Pagination not final (cite DOI) / Pagination provisoire (citer le DOI)
1
ARTICLE
The Early Cretaceous Apple Bay flora of Vancouver Island:
a hotspot of fossil bryophyte diversity1
Botany Downloaded from www.nrcresearchpress.com by HUMBOLDT STATE UNIVERSITY on 08/23/16
For personal use only.
Alexandru M.F. Tomescu
Abstract: The pre-Cenozoic bryophyte fossil record is significantly sparser than that of vascular plants or Cenozoic
bryophytes. This situation has been traditionally attributed to a hypothesized low preservation potential of the
plants. However, instances of excellent pre-Cenozoic bryophyte preservation and the results of experiments
simulating fossilization contradict this traditional interpretation, suggesting that bryophytes have good preservation potential. Studies of an anatomically preserved Early Cretaceous (Valanginian) plant fossil assemblage on
Vancouver Island (British Columbia), at Apple Bay, focusing on the cryptogamic flora, have revealed an abundant
bryophyte component. The Apple Bay flora hosts one of the most diverse bryophyte assemblages worldwide, with
at least nine distinct moss types (polytrichaceous, leucobryaceous, tricostate), one complex thalloid liverwort, and
two other thalloid plants (representing bryophyte or pteridophyte gametophytes), which contribute a significant
fraction of biodiversity to the pre-Cenozoic fossil record of bryophytes. These results (i) corroborate previous
observations and studies, indicating that the preservation potential of bryophytes is much better than traditionally thought; (ii) indicate that the bryophyte fossil record is incompletely explored and many more bryophyte
fossils are hidden in the rock record, awaiting discovery; and (iii) suggest that the paucity of the pre-Cenozoic
bryophyte fossil record is primarily a reflection of inadequate paleobryological capacity.
Key words: fossil, bryophyte, moss, Cretaceous, anatomy, permineralized.
Résumé : Le registre des bryophytes fossiles du pré-Cénozoïque est significativement plus mince que celui de plantes
vasculaires ou de bryophytes du Cénozoïque. Cette situation a été traditionnellement attribuée à un hypothétique
faible potentiel de préservation de ces plantes. Cependant, des exemples d’une excellente préservation de bryophytes
du pré-Cénozoïque et les résultats d’expériences simulant la fossilisation contredisent cette interprétation traditionnelle, suggérant que les bryophytes ont un bon potentiel de préservation. Des études d’un assemblage de plantes
fossiles anatomiquement préservées du Crétacé inférieur sur l’Ile de Vancouver (Colombie Britannique), à Apple Bay, se
concentrant sur la flore cryptogame, ont révélé une composante importante de bryophytes. La flore d’Apple Bay
comporte un des assemblages de bryophytes les plus diversifiés dans le monde, avec au moins neuf types distincts de
mousses (Polytrichacées, Leucobryacées, mousses tricostées), une hépatique thalloïde complexe et deux autres plantes
thalloïdes (représentant des gamétophytes de bryophyte ou de ptéridophyte), qui contribuent à une fraction significative de la biodiversité du registre des bryophytes fossiles du pré-Cénozoïque. Ces résultats (i) corroborent les observations et les études antérieures indiquant que le potentiel de préservation des bryophytes est beaucoup meilleur
qu’initialement présumé; (ii) indiquent que le registre de bryophytes fossiles est incomplètement exploré et que
beaucoup plus de bryophytes fossiles sont cachés dans les couches de roches, dans l’attente d’être découverts et
(iii) suggèrent que la pauvreté du registre des bryophytes fossiles du pré-Cénozoïque est surtout le reflet d’une capacité
paléobryologique inadéquate.
Mots-clés : fossile, bryophyte, mousses, Cretacé, anatomie, permineralisé.
Introduction
Extant mosses count an estimated 13 000 species (Goffinet
et al. 2009), yet only about 70 moss species have been
described from pre-Cenozoic rocks (older than 66 Ma)
(Oostendorp 1987; Ignatov 1990; Taylor et al. 2009). The
two other bryophyte lineages, liverworts and hornworts,
show similar patterns of marked paucity in the Paleozoic
and Mesozoic record (Oostendorp 1987; Taylor et al. 2009).
Pre-Cenozoic bryophyte scarcity has been traditionally
attributed to a hypothesized low preservation potential
of these plants (Stewart and Rothwell 1993; Hemsley
2001; Hübers and Kerp 2012). However, this hypothesis is
Received 25 February 2016. Accepted 17 May 2016.
A.M.F. Tomescu. Department of Biological Sciences, Humboldt State University, Arcata, CA 95521, USA.
Email for correspondence: mihai@humboldt.edu.
1This Article is part of a Special issue entitled “Mesozoic and Cenozoic Plant Evolution and Biotic Change,” a collection of research
inspired by, and honouring, Ruth A. Stockey.
Copyright remains with the author(s) or their institution(s). Permission for reuse (free in most cases) can be obtained from RightsLink.
Botany 94: 1–13 (2016) dx.doi.org/10.1139/cjb-2016-0054
Published at www.nrcresearchpress.com/cjb on xx xxx xxxx.
Pagination not final (cite DOI) / Pagination provisoire (citer le DOI)
Botany Downloaded from www.nrcresearchpress.com by HUMBOLDT STATE UNIVERSITY on 08/23/16
For personal use only.
2
rejected by the mechanical strength and chemical resilience of bryophytes, as demonstrated by experiments
that simulate fossilization conditions (Kroken et al. 1996;
Hemsley 2001; Kodner and Graham 2001; Graham et al.
2004), and by instances of exquisite preservation of even
seemingly delicate bryophyte structures (Harris 1939; Smoot
and Taylor 1986; VanAller et al. 2008). Indeed, when discovered and carefully studied, pre-Cenozoic bryophyte
fossils reveal morphology and anatomy in tremendous
detail, such as minute and ephemeral reproductive structures
(Harris 1939; Konopka et al. 1997; Shelton et al. 2015).
It has been suggested that instead of representing an
issue of preservation potential, the sparsity of the bryophyte fossil record may reflect either a real pattern of
evolutionary diversification (or, rather, lack thereof)
prior to the Cenozoic, or the failure of paleobotanists to
detect bryophytic remains (Hemsley 2001). The deep geologic age of bryophytes (Edwards et al. 1995; Wellman
et al. 2003), which are widely accepted today as being at
least as old as vascular plants (Graham 1993; Kenrick and
Crane 1997; Wickett et al. 2014), argues against the former and in support of the latter. This view is corroborated by the discovery of plant fragments attributed to
mosses in 330 Ma old Mississippian strata as a result of
use of a method uncommon for studies of those rocks
(bulk maceration; Hübers and Kerp 2012). These findings
have led Hübers and Kerp (2012) to anticipate that future
studies will show that mosses were more widespread in
the late Paleozoic than previously thought. Taken together, these imply that many more bryophytes await
discovery in the pre-Cenozoic rock record.
I argue that an aggravating factor in our inability to
thoroughly explore the bryophyte fossil record is inadequate paleobryological research capacity, i.e., the very
limited number of botanists trained and interested in
the study of both bryophytes and the plant fossil record.
This is at least partially due to a disconnect, similar to
that pointed out recently in the case of fungi (Taylor et al.
2014), between the scientists who discover the bryophyte
fossils (paleobotanists) and those who have the knowledge about extant bryophytes (bryologists) that is needed
to understand those fossils. On one hand, because plant
fossils abound in the rock record and are crucial to understanding of plant evolution and phylogeny, and of the
paleoclimates and paleogeography of different regions
and moments in geologic time, the relatively small
global paleobotanical community is stretched thin trying to cover as many geologic periods and plant groups
as possible. Additionally, bryophytes are less conspicuous than most vascular plants in the fossil record. On the
other hand, mastering bryophyte systematics and morphology involves a high degree of specialization, and the
number of extant bryophyte systematists is small. Although these factors are not necessarily the root of the
disconnect mentioned above, together they may explain
Botany Vol. 94, 2016
why the bryophyte fossil record has been poorly explored to
date, albeit not for a lack of fossil material.
The pattern of fossil discoveries corroborates the idea
that rather than reflecting low abundance and low diversity of bryophytes in the geologic past, the rarity of bryophyte fossils is due primarily to an incompletely explored
fossil record. Indeed, the bryophyte diversity discovered
in amber (mostly Cenozoic, but also Cretaceous), demonstrates that under sustained focus of existing bryological
capacities, the fossil record turns out to be much richer
than expected (e.g., Hentschel et al. 2009; Frahm 2010;
Katagiri et al. 2013; Hedenas et al. 2014; Mamontov et al.
2015). Recently, rock units spanning the Cretaceous to
Eocene on the West Coast of North America have emerged
as repositories of fossil bryophyte diversity, characterized by anatomical preservation, and amenable to indepth systematic evaluation (Steenbock et al. 2011; Tomescu
et al. 2012; Unger and Tomescu 2013; Bippus et al. 2015;
Shelton et al. 2015). Among these, the Early Cretaceous
Apple Bay flora on Vancouver Island (British Columbia) has
received a lot of attention and has been worked extensively by
R.A. Stockey, in collaboration with G.W. Rothwell.
Here, I present an overview of bryophyte diversity documented thus far in the Apple Bay flora. Study of the
Apple Bay concretions employs the traditional methods
of coal ball paleobotany: the concretions are sliced into
slabs that are then sectioned using the cellulose acetate
peel technique (Joy et al. 1956). That fact that this technique yields serial sections spaced only 20–30 m apart
is both an advantage (high spatial resolution) and a shortcoming (it is time-consuming). Given these constraints,
along with the fact that there are thousands of plantcontaining concretions collected from Apple Bay, this
account necessarily reflects only a subset of the bryophyte diversity preserved in the flora: that uncovered
since we started targeted searches for bryophytes, five
years ago. Some of the descriptive data compiled here
were reported at scientific meetings and come from the
corresponding meeting abstracts referenced throughout
this article, whereas other data, as well as interpretations and discussions, represent new information. Several pointed publications that detail fossils discussed
here will be forthcoming. I dedicate this paper to Dr.
Ruth A. Stockey, in honor of her numerous and influential contributions to paleobotany.
Materials and methods
Locality and flora
The Apple Bay flora is preserved anatomically by calcium carbonate permineralization, in concretions that
host an allochthonous fossil assemblage deposited in
nearshore marine sediments. The concretions are encased in sandstone (greywacke) beds exposed on the
northern shore of Apple Bay, Quatsino Sound, on the
west side of Vancouver Island, British Columbia, Canada
(50°36=21==N, 127°39=25== W; UTM 9U WG 951068) (Stockey
Published by NRC Research Press
Pagination not final (cite DOI) / Pagination provisoire (citer le DOI)
Botany Downloaded from www.nrcresearchpress.com by HUMBOLDT STATE UNIVERSITY on 08/23/16
For personal use only.
Tomescu
and Rothwell 2009). These plant-fossiliferous layers are
regarded as Longarm Formation equivalents, and have
been dated by oxygen isotope analyses to the Valanginian (Early Cretaceous, ca. 136 Ma) (Rothwell and Stockey
2013).
The flora includes lycophytes, equisetophytes, several
fern families (Smith et al. 2003; Hernandez-Castillo et al.
2006; Little et al. 2006a, 2006b; Rothwell and Stockey
2006; Stockey et al. 2006; Vavrek et al. 2006; Rothwell
et al. 2014), as well as numerous gymnosperms (Stockey
and Wiebe 2008; Stockey and Rothwell 2009; Klymiuk
and Stockey 2012; Rothwell and Stockey 2013; Rothwell
et al. 2014; Atkinson et al. 2014a, 2014b; Ray et al. 2014),
fungi (Smith et al. 2004; Bronson et al. 2013), a lichen
(Matsunaga et al. 2013), and numerous bryophytes (Tomescu
et al. 2012).
Fossil preparation
Carbonate concretions were sliced into slabs and then
sectioned using the cellulose acetate peel technique (Joy
et al. 1956). Slides were prepared using Eukitt mounting
medium (O. Kindler GmbH, Freiburg, Germany). To obtain a
quantitative measure of the abundance of bryophyte fossils, a
tally of bryophyte fossils observed in 39 concretions was divided by the total surface area of the sections (produced
by cutting into slabs) that exposed plant material in the
39 concretions. Because bryophyte fossils are small, few
specimens were exposed in more than one cut; those
that were exposed in more than one cut were counted
only once for the tally. Micrographs were taken using an
Olympus DP73 digital camera mounted on an Olympus
SZX16 microscope. Images were processed using Photoshop (Adobe, San José, California, USA). All Apple Bay
specimens and preparations are housed in the University
of Alberta Paleobotanical Collections (UAPC-ALTA), Edmonton, Alberta, Canada; the Budden Canyon Formation material is housed in the Humboldt State University
Paleobotanical Herbarium (HPH).
Results
Abundance
A total of 223 distinct bryophyte specimens were exposed in the 39 concretions surveyed, on planes of section totaling 0.162 m2 of surface area; therefore, one
bryophyte specimen for every 7.25 cm2. Of these, 124 are
leafy gametophyte stems, 92 are leafless bryophyte axes,
and 7 are thalloid gametophytes (Tomescu et al. 2012).
Mosses
The most abundant bryophyte fossils at Apple Bay are
the moss gametophytes. Of these, some can be assigned
to extant families, while others represent extinct lineages. Among the latter, a prominent feature of the Apple Bay flora is the diversity of tricostate mosses. The
tricostate condition is characterized by consistent occurrence of three costae per leaf in a symmetrical arrangement: one central and two lateral costae. This condition,
3
known exclusively from the fossil record, is approached
in the modern flora only by some limbidiate mosses (e.g.,
Limbella Müll. Hal.; see Shelton et al. 2015 for an in-depth
discussion). Tricostate mosses were first described by
Krassilov (1973), who erected for these forms the genus
Tricostium Krassilov, which currently includes three species that span the Triassic (or possibly Late Permian) to
Late Cretaceous interval (Ignatov and Shcherbakov 2011a,
2011b).
At Apple Bay, another tricostate genus, Tricosta Shelton,
Stockey, Rothwell et Tomescu, represented by one species
(T. multiplicata Shelton, Stockey, Rothwell et Tomescu) is
characterized by much-branched stems with densely inserted and strongly plicate leaves (Figs. 1A and 1B). The
three leaf costae are homogeneous and arise separately
in the leaf base. The ovate leaves have small alar regions.
The gametophytes bear lateral sessile perigonia and
perichaetia with preserved gametangia (Fig. 1B). Tricosta
represents the oldest unequivocal record of the pleurocarpous superorder Hypnanae and was placed in its own
family, Tricostaceae (Shelton et al. 2015). Another member of the Tricostaceae recognized in the Apple Bay flora
is Krassiloviella limbelloides Shelton, Stockey, Rothwell et
Tomescu (Figs. 1C and 1E). Krassiloviella features robust gametophytes with narrow-lanceolate leaves that exhibit
small, weakly differentiated alar regions and bear strong
homogeneous costae that arise separately in the leaf
base and are covered by an epidermal layer (Shelton et al.
2016).
For the time being, it is unclear whether genus Tricostium
is a member of family Tricostaceae. Because all Tricostium
species are based on compression material, this genus is
defined by a small set of leaf morphological characters.
In contrast, Tricostaceae are based on anatomically preserved material that reveals a wealth of characters, most
of which cannot be or have not been observed in any of
the Tricostium species because of their mode of preservation. Thus, the difference in mode of preservation leads
to high disparity in the number and type of diagnostically informative characters, and ultimately in how well
the Tricostaceae and Tricostium are understood. This precludes relevant comparisons and placement of Tricostium in
the Tricostaceae. In fact, the features recorded in
Tricostium do not provide enough evidence even for inclusion in the Hypnanae; Tricostium should therefore be
maintained as a morphogenus (i.e., a taxon defined
based only on a subset of characters of the whole plant;
Bell and York 2007) for moss compressions with tricostate leaves.
Aside from the two tricostate types already mentioned,
the Apple Bay flora hosts at least two other tricostate
mosses that await in-depth characterization. One of
these is similar to Tricosta, with plicate leaves that have a
broad lamina, but is much more robust (stems and leaves
at least twice as large as those of Tricosta) and features
more prominent costae (Fig. 1D). Whereas this type probPublished by NRC Research Press
Pagination not final (cite DOI) / Pagination provisoire (citer le DOI)
Botany Downloaded from www.nrcresearchpress.com by HUMBOLDT STATE UNIVERSITY on 08/23/16
For personal use only.
4
Botany Vol. 94, 2016
Fig. 1. Early Cretaceous moss gametophytes from Apple Bay (Vancouver Island). (A) Tricosta plicata stem, longitudinal section; note
lateral branch longitudinal section (arrowhead) and area around asterisk showing conspicuous tricostate plicate leaves in cross
section; stem tip points to the right; central tissues of stem and branches not preserved. P15425 Cbot #55a. Scale bar = 500 m.
(B) Tricosta plicata, cross-section of stem (s) and two lateral perigonial branches; empty antheridial sacs (two next to each of the
asterisks) have sinuous outlines and are surrounded by perigonial leaves; many tricostate plicate leaves are cut in cross section.
P15425 Cbot #14a. Scale bar = 300 m. (C) A second tricostate type; oblique stem section (central tissues not preserved) with leaves
diverging toward the top; note robust leaf costae (arrowheads indicate three costae of the same leaf) and lamina with discontinuous
preservation. P13131 Dbot #7c. Scale bar = 250 m. (D) A third tricostate type, stem cross section (central tissues not preserved); note
plicate leaves with conspicuous narrow costae (arrowheads indicate three costae of the same leaf). P15800 Cbot #1a. Scale bar = 300 m.
(E) Stem longitudinal section of same moss type as in Fig. 1C; note bases of robust costae diverging along the stem and branch
(asterisk); stem tip points to the right. P15800 Cbot #1a. Scale bar = 500 m.
ably fits the diagnosis of Tricostaceae, the affinities of the
fourth tricostate type are less obvious. The latter also
features relatively robust gametophytes with very broad
leaves, but the costae are elongate-lenticular in cross section and very strong (more than 200 m wide and 100 m
thick) (Fig. 2A).
Several fossils at Apple Bay exhibit anatomical features (e.g., costal anatomy) suggesting affinities with the
extant family Polytrichaceae. A subgroup of these fossils
share characters indicating that they represent the same
species. This species is characterized by stems with a
conducting central strand and densely inserted leaves
with typical polytrichaceous morphology and anatomy
(Figs. 2B–2D and 3H). The leaves have a broad, unistratose
sheathing base and a much narrower, bistratose free
lamina (Figs. 2D and 3H). The leaf costa is robust and
features complex anatomy (deuters, stereids). Adaxially,
the costa is lined with lamellae (Fig. 2D). Additionally,
Published by NRC Research Press
Pagination not final (cite DOI) / Pagination provisoire (citer le DOI)
Botany Downloaded from www.nrcresearchpress.com by HUMBOLDT STATE UNIVERSITY on 08/23/16
For personal use only.
Tomescu
5
Fig. 2. Early Cretaceous moss gametophytes from Apple Bay (Vancouver Island). (A) A fourth tricostate type; stem cross
section (central tissues not preserved) and leaves with very strong costae (arrowheads indicate three costae of the same leaf);
note free margins (asterisks) of leaf sectioned proximally to its divergence from the stem. P13172 G #23a. Scale bar = 250 m.
(B) Polytrichaceous moss; note lenticular gemmae with large cells at center of stem cross section, surrounded by tightly
packed leaves forming the gemmae cup. P15393 Bbot #1b. Scale bar = bar = 150 m. (C) Polytrichaceous moss; leaf cross
section with details of costa anatomy including large deuter cells and smaller stereids; note adaxial mammillose cells.
P15393 Bbot #10b. Scale bar = 100 m. (D) Polytrichaceous moss; cross section of distal leaf blade; note bistratose lamina and
thick costa with short adaxial lamellae. P15393 Bbot #4b. Scale bar = 100 m. (E) Leucobryaceous moss; cross section of stem
(asterisk; central tissues not preserved) branching in one plane, with one branch on either side; the branch at right has
produced its own branch (arrowhead). P13308 Gbot #57a. Scale bar = 200 m. (F) Leucobryaceous moss, stem cross section;
note characteristic leaves with thick wide costa (consisting of two layers of large leucocysts that sandwich a median layer of
narrow chlorocysts with triangular cross section) and narrow unistratose lamina (marked with asterisks on three leaves).
P13308 Gbot #2a. Scale bar = 150 m. (G) Stem cross section of moss with tristichous phyllotaxis; note triquetrous stem at
center (central tissues not preserved) and leaves tightly packed around it, keeled and with slightly recurved margin (e.g., leaf
at bottom right). P13311 Itop #3d. Scale bar = 150 m. (H) Oblique section of moss with very robust stem (central tissues not
preserved) and strong leaf costae diverging toward the right; the leaf lamina is not preserved; note abundant rhizoids
sectioned all around the stem. P17345 Ctop #1a. Scale bar = 350 m.
the moss produces gemmae in gemmae cups borne at the
tips of gametophyte shoots (Fig. 2B) (Bippus et al. 2013).
This Apple Bay polytrichacean shares the highest number
of characters with Lyellia R. Br., Bartramiopsis Kindb., and
Alophosia Cardot (Bippus et al. 2015), including a bistratose lamina with an abaxial layer of mammillose cells
and a narrow, abaxially rotund costa with highly similar
anatomy. Preliminary results of a morphology-based phylogenetic analysis show the Apple Bay polytrichacean nested
in a clade with Alophosia and Lyellia. However, whereas Lyellia,
Bartramiopsis, and Alophosia are thought to form a basal grade
in the Polytrichaceae (Bell et al. 2015), in this analysis the clade
Published by NRC Research Press
Pagination not final (cite DOI) / Pagination provisoire (citer le DOI)
Botany Downloaded from www.nrcresearchpress.com by HUMBOLDT STATE UNIVERSITY on 08/23/16
For personal use only.
6
including Alophosia + Apple Bay polytrichacean + Lyellia does
not occupy a basal position in the Polytrichaceae, and
tree topology is highly sensitive to outgroup selection
(Bippus et al. 2015). These indicate a need for further
exploration of outgroup options and character coding
regimes; further phylogenetic analyses are ongoing. Nevertheless, irrespective of the exact phylogenetic position
of this Apple Bay polytrichacean, this moss represents
the oldest unequivocal record of the family Polytrichaceae
and of moss gemmae.
Leucobryaceous mosses are also recognized in the Apple Bay flora. The group is represented by a type characterized by gametophytes that branch to form flat splays
(Fig. 2E). Gametophyte stems have marked epidermis–
cortex differentiation and a central conducting strand
(Fig. 3K). The leaves have secund tips and typical leucobryaceous anatomy, featuring a very wide costa that consists of one layer of very narrow, elongated chlorocysts
sandwiched between an adaxial and an abaxial layer of
large leucocysts (Fig. 2F). The leaf lamina, unistratose, is
only about 8 cells wide (Unger et al. 2012). This moss
shares several characters with a few genera in the family:
Leucobryum Hampe, Cladopodanthus Dozy et Molk., Holomitriopsis H. Rob., and Steyermarkiella H. Rob. While closely similar
to Leucobryum, the Apple Bay moss is most similar to
Steyermarkiella, with which it shares chlorocyst shape and
leucocyst arrangement, and from which it differs only in
the shape of leucocysts and the distribution of pores in
leucocyst and laminal cell walls. This Apple Bay moss is
the oldest known record of the leucobryaceous group.
Another moss type present at Apple Bay features a
weakly triquetrous stem bearing tristichous, helically arranged, imbricate and evenly keeled leaves (Fig. 2G). The
leaves are erect and closely spaced, with slightly recurved
margins in the upper half and unistratose lamina, which
can be bistratose near the costa. The strong costa is attenuate and exhibits some differentiation between thickerwalled epidermal cells and thinner-walled internal cells
(Fig. 2G). In the extant flora, select species of some genera
or entire genera exhibiting tristichous helical phyllotaxis are known in several moss families, including the
Meesiaceae, Seligeriaceae, Polytrichaceae, Bartramiaceae,
Catoscopiaceae, Grimmiaceae, Pottiaceae, Fontinalaceae,
Amphidiaceae, and Ditrichaceae. Of these, the Apple Bay
tristichous moss compares well with Seligeria tristicha (Brid.)
Bruch & Schimp. (Seligeriaceae), Anoectangium Schwägr.
and Triquetrella C. Müll. (Pottiaceae), Tristichum mirabile
(C. Müll.) Herz. (Ditrichaceae), and Plagiopus oederianus
H. Crum et L.E. Anderson (Bartramiaceae). A complete
description of this moss type, currently in progress, will
allow for further comparisons leading to more precise
taxonomic circumscription.
Two other Apple Bay mosses are clearly distinct from
those described above but resolution of their systematic
affinities will require in-depth characterization in the
future. One of these is a moss with very robust stems
Botany Vol. 94, 2016
(probably the most robust in the assemblage, at >500 m
diameter) exhibiting a well-defined conducting strand and
broad leaf bases. Leaf costae are also strong, up to 300 m
or more in width and 100 m or more in thickness (Fig. 3A).
The overall figure and complex costal anatomy of this moss
are strongly suggestive of polytrichaceous affinities. The
other moss type features relatively thick stems and robust
leaf costae consisting predominantly of very narrow and
long cells with thick walls; preservation of the leaf lamina
is incomplete (Fig. 2H).
Liverworts
One fossil specimen in the Apple Bay flora bears a close
resemblance to the thalloid liverworts. Among these, the
specimen, although incompletely preserved, exhibits several
features characteristic of the complex thalloid liverworts. The specimen is a wide, flat, relatively thick fragment that is devoid of any strands of conducting tissue
and consists mostly of large cells, similar to those in the
storage layer of complex thalloid liverworts (Fig. 3C). The
upper surface of this specimen preserves groups of irregularly arranged small cells with thin walls (Fig. 3G) that
could represent remnants of an assimilatory layer that
would have been protected by an upper epidermis (which
was not preserved). On the lower surface of the specimen, rhizoid bases are recognized, attached to small
thin-walled cells representing a lower epidermis (Fig. 3D).
Thalloid fossils
Several specimens in the flora represent thalloid plants
whose systematic affinities are difficult to resolve. The
absence of vascular tissues in these specimens precludes
their interpretation as fragments of tracheophyte leaves.
Thus, the only explanation for the nature of these fossils
is that they represent thalloid gametophytes belonging
to one of three groups: hornworts, liverworts, or seedfree plants (ferns, sphenopsids). Unfortunately, owing to
(i) the relative simplicity in morphology and anatomy of
thalloid plant forms; (ii) the broad range of morphological diversity of gametophytes within each group; and
(iii) the lack of extensive comparative studies covering
gametophyte anatomy for the most diverse of the thalloid gametophyte-producing group, the ferns, no operational set of criteria is available for distinguishing between
the gametophytes of the different groups. As a result,
comparisons and taxonomic decisions are speculative.
One fossil is a very thin thallus that exhibits gaps in
the ground tissue between the two epidermal layers. The
lower epidermis bears long, smooth rhizoids (Fig. 3F). It
is unclear whether the gaps in the ground tissue are due
to incomplete preservation or reflect the real anatomy of
the plant. If the latter were true, these gaps would be
consistent with the mucilage clefts present in hornwort
gametophytes or with cavities that host cyanobacterial
colonies, as seen in hornworts and some simple thalloid
liverworts (e.g., Blasia L.).
Published by NRC Research Press
Pagination not final (cite DOI) / Pagination provisoire (citer le DOI)
Botany Downloaded from www.nrcresearchpress.com by HUMBOLDT STATE UNIVERSITY on 08/23/16
For personal use only.
Tomescu
7
Fig. 3. Early Cretaceous gametophytes from Apple Bay (Vancouver Island). (A) Cross section of moss gametophyte of probable
polytrichaceous affinity; note robust stem with central tissues partially preserved and conducting strand (arrowhead), and
leaves with very wide, thick costae, also showing partial tissue preservation (asterisks). P13632 Ftop #1. Scale bar = 200 m.
(B) Thalloid gametophyte cross section; note well-differentiated epidermis, rhizoids attached to or sectioned close to lower
epidermis, and intracellular fungal colonization of central region on the lower side of thallus. P13131 Dtop #30d. Scale bar =
400 m. (C) Cross section of thalloid liverwort gametophyte; note larger cells of storage layer toward upper side of thallus;
light-colored remnants of incompletely preserved assimilatory layer are lining the upper surface of the specimen. P15393 Bbot #1b.
Scale bar = 250 m. (D) Detail of same liverwort thallus as in Fig. 3C; note light-colored rhizoid bases on lower thallus side.
P15393 Bbot #5b. Scale bar = 100 m. (E) Putative bryophyte sporangium comparable in size and wall structure with the
epidermal layer of some liverwort sporangia (e.g., Porella). P13311 Itop #1e. Scale bar = 300 m. (F) Cross section of thin
horizontal thallus with long rhizoids diverging from its lower surface (arrowheads); note rhizoid base (asterisk). P15425 Cbot
#2b. Scale bar = 250 m. (G) Detail of Fig. 3C; note light-colored remnants of incompletely preserved assimilatory layer lining
the upper surface. P15393 Bbot #1b. Scale bar = 200 m. (H) Longitudinal section of bistratose leaf lamina of polytrichaceous
moss in Figs. 2B–2D; note mammillose adaxial cells and squat abaxial cells. P15393 Bbot #1b. Scale bar = 50 m. (I) Cross
section of rhizomatous gametophyte stem with two diverging branches seen in longitudinal section; note faint, incompletely
preserved leaves around all three stems. P17623 Btop #4. Scale bar = 200 m. (J) Polytrichaceous moss, stem cross section with
conspicuous conducting strand (darker, at center); note large deuter cells in cross-sectioned leaf costae. P13158 Cbot #10. Scale
bar = 200 m. (K) Leucobryaceous moss, stem cross section with central conducting strand (consisting of narrow cells with
very thin cell walls). P14330 Bbot #35a. Scale bar = 150 m.
Another fossil is a thallus with upturned sides and
crescent-shaped cross section. The thallus exhibits welldifferentiated epidermal layers on both upper side and
underside (Fig. 3B). The lower epidermis bears rhizoids. A
well-circumscribed region located centrally in the lower
side of the thallus consistently contains intracellular
fungal hyphae (Fig. 3B). This situation is similar to that
seen in liverwort and fern gametophytes colonized by
Published by NRC Research Press
Pagination not final (cite DOI) / Pagination provisoire (citer le DOI)
8
arbuscular mycorrhizal fungi (e.g., Duckett et al. 2006;
Ogura-Tsujita et al. 2016). Because fern and Equisetum gametophytes tend to lack a well-differentiated epidermal
layer, which is conspicuous in most complex thalloid
liverworts (and some simple thalloid liverworts), the fossil is probably a liverwort.
Botany Downloaded from www.nrcresearchpress.com by HUMBOLDT STATE UNIVERSITY on 08/23/16
For personal use only.
Sporophytes
Given the abundance of bryophyte material uncovered
at Apple Bay, the absence of unequivocal bryophyte
sporophytes is intriguing. The many seemingly leafless
bryophyte axes observed in the assemblage initially fueled hopes that they would represent sporophytes. However, most of these axes probably represent rhizomatous
portions of leafy gametophytes. These are usually characterized by smaller, less robust or already decaying
leaves that are more distantly spaced and preserve poorly.
Such is the case of an axis that exhibited no attached
leaves in the plane of section that exposed it initially, but
revealed upon serial sectioning incompletely preserved
leaf bases and branching (Fig. 3I).
If some of the leafless bryophyte axes represent fragments of sporophyte setae, none of those that were followed through serial sections to date has substantiated a
sporangium or a connection to a gametophyte at either
end. Nevertheless, one specimen representing a sporangium with circular cross sectional outline is very similar
in size and anatomy (Fig. 3E) to the epidermal layer with
I-band thickenings found in sporangia of liverworts such
as Porella L. (e.g., Crandall-Stotler et al. 2009).
Discussion
Early Cretaceous bryophyte diversity as seen from
Apple Bay
Of the ca. 70 moss species known from pre-Cenozoic
deposits, only about 10 are known from Early Cretaceous
deposits (Krassilov 1973, 1982; Oostendorp 1987; Ignatov
and Shcherbakov 2011a). With at least nine distinct moss
types representing as many new species and possibly
genera, the Apple Bay flora doubles the number of Early
Cretaceous moss species and increases pre-Cenozoic moss
diversity by more than 10%. This represents a significant
addition to the known diversity of pre-Cenozoic fossil
mosses, especially for the flora of a single locality, and is
surpassed in diversity only by the Late Permian Aristovo
flora on the Dvina River (Russian Platform; Ignatov 1990),
which includes 14 moss species.
The Apple Bay moss flora demonstrates that the Early
Cretaceous vegetation hosted representatives of entirely
extinct groups, as well as those of extant families. At
least four distinct types of tricostate mosses present here
add up to the three known species of Tricostium. While it
is unclear whether all these tricostate types belong in the
hypnanaean family Tricostaceae, this diversity of Mesozoic tricostate mosses that have no close living relatives
demonstrates once again that the fossil record hosts significant sections of biodiversity (such as entire lineages)
Botany Vol. 94, 2016
that would remain unknown in the absence of paleobotanical studies (Shelton et al. 2015).
It is noteworthy that the two Apple Bay types that are
unequivocally assignable to extant families: the gemmaeproducing polytrichaceous type, and the leucobryaceous
type; each combine characters of several genera in their
respective families. This suggests that at least two lineages of modern mosses were represented by stem-group
taxa in the Early Cretaceous. The Apple Bay leucobryaceous moss is most similar to Steyermarkiella, a monotypic genus endemic to the Guayana Highlands of Venezuela
(Gradstein et al. 2001), whereas the polytrichaceous moss
is most similar to Alophosia, another monotypic genus
endemic to the Azores archipelago (Smith 1971). Both of
these cases involve wide, intercontinental distances between the Apple Bay Cretaceous mosses and their putative closest living relatives. Many extant mosses have
intercontinental ranges; in a striking example, Orthotrichum
acuminatum H. Philib., with documented occurrences in
the western Nearctic, the western Palearctic, and Paleotropical eastern Africa, demonstrates that in mosses it is
not impossible even for single species to have multiplecontinent disjunct ranges (Vigalondo et al. 2016). Whereas
the phylogenetic position of Steyermarkiella is unresolved,
Alophosia is resolved as the basal-most member of Polytrichaceae in molecular phylogenetic analyses (Bell et al.
2015). Could these imply that Steyermarkiella and Alophosia
are relictual representatives of basal leucobryaceous and
polytrichaceous groups that were more widely spread
and had originated at least as early as the Early Cretaceous?
Thalloid liverworts are known from rocks as old as the
Middle Devonian (Oostendorp 1987; VanAller et al. 2008)
and, possibly, the Lower Devonian (Guo et al. 2012). Up to
14 species are recorded in the Cretaceous (Oostendorp
1987) and relatively extensive mats of marchantioid liverworts have been reported in the Lower Cretaceous
(Aptian–Albian) of Spain (Diéguez et al. 2007). The presence at Apple Bay of a thalloid liverwort and of thalloid
plant gametophytes, in general, adds to the fossil record
of thalloid gametophytes and is the first documented
occurrence of this type of plants as permineralizations.
Preservation of bryophyte fossils
The bryophytes in the Apple Bay flora provide another
confirmation, possibly the strongest to come, thus far,
from the fossil record, of the excellent preservation potential of bryophytes. These ideas are reinforced by the
fact that the Apple Bay assemblage is undoubtedly allochthonous. The plants are preserved by permineralization within marine sediments, which implies that all the
plant material underwent transport over some distance:
from land into streams, which then transported it to sea,
where it eventually sank to the bottom and was buried in
sediment. Although the bryophyte fossils are among the
smallest bits in the assemblage, they are preserved just
as well as neighboring fragments of wood and conifer
Published by NRC Research Press
Pagination not final (cite DOI) / Pagination provisoire (citer le DOI)
Botany Downloaded from www.nrcresearchpress.com by HUMBOLDT STATE UNIVERSITY on 08/23/16
For personal use only.
Tomescu
needles, and even exhibit delicate, ephemeral parts such
as gametangia.
Given the nature of this allochthonous assemblage,
the plant fragments comprising it probably did not enter
the taphonomic window all at the same time, as demonstrated by the different degrees of decay we see in the
plant tissues across the assemblage. If bryophytes had
low preservation potential, then their presence in the
Apple Bay assemblage would imply that they are part of
the fraction that had the shortest residence time in the
taphonomic window. However, the nature of the assemblage makes this very unlikely. Furthermore, the bryophyte material at Apple Bay shows the same range of
degrees of decay that we see in the other types of plant
material in the assemblage. Thus, if there were any doubts
left about the fossil preservation potential of bryophytes,
the quantity and quality of the bryophyte material in this
allochthonous assemblage thoroughly discount them.
The fact that small and delicate bryophyte structures,
such as gametangia, are preserved in some of the specimens indicates that those specimens were among the
ones that had the shortest residence time in the taphonomic window. These specimens provide a measure of
the timing and intensity of taphonomic processes. The
numerous antheridia documented on one Tricosta gametophyte (Shelton et al. 2015) could have been preserved
only if exposure to taphonomic processes was very short
and the intensity of those processes was low. Thus, we
can infer that the plant experienced transport over a
short distance, resided in the water column for a short
time, and became buried in sediment and permineralized rapidly.
Taphonomic inferences of this type have implications
for understanding some of the interactions in the local
Early Cretaceous ecosystem. For example, the same Tricosta
plant that preserves gametangia is host to a rich community of fungi (Shelton et al. 2014). In assessing the role of
these fungi it is important to take into account the fact
that the host moss had a short residence time in the
taphonomic window — shorter than it takes ephemeral
structures, such as antheridia, to decay. This excludes
the possibility that the fungi were saprotrophs. In other
words, if the entire taphonomic history of the moss is
shorter than the decay time of antheridia, then this interval would not have been long enough to allow for such
dense fungal colonization of the moss post-mortem. Therefore, the fungi colonized the moss while it was living and
represent either necrotrophs or biotrophs. Some of these
fungi show close morphological similarity to bryophilous biotrophic fungi documented in many modern mosses
(e.g., Racovitza 1959; Döbbeler 2002; Döbbeler and Hertel
2013).
Recognizing bryophyte fossils
If bryophytes have good preservation potential, then
their relative scarcity in the pre-Cenozoic fossil record
could be explained by (i) low abundance in the geologic
9
past; (ii) taphonomic biases unrelated to preservation potential (such as growth in environments that hinder entry into taphonomic pathways leading to preservation);
or (iii) an incompletely explored fossil record. The abundance of bryophytes at Apple Bay demonstrates that they
were not rare occurrences in the Early Cretaceous flora,
and that at least a fraction of the bryophyte flora was not
subject to taphonomic biases. Together, these point to an
incompletely explored fossil record as the main cause of
fossil bryophyte scarcity. While this is due at least in part
to a lack of paleobryological capacity, the latter may be
exacerbated by a deficiency in the ability to recognize
bryophyte fossils. Indeed, in addition to generally small
sizes, owing to which bryophytes can easily go unnoticed, the arcane and rich specifics of bryophyte morphology and anatomy are unfamiliar to most paleobotanists.
To start alleviating this situation, I present below
some comments and criteria for recognizing bryophyte
fossils in permineralized material. Developed based on
observations of the Apple Bay flora and out of the need to
address the systematic affinities of bryophytes in this
flora, these criteria are not all-encompassing. For example, the general morpho-anatomical criteria discussed
below necessarily project into the past characters that
differentiate groups of extant plants. Consequently, they
bear the shortcomings of such an approach, and risk
miss-assigning fossils with combinations of characters
unknown in the modern flora. Nevertheless, their application represents a logical first step in the formulation of
working hypotheses aimed at addressing the systematic
affinities of these fossils.
Most of the bryophyte material at Apple Bay stands out
among other plant fossils owing to its coloration, which
is different from that of the vascular plant material.
Whereas the latter generally exhibits shades of chocolatebrown, dark sepia, and russet (wiki/Category:Shades_of_
brown), the bryophytes are usually light yellowish-brown
or light ochre to yellow, and a color-based bryophyte
search image is easily acquired upon familiarization with
the Apple Bay assemblage. The different coloration of bryophyte fossils as compared with that of vascular plants probably reflects differences in cell wall chemistry.
Thalloid bryophytes are most easily identified based
on cross sections of gametophyte thalli, which are devoid of vascular strands that include xylem. However,
widely-applicable and reliable criteria for distinguishing
among these thalloid liverworts (especially simple thalloid liverworts) from hornworts and from pteridophyte
thalloid gametophytes based on cross-sectional anatomy
are not available. These different groups can be identified only in special cases when diagnostic features, such
as pegged rhizoids (complex thalloid liverworts), or characteristic gametangia, are preserved.
Leafy liverworts and mosses are most easily identified
based on gametophyte cross sections that expose stem
and leaf anatomy. They are all recognized as bryophytes
Published by NRC Research Press
Pagination not final (cite DOI) / Pagination provisoire (citer le DOI)
10
Botany Vol. 94, 2016
Botany Downloaded from www.nrcresearchpress.com by HUMBOLDT STATE UNIVERSITY on 08/23/16
For personal use only.
Fig. 4. Early Cretaceous moss gametophytes. (A) Longitudinal section of stem with conspicuous leaf bases; Apple Bay
(Vancouver Island). P13422 D #1. Scale bar = 200 m. (B) Oblique section of incompletely preserved stem (asterisk) and leaves
diverging toward top of image; note leaf costa with polytrichaceous anatomy (large deuter cells; bottom right) and leaf
longitudinal section (bottom right to top left); Budden Canyon Formation (California). HPH219 Ctop #4a. Scale bar = 250 m.
(C) Detail of Fig. 1B showing polytrichaceous leaf anatomy in longitudinal section; note wide-lumen deuter cells and lamella
3–4 cells tall on adaxial side. Scale bar = 50 m.
in this plane of section by the absence of xylemcontaining strands in the stems and leaves. Additionally,
bryophyte leaves have a unistratose lamina (although in
some the lamina can be bistratose; Figs. 2D and 3H). The
presence or absence of a leaf costa (midrib) is a relatively
straightforward criterion for distinguishing liverworts
(characterized by leaves devoid of a costa; ecostate) from
mosses, whose leaves have a more or less robust costa
(and can have several costae per leaf; Shelton et al. 2015).
Additional criteria for distinguishing moss and liverwort
gametophytes include (i) anisophylly, present in liverworts that have three-ranked leaves (two ranks of lateral
leaves and one rank of underleaves); (ii) multicellular
rhizoids present in mosses; and (iii) the presence of a
conducting strand in the stem of some mosses (Figs. 3A,
3J, and 3K). Exceptions to all these criteria, such as
mosses with ecostate leaves, isophyllous liverworts, and
liverworts with a stem conducting strand, exist but do
not hinder identification of the two groups once some
familiarity with bryophyte morphology and anatomy
has been achieved. However, leaf-based criteria are less
useful in the case of rhizomatous basal portions of gametophytes, which usually have more widely spaced,
smaller, and less well-preserved leaves.
For mosses, the cross-sectional anatomy of gametophyte
stems, and particularly leaves, provides diagnostic information allowing for identification of some major
lineages. For example, many Polytrichaceae have robust costae with complex anatomy and typically feature photosynthetic lamellae on the adaxial side of
leaves; leucobryaceous mosses often have broad costae
with a characteristic combination of large leucocysts
and small or narrow chlorocysts; sphagnaleans also have
leaves with a regular arrangement of leucocysts and chlorocysts. Additionally, stem cross sections reveal phyllotaxis,
which can also be a diagnostic character that allows for
narrowing down the systematic affinities of the fossils.
Conversely, longitudinal sections are more difficult to
work with, in terms of documenting leaf anatomy or
phyllotaxis (Fig. 4A). Nevertheless, they reveal relatively
clearly whether a bryophyte has ecostate leaves or bears
costae. Ideally, a combination of cross sections and longitudinal sections through several gametophyte stems
will reveal information about a multitude of diagnostic
characters, allowing for detailed reconstructions and indepth understanding of the morphology and anatomy of
the plants, as well as high-resolution systematic placement (e.g., Steenbock et al. 2011; Shelton et al. 2015).
Recently, application of the search images and criteria
developed during studies of the Apple Bay flora has led
to recognition of a large number of anatomically preserved bryophyte fossils in another Early Cretaceous
marine unit on the West Coast of North America. The
Budden Canyon Formation, in northern California, is
only 8–10 million years younger than the Apple Bay assemblage (Unger and Tomescu 2013) and may soon rival
the Apple Bay flora in bryophyte diversity; it hosts polytrichaceous (Figs. 4B and 4C), leucobryaceous, tricostate,
and other moss types that await detailed studies.
Published by NRC Research Press
Pagination not final (cite DOI) / Pagination provisoire (citer le DOI)
Tomescu
Botany Downloaded from www.nrcresearchpress.com by HUMBOLDT STATE UNIVERSITY on 08/23/16
For personal use only.
Conclusions
Extensive exploration of a permineralized plant fossil
assemblage in the Lower Cretaceous of Vancouver Island,
at Apple Bay, has revealed an abundance of bryophyte
fossils. The Apple Bay flora hosts at least nine distinct
moss types, one complex thalloid liverwort, and two
other thalloid plants (that may represent bryophyte or
pteridophyte gametophytes), as well as potential for
additional discoveries of new bryophytes. All of these
contribute a significant fraction of biodiversity to the
pre-Cenozoic fossil record of bryophytes. Both the abundance and the diversity of bryophyte fossils in the Apple
Bay flora reach levels never before seen in another allochthonous plant fossil assemblage. This fossil bryoflora reveals the presence of extant moss families,
represented by new taxa that combine characters of several extant genera (Unger et al. 2012; Bippus et al. 2013,
2015), as well as of extinct but diverse lineages (Shelton
et al. 2015). Among these are the oldest unequivocal
occurrences for hypnanaean pleurocarps, leucobryaceous
mosses, Polytrichaceae, moss gametangia and gemmae,
and the only known record of permineralized thalloid
liverworts. In-depth characterization of bryophytes in
the Apple Bay flora and other similar assemblages, and
resolution of their systematic affinities is bound to
contribute to understanding of bryophyte evolution
and phylogeny.
Although the Apple Bay plant assemblage is allochthonous, the bryophyte material is well preserved, sometimes in surprising detail (gemmae, gametangia). The
high quality of preservation, along with the abundance
of bryophyte fossils at Apple Bay corroborate previous
observations and experimental data, rejecting the traditional hypothesis that bryophytes have low preservation
potential and demonstrating, instead, excellent preservation potential of these plants. Seen in this perspective,
the scarcity of the pre-Cenozoic bryophyte fossil record
appears to be the result of a combination between the
small size, and thus, more cryptic nature, of bryophytes
and a lack of paleobryological capacity. Fossil floras with
a rich bryophyte content, like the Apple Bay flora, are not
only encouraging for the preservation potential of these
plants, but can also provide excellent opportunities for
cross-disciplinary collaboration between extant bryophyte
systematists and paleobotanists. In turn these will foster
growth in paleobryological capacity and, ultimately, a
more densely sampled and better understood bryophyte
fossil record.
Acknowledgements
I am greatly indebted to the originators of studies of the
Apple Bay flora, Ruth Stockey and Gar Rothwell, for first
recognizing bryophytes in the fossil assemblage, for sharing their material, and for their continued support of work
on these bryophyte fossils. Numerous people developed in
much more detail than presented here several of the fossils
11
included in this article (some of which are being prepared
for future publication): Glenn Shelton, Alexander Bippus,
Christa Unger, Maria Friedman, Christopher Steenbock,
Kelly Matsunaga, Hollister Nadeau, Jamie Burnett, Kara
Frampton, Kyle Brown, Dana Blahnik, and Adolfina Savoretti;
Marie Antoine is thanked for having trained many of these
bryophyte workers. Genaro Hernandez-Castillo and Brian
Atkinson facilitated specimen transfers. Discussions with
Brent Mishler and information provided by Jaakko Hyvönen
and Neil Bell elicited ideas for some of the taxonomic considerations.
References
Atkinson, B.A., Rothwell, G.W., and Stockey, R.A. 2014a.
Hubbardiastrobus cunninghamioides gen. et sp. nov., evidence
for a Lower Cretaceous diversification of cunninghamioid
Cupressaceae. Int. J. Plant Sci. 175: 256–269.
Atkinson, B.A., Rothwell, G.W., and Stockey, R.A. 2014b.
Hughmillerites vancouverensis sp. nov. and the Cretaceous diversification of Cupressaceae. Am. J. Bot. 101: 2136–2147. PMID:
25480710.
Bell, N.E., and York, P.V. 2007. Vetiplanaxis pyrrhobryoides, a new
fossil moss genus and species from Middle Cretaceous Burmese amber. Bryologist, 110: 514–520. doi:10.1639/0007-2745(2007)
110[514:VPANFM]2.0.CO;2.
Bell, N.E., Kariyawasam, I.U., Hedderson, T.A.J., and Hyvönen, J.
2015. Delongia gen. nov., a new genus of Polytrichaceae (Bryophyta) with two disjunct species in East Africa and the
Himalaya. Taxon, 64(5): 893–910. doi:10.12705/645.2.
Bippus, A.C., Shelton, G.W.K., Stockey, R.A., Rothwell, G.W.,
and Tomescu, A.M.F. 2013. A polytrichaceous moss with gemmae from the Early Cretaceous of Vancouver Island (Canada).
Botanical Society of America meeting abstract. Available
from http://2013.botanyconference.org/engine/search/
index.php?func=detail&aid=800 [accessed 17 February 2016].
Bippus, A.C., Stockey, R.A., Rothwell, G.W., and Tomescu, A.M.F. 2015.
Phylogenetic relationships in the Polytrichaceae (Bryophyta): a
morphology-based approach. Botanical Society of America meeting abstract. Available from http://2015.botanyconference.org/
engine/search/index.php?func=detail&aid=589 [accessed
17 February 2016].
Bronson, A.W., Klymiuk, A.A., Stockey, R.A., and Tomescu, A.M.F.
2013. A perithecial sordariomycete (Ascomycota, Diaporthales) from the Lower Cretaceous of Vancouver Island, British
Columbia, Canada. Int. J. Plant Sci. 174: 278–292. doi:10.1086/
668227.
Crandall-Stotler, B., Stotler, R.E., and Long, D.G. 2009. Morphology and classification of the Marchantiophyta. In Bryophyte
biology. 2nd ed. Edited by B. Goffinet and A.J. Shaw. Cambridge University Press, Cambridge, UK. pp. 55–138.
Diéguez, C., Rodríguez-López, J.P., and Meléndez, N. 2007.
Marchantiopsid colonization mats from the Upper Aptian –
Lower Albian of the Escucha Formation (Oliete sub-basin,
Iberian Ranges, eastern Spain). C. R. Palevol. 6: 413–422. doi:
10.1016/j.crpv.2007.09.022.
Döbbeler, P. 2002. Microniches occupied by bryophilous ascomycetes. Nova Hedwig. 75, 275–306. doi:10.1127/0029-5035/
2002/0075-0275.
Döbbeler, P., and Hertel, H. 2013. Bryophilous ascomycetes
everywhere: distribution maps of selected species on liverworts, mosses and Polytrichaceae. Herzogia, 26(2): 361–404.
doi:10.13158/heia.26.2.2013.361.
Duckett, J.G., Carafa, A., and Ligrone, R. 2006. A highly differentiated glomeromycotean association with the mucilagesecreting, primitive antipodean liverwort Treubia (Treubiaceae):
Published by NRC Research Press
Pagination not final (cite DOI) / Pagination provisoire (citer le DOI)
Botany Downloaded from www.nrcresearchpress.com by HUMBOLDT STATE UNIVERSITY on 08/23/16
For personal use only.
12
clues to the origins of mycorrhizas. Am. J. Bot. 93(6): 797–813.
doi:10.3732/ajb.93.6.797. PMID:21642142.
Edwards, D., Duckett, J.G., and Richardson, J.B. 1995. Hepatic
characters in the earliest land plants. Nature, 374: 635–636.
doi:10.1038/374635a0.
Frahm, J.-P. 2010. Die Laubmoosflora des Baltischen Bernsteinwaldes. Weissdorn-Verlag, Jena, Germany.
Goffinet, B., Buck, W.R., and Shaw, A.J. 2009. Morphology, anatomy, and classification of the Bryophyta. In Bryophyte biology.
2nd ed. Edited by B. Goffinet and A.J. Shaw. Cambridge University
Press, Cambridge, UK. pp. 55–138.
Gradstein, S.R., Churchill, S.P., and Salazar-Allen, N. 2001. Guide
to the bryophytes of tropical America. New York Botanical
Garden Press, New York.
Graham, L.E. 1993. Origin of land plants. J. Wiley & Sons, New
York.
Graham, L.E., Wilcox, L.W., Cook, M.E., and Gensel, P.G. 2004.
Resistant tissues of modern marchantioid liverworts resemble enigmatic Early Paleozoic microfossils. Proc. Natl. Acad.
Sci. U.S.A. 101: 11025–11029. doi:10.1073/pnas.0400484101. PMID:
15263095.
Guo, C.-Q., Edwards, D., Wu, P.-C., Duckett, J.G., Hueber, F.M.,
and Li, C.-S. 2012. Riccardiothallus devonicus gen. et sp. nov., the
earliest simple thalloid liverwort from the Lower Devonian
of Yunnan, China. Rev. Palaeobot. Palynol. 176 –177: 35–40.
doi:10.1016/j.revpalbo.2012.03.012.
Harris, T. 1939. Naiadita, a fossil bryophyte with reproductive
organs. Ann. Bryol. 12: 57–70.
Hedenas, L., Heinrichs, J., and Schmidt, A.R. 2014. Bryophytes of
the Burmese amber forest: amending and expanding the circumscription of the Cretaceous moss genus Vetiplanaxis. Rev.
Palaeobot. Palynol. 209: 1–10. doi:10.1016/j.revpalbo.2014.05.
008.
Hemsley, A. 2001. Comparison of in vitro decomposition of bryophytic and tracheophytic plant material. Bot. J. Linn. Soc.
137: 375–384. doi:10.1111/j.1095-8339.2001.tb02332.x.
Hentschel, J., Schmidt, A.R., and Heinrichs, J. 2009. Frullania
cretacea sp. nov. (Porellales, Jungermanniopsida), a leafy liverwort preserved in Cretaceous amber from Myanmar. Crypt.
Bryol. 30: 323–328.
Hernandez-Castillo, G.R., Stockey, R.A., and Rothwell, G.W.
2006. Anemia quatsinoensis sp. nov. (Schizaeaceae), a permineralized fern from the Lower Cretaceous of Vancouver Island.
Int. J. Plant Sci. 167: 665–674.
Hübers, M., and Kerp, H. 2012. Oldest known mosses discovered
in Mississippian (late Visean) strata of Germany. Geology, 40:
755–758. doi:10.1130/G33122.1.
Ignatov, M.S. 1990. Upper Permian mosses from the Russian
platform. Palaeontographica B, 217: 147–189.
Ignatov, M.S., and Shcherbakov, D.E. 2011a. Lower Cretaceous
mosses from Khasurty (Transbaikalia). Arctoa, 20: 19–42. doi:
10.15298/arctoa.20.02.
Ignatov, M.S., and Shcherbakov, D.E. 2011b. Lower Triassic mosses
from Yamanus (Mongolia). Arctoa, 20: 65–80. doi:10.15298/
arctoa.20.04.
Joy, K.W., Willis, A.J., and Lacey, W.S. 1956. A rapid cellulose
peel technique in palaeobotany. Ann. Bot. 20: 635–637.
Katagiri, T., Mukai, M., and Yamaguchi, T. 2013. A new fossil
moss Muscites kujiensis (Bryopsida) preserved in the Late Cretaceous amber from Japan. Bryologist, 116: 296–301. doi:10.
1639/0007-2745-116.3.296.
Kenrick, P., and Crane, P.R. 1997. The origin and early diversification of land plants. Smithsonian Institution Press, Washington.
Klymiuk, A.A., and Stockey, R.A. 2012. A Lower Cretaceous (Valanginian) seed cone provides the earliest fossil record for
Picea (Pinaceae). Am. J. Bot. 99: 1069–1082. doi:10.3732/ajb.
1100568. PMID:22623610.
Botany Vol. 94, 2016
Kodner, R.B., and Graham, L.E. 2001. High-temperature, acidhydrolyzed remains of Polytrichum (Musci, Polytrichaceae) resemble enigmatic Silurian–Devonian tubular microfossils.
Am. J. Bot. 88:462–466. doi:10.2307/2657111. PMID:11250824.
Konopka, A.S., Herendeen, P.S., Smith Merrill, G.L., and
Crane, P.R. 1997. Sporophytes and gametophytes of Polytrichaceae from the Campanian (Late Cretaceous) of Georgia,
USA. Int. J. Plant Sci. 158: 489–499. doi:10.1086/297459.
Krassilov, V.A. 1973. Mesozoic bryophytes from the Bureja Basin, Far East of the USSR. Palaeontographica B, 143: 95–105.
Krassilov, V.A. 1982. Early Cretaceous flora of Mongolia. Palaeontogr. B, 181(1–3): 1–43.
Kroken, S.B., Graham, L.E., and Cook, M.E. 1996. Occurrence
and evolutionary significance of resistant cell walls in charophytes and bryophytes. Am. J. Bot. 83: 1241–1254. doi:10.2307/
2446108.
Little, S.A., Stockey, R.A., and Rothwell, G.W. 2006a. Solenostelopteris
skogiae sp. nov. from the Lower Cretaceous of Vancouver Island. J. Plant Res. 119: 525–532. PMID:16941064.
Little, S.A., Stockey, R.A., and Rothwell, G.W. 2006b. Stramineopteris
aureopilosus gen. et sp. nov.: reevaluating the role of vegetative anatomy in the resolution of leptosporangiate fern phylogeny. Int. J. Plant Sci. 167: 683–694. doi:10.1086/501156.
Mamontov, Y.S., Heinrichs, J., Schafer-Verwimp, A., Ignatov, M.S., and
Perkovsky, E.E. 2015. Hepatics from Rovno amber (Ukraine), 4.
Frullania riclefgrollei, sp. nov. Rev. Palaeobot. Palynol. 223: 31–
36. doi:10.1016/j.revpalbo.2015.08.007.
Matsunaga, K.K.S., Stockey, R.A., and Tomescu, A.M.F. 2013.
Honeggeriella complexa gen. et sp. nov., a heteromerous lichen
from the Lower Cretaceous of Vancouver Island (British Columbia, Canada). Am. J. Bot. 100: 450–459. doi:10.3732/ajb.
1200470.
Ogura-Tsujita, Y., Hirayama, Y., Sakoda, A., Suzuki, A.,
Ebihara, A., Morita, N., and Imaichi, R. 2016. Arbuscular mycorrhizal colonization in field-collected terrestrial cordate
gametophytes of pre-polypod leptosporangiate ferns (Osmundaceae, Gleicheniaceae, Plagiogyriaceae, Cyatheaceae).
Mycorrhiza, 26: 87–97. doi:10.1007/s00572-015-0648-1. PMID:
26047572.
Oostendorp, C. 1987. The bryophytes of the Palaeozoic and the
Mesozoic. Bryophytorum Bibliotheca, 34: 1–112.
Racovitza, A. 1959. Étude systématique et biologique des champignons bryophiles. Mém. Mus. Nat. Hist. Nat. Bot. 10.
Ray, M.M., Rothwell, G.W., and Stockey, R.A. 2014. Anatomically
preserved Early Cretaceous bennettitalean leaves: Nilssoniopteris
corrugata n. sp. from Vancouver Island, Canada. J. Paleontol.
88: 1085–1093.
Rothwell, G.W., and Stockey, R.A. 2006. Combining characters
of Pteridaceae and tree ferns: Pterisorus radiata gen. et sp.
nov., a permineralized Lower Cretaceous filicalean with radial sori. Int. J. Plant Sci. 167: 695–701.
Rothwell, G.W., and Stockey, R.A. 2013. Evolution and phylogeny of gnetophytes: evidence from the anatomically preserved seed cone Protoephedrites eamesii gen. et sp. nov. and
the seeds of several bennettitalean species. Int. J. Plant Sci.
174: 511–529.
Rothwell, G.W., Stockey, R.A., and Millay, M.A. 2014. Evolution of
modern Marattiales; superficially Christensenia-like synangia in the
Early Cretaceous. Botanical Society of America meeting abstract.
Available from http://2014.botanyconference.org/engine/search/
index.php?func=detail&aid=283 [accessed 17 February 2016].
Shelton, G.W.K., Stockey, R.A., Rothwell, G.W., and Tomescu, A.M.F.
2014. Bryosymbiotic fungi from the Early Cretaceous (Valanginian) of Vancouver Island, British Columbia, Canada.
Botanical Society of America meeting abstract. Available
from http://2014.botanyconference.org/engine/search/
index.php?func=detail&aid=751 [accessed 17 February 2016].
Shelton, G.W.K., Stockey, R.A., Rothwell, G.W., and Tomescu, A.M.F.
Published by NRC Research Press
Pagination not final (cite DOI) / Pagination provisoire (citer le DOI)
Botany Downloaded from www.nrcresearchpress.com by HUMBOLDT STATE UNIVERSITY on 08/23/16
For personal use only.
Tomescu
2015. Exploring the fossil history of pleurocarpous mosses:
Tricostaceae fam. nov. from the Cretaceous of Vancouver
Island, Canada. Am. J. Bot. 102: 1883–1900. PMID:26542845.
Shelton, G.W.K., Stockey, R.A., Rothwell, G.W., and Tomescu, A.M.F.
2016. Krassiloviella limbelloides gen. et sp. nov.: additional diversity in the pleurocarpous moss family Tricostaceae (Valanginian, Vancouver Island, British Columbia). Int. J. Plant
Sci. 177: (In press)
Smith, G.L. 1971. Conspectus of the genera of Polytrichaceae.
Mem. N.Y. Bot. Gard. Vol. 21, issue 3.
Smith, S.Y., Rothwell, G.W., and Stockey, R.A. 2003. Cyathea
cranhamii sp. nov. (Cyatheaceae), anatomically preserved tree
fern sori from the Lower Cretaceous of Vancouver Island,
British Columbia. Am. J. Bot. 90: 755–760. PMID:21659172.
Smith, S.Y., Currah, R.S., and Stockey, R.A. 2004. Cretaceous and
Eocene poroid hymenophores from Vancouver Island, British Columbia. Mycologia, 96: 180–186. doi:10.2307/3762001.
PMID:21148842.
Smoot, E.L., and Taylor, T.N. 1986. Structurally preserved fossil
plants from Antarctica: II. A Permian moss from the Transantarctic Mountains. Am. J. Bot. 73: 1683–1691.
Steenbock, C.M., Stockey, R.A., Beard, G., and Tomescu, A.M.F.
2011. A new family of leafy liverworts from the middle Eocene of Vancouver Island, British Columbia, Canada. Am. J.
Bot. 98: 998–1006. doi:10.3732/ajb.1000396. PMID:21613072.
Stewart, W.N., and Rothwell, G.W. 1993. Paleobotany and the
evolution of plants. 2nd ed. Cambridge University Press,
Cambridge.
Stockey, R.A., and Rothwell, G.W. 2009. Distinguishing angiophytes from the earliest angiosperms: a Lower Cretaceous
(Valanginian–Hauterivian) fruitlike reproductive structure.
Am. J. Bot. 96: 323–335. doi:10.3732/ajb.0800295. PMID:21628191.
Stockey, R.A., and Wiebe, N.J.P. 2008. Lower Cretaceous conifers from Apple Bay, Vancouver Island: Picea-like leaves,
Midoriphyllum piceoides gen. et sp. nov. (Pinaceae). Botany,
86(7): 649–657. doi:10.1139/B08-061.
Stockey, R.A., Rothwell, G.W., and Little, S.A. 2006. Relationships among fossil and living Dipteridaceae: anatomically
preserved Hausmannia from the Lower Cretaceous of Vancouver
Island. Int. J. Plant Sci. 167: 649–663. doi:10.1086/503268.
13
Taylor, T.N., Taylor, E.L., and Krings, M. 2009. Paleobotany. The
biology and evolution of fossil plants. 2nd ed. Academic
Press, Burlington, Mass.
Taylor, T.N., Krings, M., and Taylor, E.L. 2014. Fossil fungi. Academic Press, London, UK.
Tomescu, A.M.F., Steenbock, C.M., Friedman, M., and Stockey, R.A.
2012. The Early Cretaceous Apple Bay flora of Vancouver Island: a
hotspot of fossil bryophyte diversity. Botanical Society of
America meeting abstract. Available from http://2012.
botanyconference.org/engine/search/index.php?func=
detail&aid=962 [accessed 17 February 2016].
Unger, C.R., and Tomescu, A.M.F. 2013. Reappraising the Early
Cretaceous permineralized flora of the Chickabally Mudstone
(Budden Canyon Formation, Baremian–Aptian, California).
Botanical Society of America meeting abstract. Available
from http://2013.botanyconference.org/engine/search/
index.php?func=detail&aid=813 [accessed 17 February 2016].
Unger, C.R., Ortiz, A., Stockey, R.A., and Tomescu, A.M.F. 2012.
An anatomically preserved leucobryaceous moss from the Early
Cretaceous (Valanginian–Hauterivian) of Vancouver Island, British
Columbia, Canada. Botanical Society of America meeting abstract.
Available from http://2012.botanyconference.org/engine/search/
index.php?func=detail&aid=646 [accessed 17 February 2016].
VanAller Hernick, L., Landing, E., and Bartowski, K. 2008. Earth’s
oldest liverworts: Metzgeriothallus sharonae sp. nov. from the
Middle Devonian (Givetian) of eastern New York, USA. Rev.
Palaeobot. Palynol. 148: 154–162. doi:10.1016/j.revpalbo.2007.
09.002.
Vavrek, M.J., Stockey, R.A., and Rothwell, G.W. 2006. Osmunda
vancouverensis sp. nov. (Osmundaceae), permineralized fertile
frond segments from the Lower Cretaceous of British Columbia,
Canada. Int. J. Plant Sci. 167: 631–637. doi:10.1086/500994.
Vigalondo, B., Lara, F., Draper, I., Valcarcel, V., Garilleti, R., and
Mazimpaka, V. 2016. Is it really you, Orthotrichum acuminatum?
Ascertaining a new case of intercontinental disjunction in
mosses. Bot. J. Linn. Soc. 180: 30–49. doi:10.1111/boj.12360.
Wellman, C.H., Osterloff, P.L., and Mohiuddin, U. 2003. Fragments of the earliest land plants. Nature, 425: 282–285. doi:
10.1038/nature01884. PMID:13679913.
Wickett, N.J., Mirarab, S., Nguyen, N., Warnow, T.,
Carpenter, E., Matasci, N., et al. 2014. Phylotranscriptomic
analysis of the origin and early diversification of land plants.
Proc. Natl. Acad. Sci. U.S.A. doi:10.1073/pnas.1323926111.
Published by NRC Research Press
