Cunninghamia beardii sp. nov. (Cupressaceae: Cunninghamioideae), Anatomically Preserved Pollen Cones from the Eocene of Vancouver Island, British Columbia, Canada

Abstract

Premise of research. A large pollen cone cluster attached to a cunninghamioid twig and surrounded by leaves has been identified from Eocene calcium carbonate marine concretions from the Appian Way locality on Vancouver Island, British Columbia, Canada. The cluster preserves 18 cones but probably bore at least 24 pollen cones based on cone placement in the cluster. Methodology. Specimens were studied using the cellulose acetate peel technique, and reconstructions were made with ImageJ visualization software. Pollen was examined using SEM. Pivotal results. Cones are helically arranged around the tip of an ultimate leafy branch that terminates in scale leaves, each showing a central resin canal. Vegetative leaves on the twig are amphistomatic, showing typical cunninghamioid anatomy, with a large central resin canal abaxial to the vascular bundle, an elongate zone of transfusion tissue, a nonplicate mesophyll, and a hypodermis three to four cells thick. Each pollen cone is produced in the axil of a bract and has three scale leaves surrounding the base of the cone axis. Individual pollen cones have helically arranged microsporophylls, each with three elongate abaxial pollen sacs. While the cones are immature, pollen sacs with pollen are present in several cones. The exine is scabrate, with numerous orbicules, and no papilla is evident. Conclusions. This cluster provides the first detailed anatomically preserved fossil evidence for the pollen cones of Cunninghamia. It shows a large number of similarities to the pollen cone clusters of extant Cunninghamia lanceolata and Cunninghamia konishii and the Late Cretaceous Cunninghamia taylorii, strengthening hypotheses for a basal position of cunninghamioids within the Cupressaceae and further demonstrating that some characters of Cunninghamia have remained relatively unchanged since at least the mid-Cretaceous.

Full text

Cunninghamia beardii sp. nov. (Cupressaceae: Cunninghamioideae), Anatomically Preserved Pollen
Cones from the Eocene of Vancouver Island, British Columbia, Canada
Author(s): Emma L. Buczkowski, Ruth A. Stockey, Brian A. Atkinson and Gar W. Rothwell,
Source:
International Journal of Plant Sciences,
(-Not available-), p. 000
Published by: The University of Chicago Press
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CUNNINGHAMIA BEARDII SP. NOV. (CUPRESSACEAE: CUNNINGHAMIOIDEAE),
ANATOMICALLY PRESERVED POLLEN CONES FROM THE EOCENE
OF VANCOUVER ISLAND, BRITISH COLUMBIA, CANADA
Emma L. Buczkowski,* Ruth A. Stockey,
1,
* Brian A. Atkinson,* and Gar W. Rothwell*
,
†
*Department of Botany and Plant Pathology, Oregon State University, Corvallis, Oregon 97331, USA; and
†Department of Environmental and Plant Biology, Ohio University, Athens, Ohio 45701, USA
Editor: Patricia G. Gensel
Premise of research. A large pollen cone cluster attached to a cunninghamioid twig and surrounded by
leaves has been identified from Eocene calcium carbonate marine concretions from the Appian Way locality
on Vancouver Island, British Columbia, Canada. The cluster preserves 18 cones but probably bore at least 24
pollen cones based on cone placement in the cluster.
Methodology. Specimens were studied using the cellulose acetate peel technique, and reconstructions were
made with ImageJ visualization software. Pollen was examined using SEM.
Pivotal results. Cones are helically arranged around the tip of an ultimate leafy branch that terminates in
scale leaves, each showing a central resin canal. Vegetative leaves on the twig are amphistomatic, showing
typical cunninghamioid anatomy, with a large central resin canal abaxial to the vascular bundle, an elongate
zone of transfusion tissue, a nonplicate mesophyll, and a hypodermis three to four cells thick. Each pollen
cone is produced in the axil of a bract and has three scale leaves surrounding the base of the cone axis. In-
dividual pollen cones have helically arranged microsporophylls, each with three elongate abaxial pollen sacs.
While the cones are immature, pollen sacs with pollen are present in several cones. The exine is scabrate, with
numerous orbicules, and no papilla is evident.
Conclusions. This cluster provides the first detailed anatomically preserved fossil evidence for the pollen
cones of Cunninghamia. It shows a large number of similarities to the pollen cone clusters of extant
Cunninghamia lanceolata and Cunninghamia konishii and the Late Cretaceous Cunninghamia taylorii ,
strengthening hypotheses for a basal position of cunninghamioids within the Cupressaceae and further dem-
onstrating that some characters of Cunninghamia have remained relatively unchanged since at least the mid-
Cretaceous.
Keywords: conifers, Cunninghamia, Cupressaceae, Eocene, fossil, pollen cones.
Introduction
Cupressaceae Gray has one of the longest and most species-
rich fossil records of all conifer families (Stockey et al. 2005;
Escapa et al. 2008; Spencer et al. 2015). Based on seed cone
structure of both living and extinct species, the family also shows
the widest range of morphologies and the most well-documented
transform ational series from which to in fer familial-level evo-
lution of all conifers (Schulz and Stützel 2007; Rothwell et al.
2011; Atkinson et al. 2014a,2014b). Cupressaceae consists of
a morphologically diverse basal taxodioid grade with worldwide
distribution throughtime, whichconsists ofsubfamiliesCunning-
hamioideae, Taiwanioideae, Athrotaxoideae, Sequoioideae, and
Taxodioideae as well as a cupressoid clade of two terminal clades
including Northern Hemisphere Cupressoideae and Southern
Hemisphere Callitrideae (Farjon 2005; Leslie et al. 2012; Mao
et al. 2012). The most ancient Cupressaceae are either assignable
to or extremely similar to the Cunninghamioideae (Stockey et al.
2005; Escapa et al. 2008; Spencer et al. 2015), and the fossil rec-
ord for that clade is extremely rich throughout the Cretaceous
(Atkinson 2014b).
Although the genus Cunninghamia R. Br. ex Rich. does not
appear in the fossil record until the Late Cretaceous (Brink
et al. 2009; Serbet et al. 2013), it is the only surviving repre-
sentative of the earliest diverging lineage of Cupressaceae, sub-
family Cunninghamioideae, and thereby has proven to be a
crucial genus for understanding the evolution of the family
(Stockey et al. 2005; Brink et al. 2009; Serbet et al. 2013).
The earliest records of Cunninghamia are of permineralized
leafy shoots and a whole plant from the Late Cretaceous: Cun-
ninghamia hornbyensis Brink, Stockey, Beard & Wehr (2009)
1
Author for correspondence; e-mail: stockeyr@science.oregonstate
.edu.
Manuscript received June 2015; revised manuscript received August 2015;
electronically published November 23, 2015.
Int. J. Plant Sci. 177(1):000–000. 2016.
q 2015 by The University of Chicago. All rights reserved.
1058-5893/2016/17701-00XX$15.00 DOI: 10.1086/684106
000
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and Cunninghamia taylorii Serbet, Bomfleur, & Rothwell (2013),
respectively. The genus Cunninghamia was widespread in the
Cenozoic in North America, Europe, and Asia (Miki 1941;
Matsuo 1954, 1966, 1970; Lakhanpal 1958; Szafer 1958; Tanai
and Onoe 1961; Givulescu 1972; Kimura and Horiuchi 1978;
Meng et al. 1988; Walther 1989; Dillhoff et al. 2005, 2013;
Dolezych and Schneider 2007; Du et al. 2012; Yabe and Yama-
kawa 2012) and appears to have had a Northern Hemisphere
distribution throughout the past.
Typically, studies of the evolution of Cunninghamia and
cunninghamioid plants have focused on seed cones and vege-
tative morphology and anatomy (Brink et al. 2009; Serbet
et al. 2013; Klymiuk et al. 2015). Although pollen cones of
Cunninghamia display a wealth of systematically informative
characters, well-preserved pollen cones are far less common
in the fossil record. Therefore, up to the present, they have
played a far less important role in resolving the evolution
and phylogeny of Cupressaceae.
In this article, we describe Cunninghamia beardii sp. nov.,
an Eocene fossil conifer shoot terminating in large numbers of
scale leaves that surround a cluster of at least 18 helically ar-
ranged pollen cones. Cones were preserved at various stages
of immaturity at the time of preservation in the calcium car-
bonate marine nodule but show helically attached microspo-
rophylls and pollen sacs containing nonsaccate scabrate pol-
len. These pollen cones contribute additional evidence that
some characters of Cunninghamia species may have remained
relatively unchanged for at least 70 Myr (Serbet et al. 2013).
Material and Methods
A single twig with an attached pollen cone cluster was col-
lected from the Appian Way locality (lat. 49754
0
42
00
N, long.
125710
0
40
00
W; UTM 10U CA 5531083N, 343646E) on the
east coast of Vancouver Island, British Columbia, on the north-
ern periphery of the Tertiary Georgia Basin (Mustard and Rouse
1994). Permineralized fossil plants, gastropods, echinoderms,
and bivalves are found in calcareous concretions embedded in
a silty mudstone matrix representing a shallow marine environ-
ment. Molluscs, decapods (Schweitzer et al. 2003), and shark
teeth indicate that the concretions are of Eocene age (Haggart
et al. 1997; Cockburn and Haggart 2007). Sweet (2005) stud-
ied the pollen from the site and found both late Paleocene and
early Eocene signatures. Stratigraphy of the area is currently be-
ing examined (J. W. Haggart, personal communication). The
Appian Way beds unconformably overlie rocks of the late Cre-
taceous Nanaimo Group strata in the area and are estimated to
be ca. 50 Ma (Mindell et al. 2014).
Plants, including abraded wood and fruits representing nu-
merous taxa, are well preserved in the concretions (Mindell
2008; Mindell et al. 2014). Juglandaceae fruits (Elliott et al.
2006), cupules and nuts of Fagaceae (Mindell et al. 2007a,
2009), endocarps of Icacinaceae (Rankin et al. 2008), inflores-
cences of Platanaceae (Mindell et al. 2006a), flowers of Laura-
ceae (Atkinson et al. 2015), schizaeaceous (Trivett et al. 2006)
and gleicheniaceous (Mindell et al. 2006b) fern remains, leafy
liverworts (Steenbock et al. 2011), and shelf and cup fungi
(Smith et al. 2004; Mindell et al. 2007b) have already been de-
scribed from the locality. Terminal, solitary, globose, taxodi-
aceous pollen cones have been described from Appian Way as
Homalcoia littoralis Hernandez-Castillo, Stockey & Beard (2005).
However, much of the flora still remains to be described (Min-
dell et al. 2014).
Concretions were cut and peeled using the cellulose acetate
peel technique (Joy et al. 1956). Microscope slides were made
using Eukitt (O. Kindler, Freiberg, Germany) mounting me-
dium. Images were captured using a Better Light digital scan-
ning camera (Placerville, CA) and processed using Photoshop
(Adobe, San Jose, CA). Reconstructions were made using Pixel-
mator 2.0 (Vilnius, Lithuania), Photoshop, and ImageJ visuali-
zation software (Rasband 1997–2014).
Pollen was either examined on inverted peels or removed
from cellulose acetate peels for SEM using a modified Daghlian
and Taylor (1979) technique under vacuum on a Millipore fil-
ter (Bedford, MA). Stubs were coated with 100 A7 Au on a
Nanotek sputter-coater and examined using a JEOL 6301F
SEM at 5 kV.
Pollen cone–bearing branches of Cunninghamia lanceolata
were obtained from a tree in Corvallis, Oregon (Ninth and
Buchanan Streets) in February and April 2015 and dissected,
and one section was stained with saffranin O to increase visi-
bility of pollen cones and scale leaves on the shoot tip. All fos-
sil specimens and microscope slides are housed in the Royal
British Columbia Museum, Victoria.
Results
Systematics
Order—Coniferales
Family—Cupressaceae
Subfamily—Cunninghamioideae
Genus—Cunninghamia R. Br. ex Rich.
Species—Cunninghamia beardii Buczkowski, Stockey, At-
kinson et Rothwell sp. nov. (Figs. 1– 4, 6A)
Species diagnosis. Cluster of at least 18 pollen cones, sub-
terminal on leafy branch, helically arranged. Ultimate leafy
branch terminating in scale leaves, significantly increasing in
diameter where pollen cones attached. Leafy twig with paren-
chymatous pith surrounded by cylinder of secondary xylem,
parenchymatous cortex with numerous resin canals, hypoder-
mis of thick-walled cells. Vegetative leaves amphistomatic,
with large central resin canal abaxial to vascular bundle, elon-
gate zone of transfusion tissue, nonplicate mesophyll, hypo-
dermis three to four cells thick. Pollen cones at least 2 mm
in diameter, produced in axil of bract; three scale leaves sur-
rounding base of cone axis. Microsporophylls helically ar-
ranged. Pollen sacs abaxial, three per microsporophyll, elon-
gate. Pollen subspheroidal; exine scabrate, orbiculate, no
papilla evident.
Holotype hic designatus. Cunninghamia beardii Buczkow-
ski, Stockey, Atkinson et Rothwell sp. nov. AW 358 A bot, B
1
top, B
1
bot.
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Repository. Royal British ColumbiaMuseum, Victoria, Brit-
ish Columbia, Canada.
Type locality. Appian Way (lat. 49754
0
42
00
N, long. 1257
10
0
40
00
W; UTM 10U CA 5531083N, 343646E), Vancouver
Island, British Columbia, Canada.
Age. Eocene.
Etymology. The species is named in honor of Graham
Beard (Vancouver Island Paleontological Museum, Qualicum
Beach, British Columbia, Canada), who has collected and pre-
pared large numbers of fossil plant specimens, particularly
from the Appian Way locality, and generously provided the
plants for study.
Description. A single large pollen cone cluster has been
identified in the calcium carbonate concretion from Appian
Way (fig. 1A). The cone is present on one face, while the leafy
branch to which it was attached appears on the other side of
the saw cut and on the opposite face of the adjacent slab.
Cone axes of 18 individual pollen cones have been mapped
on the first peel of the sequence (figs. 1A,6A). Based on sym-
metry of the cone cluster, however, we estimate that approx-
imately 24 pollen cones were produced in the cluster. There
are numerous terminal scale leaves at the center of the pollen
cone cluster, each with a centrally located resin canal (figs. 1A,
2A). This indicates that the pollen cones are actually subtermi-
nal on the twig.
Each pollen cone of the cluster is subtended by a large bract
(fig. 1A,1B) at least 3 mm wide and 0.2 mm thick that has a
central resin canal and an abaxial hypodermis about three
cells thick. Three helically arranged scale leaves surround the
base of each pollen cone axis (figs. 1B, arrowheads, 6C), each
containing a single centrally located resin canal, and in some
sections, three resin canals, one large central and two lateral
smaller, appear. The outermost scale leaf is 1.8–2.0 mm wide,
the second is 1.1–1.5 mm wide, and the innermost scale leaf is
1.1–1.25 mm wide (fig. 1B). Preservation of these scale leaves
is inadequate to enab le a detailed description of their inter-
nal tissues. The bract and scale leaves almost completely sur-
round (figs. 1B,6C) and encl ose the apex of the smallest
cones, indicating that such cones were immature at the time
of preservation.
Pollen cones are variable in size and apparently at different
stages of maturity. The largest are near the periphery of the
cluster (2 mm wide), while the smallest (0.9 mm) and most im-
mature are near the center (fig. 1A,1B). Cone axes are not
well preserved, but a ring of 14–16 resin canals can be seen
in the cortex of some of the cone axes (fig. 1B,1C). Mi-
crosporophylls helically arranged around the cone axis are
0.3 mm long with a lamina about 0.3 mm wide (figs. 1C,
6C–6E
). Each sporophyll extends toward the periphery of
the cone as a terete stalk, turns distally, and expands into
the sporophyll lamina (figs. 1C,6D). There is a centrally located
resin canal in each of the microsporophylls (figs. 1C,2B). Pol-
len sacs are elongate, 0.7–1.0 mm long, 0.24–0.34 mm wide
(fig. 2B,2C), and abaxially attached to the sporophyll at the
base of the upturne d lamina (fig. 2B,2C). Two of the pollen
sacs are situated slightly above the third, which is more abax-
ial (fig. 2B,2C). Pollen sac walls have dark-colored contents
and are incompletely preserved (fig. 2B–2D).
Pollen in all cones is immature, 24–27 mm in diameter
(mean p 26 mm, n p 10), compressed together, and closely
packed (figs. 2D,3A,3B). Grains are folded, and apertures have
not been identified. As is characteristic of many taxodioid-grade
Cupressaceae, the exine consists of a relatively uniform nexine
(fig. 3B,3C, bottom) and a scabrate sexine with numerous
orbicules (fig. 3C, top). It is possible that grains are in a late tet-
rad stage, but this could not be determined with certainty.
The leafy branch that bears the pollen cone cluster (fig. 4A)
has a diameter of 4 mm and swells and increases in size to a
diameter of 7 mm just below the pollen cone cluster (fig. 4B
).
The pith of the stem is about 1 mm wide proximally (fig. 4A)
and increases to 2.45 mm wide near the pollen cone cluster
(fig. 4B). The pith and cortex are parenchymatous and have
scattered cells with amber contents, some of which appear
to be sclereids (fig. 4C). The pith is surrounded by a cylinder
of radially aligned secondary xylem tracheids, fi ve to six cells
wide, that is interrupted by pith rays (fig. 4A–4C). The cortex
contains a ring of numerous resin canals with an epithelial lin-
ing that enter the bases of vegetative leaves (fig. 4A–4E). The
stem periphery shows a narrow sclerotic hypodermis that ex-
tends into the leaf bases.
The cross section of the stem nearest the pollen cone cluster
shows a larger number of attached leaves (fig. 4B). Leaves are
amphistomatic and 2.0–2.4 mm wide at the base and contain
a single vascular bundle with an abaxial resin canal and an
elongate zone of transfusion tissue (fig. 4D–4F). Transfusion
tracheids are short and have circular-bordered pits (fig. 4F).
The mesophyll is nonplicate, and the hypodermis is three to
four cells thick (fig. 4D,4E).
Extant Cunninghamia lanceolata
Collections of branches bearing pollen cones of C. lanceo-
lata show that pollen cones can remain on the tree for at least
4yr(fig. 5A). When the cone clusters first mature, they appear
to be terminal. However, there are terminal vegetative leaf
primordia at the center (i.e., apex) of each pollen cone cluster
(fig. 6B) that grow out during the next year to produce addi-
tional leafy branches with subterminal pollen cones (fig. 5A).
Pollen cones are tightly packed in clusters when they are im-
mature (fig. 5B,5C), with cones elongating and separating from
the cluster at maturity (fig. 5D). They are helically arranged
around a vegetative stem with a developmental gradation, the
older cones occurring farthest from the center (i.e., being most
basal; figs. 5B,5C,6B). Immature cones in clusters at a compa-
rable stage to those seen in the Appian Way fossil (fig. 5B,5C)
are 2–5 mm in diameter (mean p 2.57, n p 60). The immature
cones are 3–9 mm long (mean p 4.63, n p 60). Mature pollen
cones are 8–22 mm long (mean p 13.4, n p 60). Each cone is
subtended by an elongate bract (fig. 5C,5E); three smaller scale-
like leaves occur at the base of the cone axis (fig. 5E). Cones are
borne on the axis subterminally, and the apical portion of the
stem bears numerous helically arranged scale leaves (fig. 6B),
as in the Appian Way cone (fig. 6A). These axes routinely grow
out in the subsequent year, producing new vegetative shoot
growth and then terminating in a new subapical pollen cone
cluster (fig. 5A
). There are two to four pollen sacs per microspo-
rophyll, with most sporophylls having three elongate pollen
sacs on their abaxial surfaces (mean p 2.91, n p 100), that
are attached near the base of the sporophyll lamina. Two
BUCZKOWSKI ET AL.— CUNNINGHAMIA BEARDII SP. NOV. 000
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Fig. 1 Cunninghamia beardii sp. nov. Holotype, AW 358. A, Pollen cone cluster with subtending leaves at periphery, immature leaves at
center (arrow), and pollen cones between. Note each pollen cone in axil of bract (b) and that basalmost pollen cones (near periphery) are larger
and have more mature pollen sacs than cones closer to center (i.e., more apical). A bot #8 #19. B, Two immature pollen cones, each in the axil
of bract and with three scalelike leaves (arrowheads). Note helically arranged sporophylls with narrow stalk and distal lamina. A bot #6 #43. C,
Enlargement of immature pollen cone showing resin canals in cortex of axis and single resin canal in stalk and distal lamina of each sporophyll.
A bot #16 #100.
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pollen sacs are situated above the third, as in the Appian Way
pollen cones.
Discussion
The pollen cone cluster from Appian Way clearly represents
a taxodioid-grade cupressaceous conifer with helically arranged
leaves and typical taxodioid pollen. Previously described pollen
cones of Homalcoia littoralis from Appian Way are terminal and
globose, with numerous subtending scale leaves and ellipsoidal
pollen sacs. Pollen is 11–20 mm in diameter and papillose at ma-
turity. While the pollen of Cunninghamia beardii is immature,
it is larger at this stage of development when compared to H.
littoralis and lacks any discernible papilla. Homalcoia pollen
cones are solitary and not borne in clusters, as in the pollen cones
described here.
Similarities of C. beardii to extant Cunninghamia spp. are
striking. Using extant Cunninghamia lanceolata (Lamb.) Hook.
and Cunninghamia konishii Hayata for comparison to the Ap-
pian Way fossil, all three species have subterminal pollen cone
clusters with helically arranged pollen cones surrounding a veg-
etative stem that has terminal scale leaves and the capacity to
grow through the next year (Farjon 2005). The Appian Way
cones were immature at the time of preservation. This can be
seen in the tightly spiraled nature of the cones of the cluster as
well as the immature pollen contained in the pollen sacs, and
in these features, they compare closely with the immature C.
lanceolata pollen cone clusters in figure 5B,5C. The smallest
Appian Way cones have bracts and scale leaves that extend
up around the pollen cone apex, a feature that is characteristic
of immature conifer pollen cones that have yet to grow beyond
their basal bud scales. This character suggests that the least ma-
Fig. 2 Cunninghamia beardii sp. nov. Holotype, AW 358. A, Central leafy zone of pollen cone cluster. Note that each immature scalelike
leaf has a central resin canal. A bot #6 #30. B, Cross section of single pollen cone showing sporophylls diverging from cone axis. Note single
resin canal in sporophyll stalk (s) and three pollen sacs (right) attached to lamina (l). A bot #8 #61. C, Cross section of single pollen cone show-
ing sporophyll lamina with three attached pollen sacs (p), two of which show elongation toward cone axis. A bot #16 #124. D, Enlargement of
somewhat immature pollen sac showing closely packed pollen grains. A bot #10 #440.
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ture fossil cones were younger than the most immature extant
cones illustrated here (fig. 5C,5E).
Among extant conifers, pollen cone clusters are reported in
several pinaceous genera including Keteleeria Carrière and
Pseudolarix Gord. (Schulz et al. 2014), in which the clusters
are borne terminally or laterally on branches (Farjon 1990);
however, leaf anatomy, pollen type (bisaccate), and two pollen
sacs per microsporophyll preclude assignment of the Appian
Way cones to the Pinaceae. Likewise, Podocarpus L’Héritier ex
Persoon, Retrophyllum C. Page, Acmopyle Pilger, and Nageia
J.Gaertner in the Podocarpaceae are also reported to bear pol-
len cones in clusters (Schulz et al. 2014), but podocarpaceous
pollen cone clusters tend to be borne on small, specialized lat-
eral shoots that have widely spaced pollen cones. The leaf anat-
omy, pollen type (bisaccate), and presence of two pollen sacs
per microsporophyll (Sporne 1965; Woltz 1986; Eckenwalder
2009) clearly differentiate those podocarpaceous pollen cone
clusters from the cone cluster described here.
Among all conifer families, pollen cone clusters are most
common in fossil and living species of Cupressaceae. Pollen
cones of the most ancient cupressaceous fossils from the Early
Jurassic of Argentina, Austrohamia minuta Escapa, Cúneo &
Axsmith, occur in terminal clusters of up to seven, while those
of the Middle Jurassic Sewardiodendron laxum (Phillips) Flo-
rin are borne in terminal clusters of seven to eight (Yao et al.
1998). Shi et al. (2014) report clusters of up to nine pollen
cones attached to twigs in their reconstruction of the cun-
ninghamioid Elatides zhoui Shi, Leslie & Herendeen, lignitic
fossils from the Early Cretaceous (Aptian-Albian) of Mongolia.
Those cones are located along the stem near the shoot apex and
occur in the axils of modified bracts, which are much broader
and more triangular than the vegetative leaves. Therefore, they
form a less dramatically expanded cluster at the shoot apex (Shi
et al. 2014) than seen in C. beardii (i.e., fig. 2 of Shi et al. 2014).
Among extant species of Cupressaceae, Taiwania cryptomeri-
oides Hayata bears pollen cones in terminal clusters of up to
seven, and Amentotaxus Pilger in the Taxaceae also has clusters
of pollen cones (Schulz et al. 2014). Cunninghamia beardii is
easily distinguished from all of these species by the much larger
number of pollen cones (∼24) that occur in clusters of a much
larger size.
The highly distinctive and systematically isolated living spe-
cies Sciadopitys verticillata (Thunb.) Siebold & Zucc. also pro-
duces clusters of apparently terminal to subterminal pollen cones
that are superficially similar to those of C. beardii (Farjon 2005),
but individual cones of Sciadopitys are tightly packed and form
an ovoid cluster, and the branch tip does not expand as greatly
as in Cunninghamia (R. A. Stockey and G. W. Rothwell,personal
observation). Pollen cones of Sciadopitys are larger in diame-
ter (Farjon 2005) and more distinctive within each cluster than
Fig. 3 Cunninghamia beardii sp. nov. Holotype, AW 358. SEMs
of pollen sac with somewhat immature pollen. All A bot #7. A, Closely
packed pollen within incompletely preserved pollen sac wall (upper
left). #850. B, Enlargement of possible tetrad at lower left in A. Note
that the pollen wall consists of two zones. #2750. C, Cross section
of pollen wall showing nexine (bottom) and scabrate sexine with orbic-
ules (top). #72,000.
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Fig. 4 Cunninghamia beardii sp. nov. Holotype, AW 358. A, Shoot-bearing pollen cone cluster showing helically arranged leaves, stem with
pith, stele with diverging leaf traces, and parenchymatous cortex. Note resin canals in cortex, single resin canal in leaf bases, and narrow sclerotic
hypodermis on diverging leaves. B
1
bot #1 #17. B, Cross section at base of pollen cone cluster, with increased stem size, enlarged pith, and
larger number of leaves. Note ring of small resin canals at outer margin of stele and slightly larger resin canals scattered within cortex. B
top #2 #12. C, Histological features of stem bearing pollen cone cluster, showing pith and cortical parenchyma with empty lumens and scattered
cells with amber contents, some that appear to be sclereids (arrows). Note radially aligned tracheids of stelar xylem, diverging leaf traces (lt), and
resin canals (r) with epithelial lining. B
1
bot #2 #65. D, Diverging leaf base at periphery of stem showing vascular bundle (vb), resin canal (r),
and band of transfusion tissue (t). Note sclerotic hypodermis on abaxial surface of leaf base (right). Arrowhead on transfusion tracheid enlarged
in F .B
1
bot #2 #97. E, Cross section of leaf base at level of separation from stem, showing position of vascular bundle (vb), resin canal (r),
parenchymatous mesophyll, and sclerotic hypodermis. B
1
bot #2 #45. F, Enlargement of transfusion tracheid with circular-bordered pits. B
1
bot #2 #690.
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Fig. 5 Extant Cunninghamia lanceolata . A, Leafy shoot showing positions of pollen cone clusters from current year (0), 1 yr ago (1), 2 yr
ago (2), and 3 yr ago (3). #0.5. B, Pollen cone cluster sectioned below apex showing somewhat immature pollen cones crowded within
subtending leaves. Note that pollen cones appear to occupy stem apex at this level. #4. C, Pollen cone cluster showing somewhat immature
cones, each subtended by bract-like leaf. As in fig. 4B, cones appear to occupy apex of branch in this view. #3. D, Shoot tip showing cluster
of mature pollen cones. Note that cones elongated at maturity to expose pollen sacs. #2. E, Immature pollen cone with subtending bract (b) at
right and three scale-like leaves (arrowheads) at cone base. #14.
000
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Fig. 6 Cunninghamia beardii sp. nov. and Cunninghamia lanceolata pollen cone clusters in cross section just distal to stem apex. A,
Cunninghamia beardii with bracts (green), scale leaves at base of cones (blue), cone axes and sporophylls (red), and pollen sacs (yellow).
AW 358 A bot #1. Holotype. #18. B, Cunninghamia lanceolata at comparable level to fossil in A, showing zone of slightly immature cones
within peripheral subtending leaves and central zone of vegetative leaf bases. #7. C, Cunninghamia beardii, diagram illustrating the relationships
among pollen cones (red), scale leaves (sc; blue), and subtending bract (b; green). AW 358 A bot #6. Holotype. #60. D, Cunninghamia beardii, three-
dimensional reconstruction of one pollen cone as viewed from cut surface. #65. E, Cunninghamia beardii, three-dimensional reconstruction of
apex of cone surface showing tightly appressed microsporophyll heads. #55.
000
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those of Cunninghamia. Individual pollen cones of Sciadopitys
are subtended by a bract such as that in Cunninghamia, but each
cone lacks basal scale leaves (R. A. Stockey, personal observat-
ions). Likewise, two pollen sacs per microsporophyll, inaper-
turate pollen, and highly distinctive short shoots that appear
to be leaves in Sciadopitys easily distinguish that genus from
C. beardii.
In position on the shoot, size, shape, number of pollen
cones, microsporophyll structure, pollen type, and morphol-
ogy and anatomy of subtending leaves and stems, the Appian
Way pollen cone cluster is much more similar to those of
the genus Cunninghamia. The only previously known occur-
rence of Cunninghamia pollen cones in the fossil record was
described by Serbet et al. (2013) for Cunninghamia taylorii
Serbet, Bomfleur & Rothwell from the Upper Cretaceous (Cam-
panian) Horseshoe Canyon Formation near Drumheller, Alberta,
Canada. Those pollen cones are borne in clusters of up to 17
that appear to terminate vegetative shoots and are surrounded
by scale leaves that are anatomically similar to those of both
C. beardii and living species of Cunninghamia (Serbet et al.
2013). The pollen cones of C. taylorii are represented by only
the cone axis and the basal scalelike leaves (microsporophylls,
pollen sacs, and pollen having been lost from those specimens).
While the pollen cone clusters of C. taylorii are similar to those
of C. beardii in most known features, the two species can easily
be distinguished by the number of scale leaves at the base of
each cone, three in C. beardii and five or six in C. taylorii (Serbet
et al. 2013).
Cunninghamia beardii is most similar to the pollen cone
clusters of the living Cunninghamia species (i.e., C. konishii
Hayata and C. lanceolata [Lamb.] Hook.; Farjon 2005; Ser-
bet et al. 2013). Similarities include size, overall shape, and
pollen cones that appear to be terminal (but are actually subter-
minal), all having the potential to grow out in subsequent years
to produce an additional plastichron of vegetative/fertile growth.
Extant Cunninghamia species and C. beardii have similar num-
bers of pollen cones of relatively similar sizes in each cluster, and
each cone produces three basal scalelike leaves. Moreover, as
far as is known, leaf histology is comparable in the two.
Given the structural similarities between C. beardii, C. lanceo-
lata, and C. konishii, one may be tempted to assign the fossil
to one of the living species. However, with more careful con-
sideration it becomes clear that there are no characters to deter-
mine to which of the two species the fossils would be assigned.
More importantly, we have excellent evidence from other fossil
taxodioid-grade Cupressaceae that species differences are often
extremely subtle and that confident species identifications often
cannot be made until ranges of variation for a wide variety of
organs have been determined. For example, compression fossils
of the genus Metasequoia Miki extend from the Cretaceous to
the recent, with as many as 21 species having been described, of-
ten from relatively small numbers of specimens and few organs
(Liu et al. 1999; Stockey et al. 2001). However, a comprehen-
sive review of fossil Metasequoia has revealed that all fossils
may be assignable to only three species (Liu et al. 1999). So sub-
tle are the differences between species of Cretaceous, Paleogene,
and Neogene Metasequoia that more than 10,000 specimens
of branches, leafy shoots, pollen cone–bearing shoots, pollen
cones, pollen, seed cones, seeds, and seedlings were required to
clearly distinguish Metasequoia foxii Stockey, Rothwell & Falder
(2001) from the other fossil and living species.
Due to our growing understanding of mosaic character evo-
lution within the Cupressaceae, it appears that some repro-
ductive organs have undergone a higher rate of evolution
compared to the vegetative organs than have others (Atkinson
et al. 2014a
). Many extinct species have similar leaf anatomy
and morphology in many organs, while ovulate cones show
novel combinations of characters that are not typically found
in living cunninghamioids (Atkinson et al. 2014a). Conifer
pollen cones are relatively uncommon in the post-Paleozoic
fossil record, and the diversity of extinct cupressaceous pollen
cones is virtually unknown. If C. beardii is characteristic of
extinct cupressaceous pollen cones in general, then pollen
cone evolution has been far less dramatic than seed cone evo-
lution within the family, as has been suggested for conifers in
general (Leslie 2011). Within this context, C. beardii provides
important data for understanding the evolution of pollen
cones within this group.
Although C. beardii closely resembles the pollen cone clus-
ters of both living species of Cunninghamia (i.e., C. lanceolata
and C. konishii), the most prudent taxonomic placement for
the Appian Way fossil is in a new species. This decision actu-
ally represents a conservative taxonomic judgment that is con-
cordant with recently modeled evolutionary dynamics for the
family Cupressaceae (Leslie et al. 2012), in which the clado-
genic event leading to the origin of C. lanceolata and C. ko-
nishii from a putative common ancestor occurred in the Neo-
gene, at least 30 Myr after fossilization of the Appian Way
flora (Leslie et al. 2012; Mindell et al. 2014). Whether that
putative common ancestor is the species represented by C.
beardii or some other as of yet to be recognized extinct species
of Cunninghamia awaits discovery of the unknown vegetative
and fertile organs of C. beardii and much denser sampling of
Cretaceous and Tertiary Cupressaceae. However, in either case,
exquisitely preserved fossils from carbonate marine concretions
will undoubtedly play a major role in both fleshing out the
patterns of evolution for crown group conifers and testing hy-
potheses of conifer phylogeny generated by analyses of living
species using molecular characters and phylogenetic modeling
exercises that rely on those hypotheses as sources of data.
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