposed surfaces to document cone features in cross section. Microscope slides
were made from those peels. Two 25 x 75 mm slides were made of peels from the apical-most
segment (at the top of Fig. 1A; i.e., slides C1-1 and C1-2) and two 25 x 77 mm slides were made
of peels from the adjoining face of the next segment (i.e., slides C2-1 and C2-2). These revealed
tangential sections near the apex of two bract/scale complexes that are attached near the apex of
the cone axis (i.e., Figs. 3A, 5A). Seventeen 50 x 75 mm slides were made of peels showing
cone cross sections from surfaces of other segments (i.e., slides a-1, 1-1, 1-2, 1-77, 2, 2-1, 2-2, 3,
3-2, 4, 4-2, 5, 5-1, 5-2, 6, 6-1, and 6-2). The exact surfaces from which the peels were made are
not known because those surfaces are no longer exposed. The cone segments were then glued
back together, leaving the appropriate thickness to accommodate material lost in the saw cuts,
and the specimen was re-cut to expose the cone in slightly oblique radial view (see Fig. 1A).
Four 50 x 75 mm slides were made from peels (two from each side of the longitudinal saw cut
(i.e., slides L1-1, L1-2, L2-1, L2-2). The cone was also ground from the outside to expose the
bract-scale complexes in tangential views (e.g., Fig. 3C), and five 25 x 75 mm slides were made
from those peels (i.e., slides T1 – T5).
Peels were made using the cellulose acetate peel technique (Joy et al. 1956). Images were
captured with transmitted light at Oregon State University by a Better Light digital scanning
back (Better Light, Placerville, California) focused through a Leitz Aristophot large-format
camera using either Summar macro lenses or a Zeiss Model L compound microscope, and
processed using Adobe Photoshop (Adobe, San Jose, California, USA). Line diagrams of
bract/scale complex vascular tissue were prepared by tracing xylem bundles from photographs of
the relevant levels.
Systematic Paleobotany
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Order Coniferales sensu Eckenwalder
Family Cupressaceae Gray
Subfamily Sequoioideae Saxton
Genus Stockeystrobus Rothwell & Ohana gen. nov.
Generic diagnosis: Cylindrical sequoioid seed cone with large number of helically
arranged peltate bract/scale complexes. Adjacent peltate heads closely spaced, connected by
interdigitating epidermal trichomes. Vascularization of complexes diverging as single radial
bundle; dividing laterally to produce adaxial row of terete bundles, and vertically to produce
single abaxial bundle; abaxial bundle dividing distally to form concentric ring within peltate
head. Inverted seeds borne in single row on inside of adaxial surface of peltate head; seeds with
nucellus free from integument distal to chalaza; nucellar apex convoluted.
Etymology: The generic name Stockeystrobus (Stockey + strobus [= cone]) is proposed in
honor of Dr. Ruth A. Stockey, Oregon State University, Professor Emerita from the University of
Alberta, for her recognition of the global occurrence of anatomically preserved plant remains in
Jurassic-Neogene marine deposits worldwide, her tireless development of the paleobotanical
history of Canada, and her transformational contributions to the understanding of conifer
structure, phylogeny and evolution through time.
Type species: Stockeystrobus interdigitata Rothwell & Ohana sp. nov., (Figs. 1-5).
Specific diagnosis: Cone >4.7 cm long, ~2.7 cm in diameter; woody axis with complete
cylinder of secondary xylem, scattered sclereids in parenchymatous pith; cortical resin canals
absent. Complex ground tissue parenchymatous, with numerous resin rodlets, abaxially
positioned resin canals in peltate head; abaxial hypodermis of closely spaced parenchyma and
sclerotic bundles. Conspicuous epidermal cells elongating at lateral margins of bract/scale head
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to form interdigitating trichomes. Seeds six – eight per bract/scale complex, disc-shaped with
broad wing surrounding body.
Holotype hic designatus: National Museum of Nature and Science specimen number
NSM PP-9373.
Repository: Department of Geology and Paleontology, National Museum of Nature and
Science, Tsukuba, Ibaraki 305-0005, Japan.
Type locality: Stream bed near Tappu, Obira-cho, Rumoi-gun on the Japanese Island of
Hokkaido, Japan.
Stratigraphy and age: Hoborogawa Formation, Upper Yezo Group; Late Cretaceous
(Conacian – Santonian; Takashima et al. 2004).
Etymology: The specific epithet interdigitata refers to the inter-fingering epidermal
trichomes that connect adjacent bract/scale complex heads, and that provide complete post-
pollination enclosure of the seeds.
Description
The specimen is cylindrical, at least 4.7 cm long and 2.7 cm in diameter, with parallel sides
and a rounded apex (Fig. 1A). The cone base is not present, so the original length of the
specimen is longer than the preserved segment. More than 40 helically arranged, peltate
bract/scale complexes (Figs. 1A, 1B) diverge from the woody axis, each producing a single row
of six to eight seeds that fill the interior of the cone (Figs. 1A, 1C, 5C). Tangential views of the
cone reveal that each complex head is laterally elongated and either is adjacent to and/or closely
spaced with respect to the heads of adjacent complexes (Fig. 3C). This includes the apical-most
complexes, which are fertile and appear to be well formed (Figs. 1A, at top; Fig. 5A).
The pith of the cone axis is parenchymatous with small clusters of scattered sclereids (Fig.
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2A, at red arrowhead). Many pith parenchyma cells have dark contents, but some display clear
lumens (Figs. 2A, 2B). Primary xylem is difficult to identify (e.g., Fig. 2B). Vascular tissue
surrounding the pith consists of a continuous cylinder of secondary xylem made up of radially
aligned tracheids, 24 - 49 mµ in diameter, that are rectangular to oval in cross section. Regular
radial rows of secondary tracheids extend from near the pith to the periphery of the zone on some
radii (Fig. 2A). On other radii (Fig. 2A, upper right; 2B) the evenness of the rows is disrupted
about eight to twelve cells from the pith, and there is an abrupt change in the size of the tracheids
in each row (Fig. 2B), suggesting the presence of an incomplete possibly traumatic growth ring.
However, tracheids throughout the wood are inconsistently preserved as the result of what
appears to be destructive calcite recrystallization (Figs. 2A, 2B), irregularities in the tracheid
rows undoubtedly having been amplified by taphonomy. Secondary tracheids display wall
thickening patterns that range from scalariform (Fig. 2D) to uniseriate, circular bordered pits
(Fig. 2D, at blue arrowhead).
Tissues to the periphery of the woody cylinder are incompletely preserved, so that vascular
cambium, secondary phloem cannot be distinguished from cells of the primary cortex (Fig. 2A).
There is no evidence of resin canals in the cone axis. A continuous zone of periderm made up of
several rows of radially aligned cells is present near the margin of the cone axis (Fig. 2A, at p).
Bract/scale complexes diverge from the axis at about 90o (Figs 1A and 1B, at red
arrowheads) as a slender woody stalk (Figs. 1A, 1B, 2C). Stalks extend for approx. 5 mm before
broadening into a head that measures ca. 15 mm wide, 10 mm high, and 2 mm thick, and that lies
closely adjacent to the heads of adjacent complexes (Figs. 1A and 1B, at black arrowheads).
Internally, the stalk is dominated by a radial woody trace (Figs. 1B, 2C, 4A) that is surrounded
by a narrow zone of incompletely preserved ground tissue like that of the cone axis (Fig. 2C),
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including a narrow zone of periderm near the surface of the axis (Fig. 2C, at p).
Vascular tissue to each bract/scale complex diverges from the axis as a radial rod (Figs. 1A
and 1B at t, 2C; 4A) that divides at the base of the peltate head to produce a line of adaxial
collateral bundles (Figs 1C-E, 4B, 4C) and a single abaxial collateral bundle (Figs 1C and 1D, at
black arrowheads, 4B). In cross sections of the cone (Fig. 1C) the vascular tissue forms a T-
shaped configuration at this level (Fig. 4B). Bundles are represented by radial rows of tracheids
(Fig. 3B). The abaxial bundles diverge from the lateral margins of central trace to produce the
row of bundles in the complex head (Figs. 1D, 1E; 4B). In the most distal sections the adaxial
row (Fig. 4D) forms an irregular line (Figs. 3A, at green arrowheads; 4D, 5A) in which the
bundles are roughly inverted in orientation (i.e., with the position of the phloem toward the
adaxial surface; directions of green arrowheads in Fig. 3A). The abaxial bundle divides at a
more distal level (Fig. 4C) to produce a concentric ring of collateral bundles (Figs. 3A, 4C, 4D)
in which the positions of phloem are oriented toward the periphery of the ring (Fig. 3A, in
directions of red arrowheads).
Ground tissue of the complex head is often incompletely preserved (Figs 3A-D, 3F), but
when well preserved it consists of closely spaced parenchyma cells. There are a large number of
resin rodlets in the peltate heads (Fig. 3G), which are quite prominent in those complexes where
parenchyma is absent or incompletely preserved (Fig. 3F). Toward the abaxial surface of the
peltate head the parenchyma cells are somewhat smaller than elsewhere, and form a hypodermis
in which there is a row sclerenchyma bundles (Figs. 3F, 3G at arrow). No resin canals have been
identified in the complex stalks, but there are resin canals toward the abaxial side of in the peltate
complex heads (e.g., Figs. 1E and 3G, at r). Proximal to the peltate head, the epidermis is made
up of small cells and is inconspicuous (Figs. 3F, at bottom; 3G, at right). By contrast, cells of the
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adaxial epidermis become larger and much more prominent near the head (Figs. 3E, at upper left;
3F, at top; 3H, at left). Such epidermal cells have an inflated appearance (e.g., Figs. 3E, 3F, 3H).
All epidermal cells become much more elongated at the lateral margins of the peltate head (Fig.
3I), and interdigitate (Figs. 3C-3E, 3H). So tightly interlocking are the trichomes of adjacent
complexes (Figs. 3E, 3H) that the interior of the cone must have been almost completely sealed
prior to seed dispersal. Interlocking trichomes are unicellular, have a wall at the base,
intermittently contain dark contents (Figs. 3E, 3H, 3I), and range up to 500 µm long.
The interior of the cone is tightly packed with inverted seeds that are elongated in
longitudinal sections and cut in the minor plane of seed symmetry (Figs. 1A, 1B, 5C, 5E).
Individual seeds are attached in a single row to the adaxial surface on the inside of the peltate
bract/scale complex head (Fig. 5A), and oriented with the micropyle directed back toward the
cone axis (Fig. 5C). In cross sections the seeds appear to be flattened because of the occurrence
of a broad wing that surrounds the roughly cylindrical seed body (Figs. 5B, 5D), and that gives
the seeds a round/oval outline in longitudinal sections of the major plane of symmetry (Fig. 5D,
at bottom). Seeds measure ca. 5.5 mm long, 5.5 mm wide in the major plane of symmetry, and
1.0 mm thick in the minor plane of symmetry.
The integument consists of an outer epidermis (Fig. 5F, at arrows) a zone of sclereids two
to three cell layers thick, and an inner zone of thinner walled cells that are incompletely
preserved (Figs. 5C-5G). A prominent cuticle is preserved at the inner margin of the integument
(Figs. 5E-5G). At the chalaza, the sclerotic zone of the integument is concave in longitudinal
sections (Figs. 5C, 5E), and in areas of seed attachment each seed appears to be elevated on a
mound of bract/scale complex tissue (Fig. 5A). No vascular tissue has been identified extending
toward or entering the base of the seeds.
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The nucellus is attached to the integument only at the base of the seed (Fig. 5E). It is free
distally, which is emphasized by a prominent nucellar cuticle and an inner integumentary cuticle
(Figs. 5E, 5F). There are two or three layers of nucellar cells that surround a central area that
either is empty (Fig. 5F) or that contains a granular material (Fig. 5E). The latter may represent
the remnants of cellular megagametophyte tissue that otherwise is not preserved. Alternatively,
the ovules may have been preserved at the free nuclear stage of megagametophyte development.
At the apex of the seed the nucellus consists of incompletely preserved cells, and has a distinctly
undulating outer margin of (Fig. 5G). Whether the central area represents a pollen chamber or a
cellular nucellar apex could not be determined from the available specimens. However, there is
no evidence of pollen within the apical region of the nucellus or elsewhere within the cone or
seeds.
Discussion
Compact seed cones with large numbers of helically arranged bract/scale complexes are
produced by conifers of the Voltziaceae, Cheirolepidiaceae, Pinaceae, Araucariaceae,
Sciadopityaceae, Cupressaceae, and Podocarpaceae (i.e., Saxegothaea), but many taxa have only
one or two seeds per bract/scale complex (i.e., species of Cheirolepidiaceae, Pinaceae, and
Saxegothaea; Sporne 1965; Rothwell et al. 2005; Escapa et al. 2012; Leslie et al. 2012), whereas
Stockeystrobus has six to eight. Voltziacean seed cones typically are long narrow structures with
a lax arrangement of bract/scale complexes, distinctive evidence of vegetative scales, one to
three seeds per fertile short shoot or ovuliferous scale complex, and are much more ancient than
the new cone described here (e.g., Florin 1948-51; Mapes and Rothwell 1984; Clement-
Westerhof 1988; Hernandez-Castillo et al. 2001; Rothwell et al. 2005; Looy, 2007; Leslie 2011).
Compact cones with larger numbers of seeds, like Stockeystrobus, are found in the families
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Sciadopityaceae and Cupressaceae (e.g., Hirmer, 1936; Sporne, 1965). Among such species,
only cones of Cupressaceae subfamily Sequoioideae and a few Cretaceous cupressaceous
conifers of uncertain affinities (e,g., Cunninghamites lignitum [Sternberg] Kvaček) consist of
cones with numerous helically-arranged complexes which bear several inverted seeds that are
adaxially attached to the underside of a peltate head (Hirmer, 1936; Schulz and Stützel 2007).
Cunninghamites originally was thought to be closely related to the cunninghamioid
Cupressaceae (e.g., Cuninghamites K.B. Presl ex Sternberg) on the basis of similar vegetative
features. However, the occurrence of specimens with a solitary pollen cone attached to a leafy
shoot (i.e., Cunninghamites oxycedrus Presl ex. Sternberg), and with seed cones composed of
helically arranged, peltate bract/scale complexes attached to leafy shoots (e.g., Cunninghamites
lignitum, C. squamosus Heer; Table 1; Kvaček 1999; Bosma et al. 2012) suggest that those
species could have closer affinities to the cupressaceous subfamily Sequoioideae (Table 1).
Krassilovia mongolica Herrera, Shi, Leslie, Knopf, Ichinnorov, Takahashi, Crane et
Herendeen (Herrera et al. 2015) is an Early Cretaceous (Aptian-Albian) fossil conifer with seed
cone characters that are somewhat reminiscent of Stockeystrobus and other genera of the
Sequoioideae. As also is common among cupressaceous seed cones, those of K. mongolica are
ovoid with helically arranged bract/scale complexes (Farjon 2005). In agreement with species of
Sequoioideae, the ovuiferous scale of K. mongolica is roughly peltate with a row of five inverted
and winged seeds attached adaxially to the underside of the peltate head (Herrera et al. 2015).
However, K. mongolica has a narrow bract that separates from the complex and displays a free
tip like that of Cryptomeria japonica (Hirmer 1936; Takaso and Tomlinson 1989) rather than the
completely fused bract and scale of sequoioid cupressaceous seed cones (Table 1).
Krassilovia has five extremely distinctive spines at the margin of the peltate scale head that
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are reminiscent of those on the ovuliferous scale of Cryptomeria japonica and many Permian and
Triassic species of Voltziaceae (Clement-Westerhof, 1988; Rothwell et al. 2005), but that
interlock with adjacent scales in a unique fashion not known from any other fossil or living
conifer (Herrera et al. 2015). Moreover, seed cones of Krassilovia disaggregate at maturity to
shed individual bract/scale complexes (Herrera et al. 2015), as do some species of some
taxodiaceous Cupressaceae (e.g., Taxodium disticum [L.] Rich.). If vegetative leafy shoots
commonly associated with fossils of Krasslovia and assignable to Podozamites Braun represent
the same plant as K. mongolica, then that species may be transitional between Voltziaceae and
stem group Cupressaceae (Andrew Leslie, pers. comm., January 2016), but K. mongolica does
not have the appropriate combination of characters to be assigned to the Sequoioideae.
Stockeystrobus shares with most other genera of Cupressaceae, subfamily Sequoioideae a
helical arrangement of bract/scale complexes, inverted seeds, and seeds that are attached in a
single row (Table 1; Farjon 2005; Stockey et al. 2005). While cylindrical seed cones, like that of
S. interdigitata are not characteristic of other species within the subfamily, (Table 1; Farjon
2005) some species occasionally produce cones that approach a cylindrical shape (e.g., see
Sequoiadendron giganteum; https://www.google.com/#q=Sequoiadendron+giganteum).
Stockeystrobus also has a unique vascular architecture of the bract/scale complex. As is
common for species of Cupressaceae, the bract/scale complex vasculature of S. interdigitata
diverges from the cone stele as a single bundle (Fig. 2C; Lemoine-Sebastian 1968, 1969) that
divides distally (Table 1; Lemoine-Sebastian 1968, 1969; Ohsawa 1994; Rothwell et al. 2011;
Atkinson et al., 2014a, 2014b). As interpreted by Lemoine-Sebastian, the adaxial bundles would
represent the ovuliferous scale, while the abaxial bundle represents the bract trace (Lemoine-
Sebastian 1968, 1969). Only in Stockeystrobus does the bract/scale complex vascular bundle
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first divide to produce a row of adaxial “ovuliferous scale trace” bundles and a single abaxial
“bract trace” bundle (Figs. 1C-1E), with the abaxial bundle dividing more distally to produce a
concentric ring of bundles toward the bract/scale apex (Fig. 3A, 4).
An additional distinctive feature of the bract/scale vasculature of Stockeystrobus is the
orientation of the collateral bundles near the bract/scale apex. The adaxial row consists of
cauline bundles with the position of the phloem oriented toward the adaxial surface (orientation
of green arrow heads in Fig. 3A), whereas the abaxial bundles form a concentric ring with the
position of the phloem oriented toward the outside of the ring (orientation of red arrowheads in
Fig. 3A). This distal bract/scale complex vascular tissue configuration is not known elsewhere
among seed cones of the Cupressaceae (Lemoine-Sebastian 1968, 1969; Ohsawa 1994).
The highly convoluted, invaginated, or “stipitate” (Eames 1913) apical region of the
nucellus of S. interdigitata (Fig. 5G) is a particularly distinctive character of Stockeystrobus.
Among living and extinct conifers such a convoluted nucellus occurs most commonly in the
Araucariaceae (Stockey 1975, 1978). In Araucariaceae this character is associated with a
specialized mode of pollination wherein the nucellus extends out of the micropyle of the ovule;
pollen lands on the cone scale or extended nucellar apex, and then the nucellus is withdrawn
back into the integument as pollen tubes grow toward the megagametophyte (Eames 1913). As
illustrated by Eames (1913) for Agathus australis, withdrawal of the nucellar apex back through
the micropyle into the seed cavity results in a convoluted surface of the nucellus in post-
pollination stages of development (Plate I, Fig. 4 of Eames 1913; Owens et al. 1995). A similar
pollination mechanism appears to characterize Saxegothaea conspicua Lindley (Tison, 1908;
Chamberlain, 1935), but it is unclear whether the post-pollination nucellus displays a highly
convoluted apical region. Although the structure of the pollen chamber has been characterized
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for several species of both living and extinct Cupressaceae e.g., Takaso and Owens 1996; Owens
et al. 1998; Tomlinson 2012; Spencer et al. 2015), Stockeystrobus digitata is the first species of
the family in which this character has been found. This feature could be interpreted as either a
strong indication that a specialized pollination mechanism like those of Araucariaceae and
Saxegothaea (Tison, 1908; Owens et al. 1998) also was characteristic of some Cretaceous
species of the subfamily Sequoioideae, or that it is plesiomorphic among the (Sciadopityaceae +
Cupressaceae) + (Araucariaceae + Podocarpaceae) clade (Leslie et al., 2012) as a whole.
Perhaps the most novel feature of Stockeystrobus interdigitata is the closely spaced and
elongated epidermal trichomes that occur along adjacent surfaces bract/scale complexes (Figs.
3C, 3D, 4B-D), and that tightly interlock (Fig. 3G) to seal the interior of the cone. Such
trichomes are unicellular and represent elongations of the ordinary epidermal cells found
elsewhere on the bract/scale complexes. Whereas closely adjacent (e.g., in living species of
Sequoioideae prior to seed dispersal) and even laterally fused bract/scale complexes (e.g., in
species of Juniperus) are common in the family Cupressaceae (Farjon 2005), Stockeystrobus is
the only genus in which the closely adjacent complexes are connected by tightly interlocking
epidermal trichomes to seal the interior of the cone and presumably to protect the developing
seeds from predation.
Within Cupressaceae some cones have ovuliferous scales that either develop relatively late
with respect to other cone structures, or remain diminutive to maturity, or are so highly fused to
the bract that the ovuliferous scale complex appears to be a single structure (e.g., Takaso and
Tomlinson 1989a, 1989b, 1990, 1991, 1992; Schulz and Stützel 2007). This has led some
authors to suspect that some conifer seed cones may be equivalent to simple, rather than
compound shoot systems, and therefore have an independent evolutionary origin from conifers
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that have compound seed cones (e.g., Tomlinson et al. 1993). However, more recent studies that
include transformational series of cone scale morphologies from Voltziaceae to Cupressaceae
(Rothwell et al. 2011), and that emphasize comparative developmental morphology (Schulz and
Stützel 2007) and the regulatory genetics that underlies variations in mature cone scale structure
(Rothwell et al. 2011; Rudall et al. 2011; Spencer et al. 2015), reveal that all cupressaceous
cones are variously modified compound shoot systems as originally hypothesized by Florin
(1951, 1954) and summarized by Rothwell et al. (2011). These studies explain our inability to
recognize morphologically distinct bracts and ovuliferous scales in the compound seed cones of
sequoioid Cupressaceae, including Stockeystrobus.
Throughout the history of lignophytes there has been a progressive trend toward
condensation of seed-producing structures into increasingly modified and compact fertile
structures (e.g., Rothwell 1982) that represent parallel evolution (Taylor and Taylor 2009) for
heightened levels of protection of developing ovules and seeds (Leslie 2011). Notable examples
of those are the cupulate seed bearing organs produced by a wide variety of extinct plants
referred to as seed ferns (Taylor et al. 2006; Taylor and Taylor 2009; Taylor et al. 2009;
Rothwell and Stockey 2016), and the compact seed cones of Bennettitales (Wieland 1906).
More specifically to the focus of the current study, ovulate fructifications of the most ancient
conifers are lax aggregations of either fertile zones (e.g., Thucydia mahoningensis Hernandez-
Castillo, Rothwell et Mapes; Hernandez-Castillo et. al. 2001) or compound cones (e.g., Emporia
[Mapes & Rothwell] Rothwell & Mapes spp.; Hernandez-Castillo et al. 2009) that become
successively more compact through time (Leslie, 2011).
This trend is clearly reflected by the increasingly compact and consolidated seed cones at
successively more distal levels of the cupressaceous phylogenetic tree (i.e., from Subfamily
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Cunninghamioideae to subfamily Sequoioideae to tribe Cupresseae of subfamily Cupressoideae;
Farjon 2005). Among living species of conifers, seed protection is achieved either by having the
complexes closely-spaced prior to seed dispersal (e.g., Sequoioideae), by the production of
spine-like structures on the cones (e.g., Pinus; Coffey et al. 1999; and possibly Krasslovia;
Herrera et al. 2015) or by the close spacing and fusion of adjacent complexes (e.g., Juniperus
L.). Sealing of the cone by tightly interlocking epidermal trichomes of closely adjacent
bract/scale complex heads, and pollination via a mechanism that produces the highly convoluted
apical surface of the nucellus (e.g., Eames, 1913) as illustrated by Stockeystrobus, reveals the
occurrence of a combination of reproductive specializations that previously have been unknown
among living or extinct cupressaceous cones. These mechanisms not only emphasize that that
the subfamily Sequoioideae was more systematically diverse in the Late Cretaceous than in the
modern flora, but also reveals that the extinct sequoioid conifers were more biologically diverse
as well.
Acknowledgements
We are most grateful to Ashley A. Klymiuk, University of Kansas, Selena Y. Smith,
Michigan State University, and Stefan A. Little, Université Paris Sud for inviting us to
participate in this tribute to Ruth A. Stockey. The senior author thanks Dr. Toshihiro Yamada,
Kanazawa University, Kanazawa, Japan, and Dr. Harufumi Nishida, Chuo University, Tokyo,
Japan, for providing detailed background information on the geological setting and mode of
fossilization for the marine plant-bearing deposits of Hokkaido during field collecting in
September 2015 and for their continuing assistance in interpreting the Hokkaido fossils. Dr.
Atsushi Yabe, National Museum of Nature and Science, Japan generously provided access to
specimens and facilitated the loan of material, and Brian Atkinson made helpful suggestions for
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improving presentation of the work. We also thank Dr. Andrew Leslie, Brown University, Dr.
Jiri Kvaček, National Museum, Prague, and Ruth A. Stockey, Oregon State University for their
instructive discussions about Cretaceous conifer seed cones, and Dr. Ignacio Escapa, CONICET-
Museo Paleontologico Egidio Feruglio, and a second anonymous reviewer for their helpful
critiques of the manuscript.
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Table 1. Morphological/anatomical characters of living and extinct seed cones that conform to the sequoioid Cupressaceae. Characters of Stockeystrobus interdigitata and concordant characters of other
species in bold type.
Character
Species
Geol.
Age/range Shape
Length
(mm)
Max. diam.
(mm)
Complex
arrang.
No. of
complexes
Axial
resin
canals
Complex
form
Interdigitate
tricomes
V.T. in
peltate
head
Seeds
per
scale
Rows of
seeds
Seed
orient.
Seed
wing
Convoluted
nucellar
apex
Stockeystrobus
interdigitata
Late
Cretaceous
(Coniacian-
Santonian)
cylindrical >42 24 helical >40 - peltate +
adaxial row
+ abaxial
ring
6-8 1 inverted wide +
1Archicupressus
nihongii
Late
Cretaceous
(Coniacian-
Santonian)
ellipsoidal 38 17 helical 12+ + peltate
with apical
spine
- reniform
ring 1 1 erect
narrow
or
absent
-
2Austrosequoia
wintonensis Late
Cretaceous ellipsoidal 9-16 6-11 helical 29-49 -
peltate
with distal
groove
- 2 bundles 4-7 1 inverted ? ?
3Cunninghamites
lignitum
Late
Cretaceous
(Cenomanian)
ovoid 55-65 25-35 helical 45-55 ? peltate
with apical
spine
- ? 4 1 ? absent ?
4Cunninghamites
squamosus Late
Cretaceous ovoid 45-63 30-42 helical
>34
(≤52) ?
peltate with apical
spine
- ?
2
(or
more) 1 ? ? ?
5Drumhellera
kurmanniae
Late
Cretaceous
(Campanian)
ellipsoidal 20-30 17-23 helical ≤ 27 + peltate - flattened oval
ring ≤ 13 2 inverted wide ?
6Haborosequoia
nakajimae
Late
Cretaceous
(Santonian)
ovoid ? 24 helical 15+ + peltate - flattened oval
ring ? ? inverted? ? ?
7Metasequoia milleri Eocene
subglobose
-cylindrical ~25 ~17 decussate ≤ 30 +
peltate with distal
groove
- flattened oval
ring 4+ 1 inverted wide -
8Nepharostrobus
bifurcatus
Late
Cretaceous ellipsoidal >50 15 helical >40 + peltate -
flattened oval
ring ? ? ? ? ?
8Nepharostrobus
cliffwoodensis Late
Cretaceous ellipsoidal >15 14 helical >20 + peltate - reniform ring 5-7 ? inverted?
narrow/
absent ?
9Parataxodium
wigginsii Late
Cretaceous ellipsoidal ~13 ~10 ? 20-30? ? peltate - ? ? ? ? ? ?
10Sequoia-like
Hokkaido cone Late
Cretaceous ellipsoidal 22 17 helical >15 -
Peltate with distal
groove
- reniform ring ? ? ? ? ?
10Yezosequoia
shimanukii
Late
Cretaceous
(Coniacian-
Santonian)
ellipsoidal 22-25 25-29 helical ~35 + peltate
with apical
spine
- flattened oval
ring 4 1 inverted narrow ?
11Yubaristrobus
nakajimae
Late
Cretaceous
(Coniacian-
Santonian)
ellipsoidal 45 26 helical 25+ + peltate
with distal
groove
-
oval ring +
intern.
bundles
3-4 1 erect narrow ?
7, 12, 13Metasequoia
glyptostroboides recent ellipsoidal 15-30 15-18 decussate 18-25 -
peltate
with distal
groove
- reniform
ring 6-8 1 inverted
narrow-
wide -
12, 14Sequoia
sempervirens recent ellipsoidal 15-30 13-18 helical 18-25 -
peltate with distal
groove
- reniform
ring 6-8 1 inverted narrow -
12, 14Sequoiadendron
giganteum recent ellipsoidal 30-95 25-65 helical 28-45 -
peltate with distal
groove
- flattened oval
ring 8-10 2 inverted wide -
1Ohsawa 1992;
2Peters and Christophel 1978;
3Kvaček 1999;
4Bosma 2012;
5Serbet 1997;
6Ohsawa et al. 1992a;
7Basinger 1984;
8LaPasha and Miller 1981;
9Arnold and Lowther 1955;
10Ohsawa et al. 1992b;
11Ohsawa et al. 1993;
12Lemoine-Sebastian 1968;
13Hollick and Jeffrey 1909;
14Hirmer 1936.
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Figure captions
Fig. 1. Stockeystrobus interdigitata gen. et sp. nov. Holotype, National Museum of Nature and
Science specimen number NSM PP-9373. A, Slightly oblique longitudinal section of cone, near-
radial at apex and radial at base, showing cylindrical shape, peltate (red arrowhead) bract-scale
complexes with heads (h) that are connected by interlocking trichomes (black arrowheads),
radial complex traces (t) diverging from axis (a) and numerous inverted seeds. Five horizontal
white lines across cone represent cross sections (e.g., Fig. 1B) made before cone was
reassembled, leaving spaces to compensate for thickness of cone removed. Slide L1-1 x3. B,
Cross section of cone showing axis (a), diverging complex traces (t), one attached peltate bract-
scale complex (red arrowhead), and numerous inverted seeds in growth position on the inner
surface of peltate complex heads (h). Black arrowheads identify positions of interlocking
trichomes that attach adjacent heads. Slide 4 x4.4. C, Cross section of cone showing bract/scale
trace (t) at level where trace begins to divide to produce adaxial bundle (black arrowhead) and
several abaxial bundles. Slide 1-77 x11. D, Cross section of cone showing complex head at
slightly more adaxial level than Fig. 1C, where adaxial bundle (arrowhead) and several adaxial
bundles already have separated. Note several seeds in position of attachment, and resin canal (r)
in ground tissue. Slide 1-2 x8. E, Cross section of cone showing complex head at slightly more
adaxial level than Fig. 1D, where adaxial bundles form single row, and there is one adaxial
bundle (at arrowhead). Note histology, resin canal (r), and periderm on adaxial surface of head.
Slide 2-1 x9.
Fig. 2. Stockeystrobus interdigitata gen. et sp. nov. Holotype, National Museum of Nature and
Science specimen number NSM PP-9373. A, Cross section of cone axis showing pith, cylinder
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of wood, and primary cortex both inside and outside of radially aligned periderm cells. Red
arrowhead identifies sclereids in pith. Slide A1 x35. B, Enlargement of pith and wood of cone
axis, showing parenchyma with and without dark internal contents, and rows of radially aligned
secondary tracheids. Gaps between rows of tracheids represent uniseriate rays. Slide A1 x80. C,
Oblique cross section of complex stalk enlarged from Fig. 2B, showing radial structure with
abundant wood, primary cortex, and periderm (p). Slide 4 x28. D, Radial section of wood
showing tracheids with scalariform thickenings and uniseriate bordered pits (blue arrowhead).
Slide 1-2 x380.
Fig. 3. Stockeystrobus interdigitata gen. et sp. nov. Holotype, National Museum of Nature and
Science specimen number NSM PP-9373. A. Tangential section of cone showing peltate head of
complex in cross section, and distal to seed attachment. Note row of vascular bundles toward
adaxial surface (green arrowheads) and ring of vascular bundles (red arrowheads) toward abaxial
surface. Ground tissues incompletely preserved. Arrowheads point in direction that xylem
maturation occurred and secondary xylem tracheids were added. Slide C2-1 x37. B,
Enlargement of vascular bundle at lower right of Fig. 1A, showing rows of secondary tracheids
that reveal bundle orientation, and spaces between tracheid rows that represent uniseriate rays.
Slide C2-1 x140. C, Tangential section of cone showing adjacent complex heads (h) with
incompletely preserved ground tissues and dense interlocking trichomes on adjoining surfaces.
Horizontal white line represents position of saw cut. Slide T5 x9. D, Enlargement of trichomes
interconnecting adjacent complex heads (h) in Fig. 3D. Slide T5 x16. E, Interdigitating
trichomes at lateral margins of adjoining peltate bract/scale complex heads. Note how epidermal
cells in adjacent regions (upper left) increase in size to form the elongated trichomes. Slide L1-1
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x75. F, Cross section of complex at level between position of seed attachment and level where
adjacent complexes are connected by interlocking trichomes. Adaxial epidermis consists of
papillate cells. Note abaxial hypodermis of tightly-packed parenchyma and fibers, adjacent resin
canals (r), and internal zone of less completely preserved tissue that shows prominent resin
rodlets. Slide 3-2 x40. G, Longitudinal section of well-preserved complex head with distal
surface at right. Note longitudinal rows of ground parenchyma with resin rodlets, hypodermis of
tightly packed parenchyma and fibers, and resin canal (r). Slide 5-2 x32. H, Cross section of
cone showing interlocking epidermal trichomes that connect adjacent bract/scale complex heads
(h). Slide 1-2 x28. I, Interdigitating trichomes and adjacent mesophyll cells at margin of peltate
bract/scale complex head, showing that each trichome consists of single enlarged epidermal cell.
Slide 1-77 x130.
Fig. 4. Line diagram tracings of vascular system in holotype of Stockeystrobus interdigitata gen.
et sp. nov. All from cross sections of cone, x5. National Museum of Nature and Science
specimen number NSM PP-9373. Bract/scale margin drawn in zig-zag pattern where lined with
interdigitating trichomes; xylem bundles represented in black. A, Proximal level of stalk at level
where xylem forms a rod with abundant secondary xylem. Slide 3. B, Roughly T-shaped bundle
dividing at base of peltate head, producing row of abaxial bundles and single adaxial bundle.
Slide 5-2. C, Slightly more distal section than in Fig. 4B, showing row of abaxial bundles, and
adaxial bundles dividing to form ring. Slide 2-1. D, Distalmost section of peltate head, showing
abaxial row and adaxial ring of xylem bundles. Slide C2-1.
Fig. 5. Stockeystrobus interdigitata gen. et sp. nov. Holotype, National Museum of Nature and
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Science specimen number NSM PP-9373. A, Tangential section of two peltate bract/scale
complex heads (h) from apex of cone, showing adaxially attached seeds (s) on head toward
bottom of figure. Note adaxial row of bundles in each head. Adaxial surfaces of adjacent heads
oriented toward each other, because heads arise from opposite sides of cone axis apex. Slide C2-
1 x9. B, Seeds in various planes of section, several of which show wide wings at each side of
nearly round seed cavity. Slide L1-1 x9. C, Cross section of cone showing inverted seeds in
longitudinal view and in position of attachment to underside of adaxial surface of complex head.
Note adaxial row of vascular bundles in complex head (arrowheads), separation of seeds from
complex head by periderm (p) that also surrounds cone axis (a). Slide 2-2 x14. D, Seeds in
various planes of section, showing wide wings (w) surrounding seed body (b) in cross section
(upper right) and in major plane of longitudinal section (bottom). Note periderm (p) of cone axis
(at right) extends out onto adaxial surface of bract-scale complex (at bottom) to level of seed
attachment (Fig. 4C near left). Slide L1-1 x 9. E, Longitudinal section of seed in position of
growth with micropyle at right. Note nucellus (n) attached to integument (i) only at chalaza, and
chalazal chamber (at left). Slide 2-1 x30. F, Oblique cross section of seed cavity at mid-level
showing integument with external epidermis (arrow) zone of sclereids, and inner zone in
longitudinally oriented cells bounded by internal cuticle (i). Note nucellus (n) consists of two to
three cell layers surrounding central hollow and bounded by external cuticle. Slide 4 x70. G,
Oblique longitudinal section near seed apex showing convoluted nucellar apex (na) within
integument (i). Slide 4 x50.
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207x239mm (300 x 300 DPI)
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192x206mm (300 x 300 DPI)
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199x222mm (300 x 300 DPI)
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119x159mm (600 x 600 DPI)
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219x268mm (300 x 300 DPI)
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