Revision of the Barremian fern Coniopteris laciniata from Las Hoyas and El Montsec (Spain): Highlighting its importance in the evolution of vegetation during the Early Cretaceous

Abstract

The species Coniopteris laciniata and Sphenopteris wonnacottii are heterophyllous ferns recovered from two Spanish Barremian localities, Las Hoyas and El Montsec respectively. The similarities between these species, observed in a study of a total of 66 hand specimens from both localities, indicate that they are conspecific. Following the rule of priority in botanical nomenclature, and because there are doubts about the assignment of this species to a higher taxonomic rank, the name Coniopteris is maintained. Characters of this fern and additional characters of other species of Coniopteris would support a diversification of polypod ferns during the Early Cretaceous. Metric architecture analyses suggest that the heterophylly of the plant was probably caused by the submersion of the apical part of fronds in water during their development, which would be consistent with the taphonomy of the remains in both localities.

Full text

Revision of the Barremian fern Coniopteris laciniata from Las Hoyas
and El Montsec (Spain): Highlighting its importance in the evolution
of vegetation during the Early Cretaceous
Candela Blanco-Moreno
1,2,3
&´
Angela D. Buscalioni
1,2
1Unidad de Paleontología and CIPb-UAM Departamento de Biología, Universidad Autónoma de Madrid, Cantoblanco, Madrid, Spain
2Centro para la Integración en Paleobiología (CIPb-UAM), Universidad Autónoma de Madrid, 28049 Cantoblanco, Madrid, Spain
3Biological Sciences Department, California State Polytechnic University, Humboldt, Arcata, California 95521, U.S.A.
Address for correspondence: Candela Blanco-Moreno, candelablanmor@gmail.com
DOI https://doi.org/10.1002/tax.12888
Abstract The species Coniopteris laciniata and Sphenopteris wonnacottii are heterophyllous ferns recovered from two Spanish
Barremian localities, Las Hoyas and El Montsec respectively. The similarities between these species, observed in a study of a total
of 66 hand specimens from both localities, indicate that they are conspecific. Following the rule of priority in botanical nomenclature,
and because there are doubts about the assignment of this species to a higher taxonomic rank, the name Coniopteris is maintained.
Characters of this fern and additional characters of other species of Coniopteris would support a diversification of polypod ferns
during the Early Cretaceous. Metric architecture analyses suggest that the heterophylly of the plant was probably caused by the sub-
mersion of the apical part of fronds in water during their development, which would be consistent with the taphonomy of the remains
in both localities.
Keywords Early Cretaceous; filiform frond; heterophylly; margin-dweller fern
■INTRODUCTION
The laminated limestones of El Montsec (Barremian of
Lleida, Spain) and Las Hoyas (Barremian of Cuenca, Spain)
are rich in ferns of Coniopteris-like or Sphenopteris-like fo-
liage types. Both taxa were erected as form genera used to de-
scribe fern foliage with different systematic assignments.
Coniopteris Brongn. includes specimens from the Early Juras-
sic to the Early Cretaceous (Li & al., 2020) and this genus is
generally included in Dicksoniaceae (Brongniart, 1849), but
recently, some Coniopteris species have been grouped within
Polypodiales (Li & al., 2020). Sphenopteris Brongn., on the
other hand, includes specimens from localities that encompass
Palaeozoic and Mesozoic concerning both ferns and pterido-
sperms (Taylor & al., 2009). As a result, both genera present
widespread spatial and temporal distributions, and they have
been recorded in many different habitats and environments
(Van Konijnenburg-van Cittert, 2002; Taylor & al., 2009).
The remains assigned to Coniopteris laciniata Diéguez
& N.Meléndez from Las Hoyas and to Sphenopteris
wonnacottii Dilcher & C.R.Hill from El Montsec are morpho-
logically quite similar showing heterophylly with lobed and
filiform pinnules present in the same frond (Diéguez
& Meléndez, 2000; Dilcher & Hill, 2003). Nonetheless,
different interpretations of the heterophylly have been
addressed. Diéguez & Meléndez (2000) suggest that the
reduction of the lamina of pinnules in Coniopteris laciniata
is due to them bearing fertile organs, whereas Dilcher & Hill
(2003) interpret the filiform pinnules in Sphenopteris
wonnacottii as an adaptation to submersion in water, similarly
to the extant Ranunculus aquatilis L. These authors interpret
reniform pinnules at the apical area of the pinnae as fertile,
although no sori were observed.
This contribution is a revision of the El Montsec and Las
Hoyas Coniopteris-like and Sphenopteris-like foliage, in par-
ticular of those specimens which can be assigned either to
Coniopteris laciniata or Sphenopteris wonnacottii. Revising
the assignation of these ferns is relevant because it can prompt
new evidence for the distribution of ferns and possibly the
early distribution and diversification of Polypodiales. To such
extent, 66 specimens from both localities have been studied to
provide a precise description of the plant, and 24 specimens
have been metrically characterised by means of the branching
algorithms method (Campbell, 1996; Blanco-Moreno
& al., 2019). Establishing the variability of the pinnules of
these ferns and identifying the architectural factors that char-
acterize lobed and filiform pinnules allow for a more precise
determination and comprehension of the whole plant. The re-
sults of this comparative study have consequences on the
interpretation of both the palaeoecology and distribution of
Article history: Received: 18 Jun 2022 | returned for (first) revision: 27 Oct 2022 | (last) revision received: 26 Jan 2023 | accepted: 9 Feb 2023
Associate Editor: Jim Doyle | © 2023 The Authors.
TAXON published by John Wiley & Sons Ltd on behalf of International Association for Plant Taxonomy.
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TAXON 00 (00) •1–13 Blanco-Moreno & Buscalioni •An heterophyllous Early Cretaceous fern
RESEARCH ARTICLE

these ferns. A discussion of the habit and habitat of the plants
is also presented.
Geological context and taxonomic background. —El
Montsec fossil site is located in the Serra del Montsec, in the
province of Lleida (South Central Pyrenees, OrganyàRift
Basin; Martín-Chivelet & al., 2019), and comprises two sites
in the same area: La Pedrera de Meià, coordinates 46°55′N;
03°26′E, and La Cabrúa, coordinates 46°55′N; 03°32′E
(de Gibert & al., 2000), which are Barremian in age (Martín-
Chivelet & al., 2019). The sites correspond to the same
sequence of laminated limestones (Barale & al., 1984) that
was interpreted as deposits generated in open lacustrine condi-
tions (de Gibert & al., 2000).
Las Hoyas fossil site (coordinates 40°05′N; 01°53′W) is
located in the Serranía de Cuenca (southwestern Iberian sec-
tor; Fregenal-Martínez & Meléndez, 2016), in the municipal-
ity of La Cierva, and has been proposed as the parastratotype
of La Huérguina Formation. Las Hoyas consists of a set of
laminated limestone lithosomes deposited during the Barre-
mian, 126 to 129 Ma, based on charophytes and ostracods
(Diéguez & al., 1995; Vicente & Martín-Closas, 2013) and
this formation has been interpreted as a freshwater, regional,
inland subtropical system of wetlands (Fregenal-Martínez
& al., 2017).
In relation to the palaeobotanical content, Vidal (1902,
1915) was the first to identify Coniopteris-/Sphenopteris-like
foliage at El Montsec and assigned it to Sphenopteris
cf. microclada Saporta. In more modern revisions, Menéndez
Amor (1951) assigned the Sphenopteris-like specimens to Hi-
menophyllites tenellinervis Saporta, but Teixeira (1954) and
Barale (1995) did not figure or discuss them. Later, Dilcher
& Hill (2003) described a new species, Sphenopteris wonna-
cottii Dilcher & C.R.Hill, based on remains from El Montsec
that are housed at the Natural History Museum, London.
At Las Hoyas, Diéguez & Meléndez (2000)werethefirst
to identify two species of Sphenopteris (S. fontanei Seward,
S. fittonii Seward), and two species of Coniopteris
(C. laciniata Diéguez & N.Meléndez, C. murrayana Brongn.).
The specimens identified as the genus Sphenopteris and the
species Coniopteris cf. murrayana Brongn. by Diéguez & Me-
léndez (2000) were discussed as belonging to genera Ruffordia
Seward or Cladophlebis Brongn., in the corresponding
synthesis on the Las Hoyas floral association (Martín-Closas
& al., 2016).
■MATERIALS AND METHODS
The fern material presenting Sphenopteris-like or
Coniopteris-like foliage from Las Hoyas, housed in the
Museo de Paleontología de Castilla-La Mancha (Cuenca,
Spain), and from El Montsec, housed in the Institut d’Estudis
Ilerdençs (Lleida, Spain) and in the Muséum national
d’Histoire naturelle (Paris, France), was thoroughly revised
and described in detail to identify specimens that could be
assigned either to Coniopteris laciniata or Sphenopteris
wonnacottii. Additionally, high-resolution pictures of the
holotype of Sphenopteris wonnacottii (BMNH V.41257;
Dilcher & Hill, 2003), housed at the Natural History Museum
(London, U.K.) were studied (Fig. 1A,B). The remains of
these two taxa mainly consist of penultimate and ultimate pin-
nae (Fig. 1). Additionally, two specimens preserving the rhi-
zome and attached pinnae have been recovered: one from El
Montsec presenting lobed pinnules, and another from Las
Hoyas presenting filiform pinnules (Fig. 2). The remains were
compared by a descriptive morphological study of each
species.
Material examined. —The material from Las Hoyas con-
sists of 39 hand specimens with one fragment each, and the ma-
terial from El Montsec consists of 27 fragments preserved in
13 hand specimens. Las Hoyas: MUPA-LH 371, 6337 a/b,
13576 a/b*, 14357 a/b*, 17262, 20016*, 20227 a/b, 20287
a/b, 20336, 20463 a/b, 21028 a/b, 21194*, 22448 a/b*, 23057
a/b, 23112, 23266 a/b*, 23459 a/b*, 26047*, 26375 a/b*,
28057, 28063 a/b, 28272 a/b, 28537*, 29498, 29729, 30368,
30451*,30763*, 30836, 30837*, 30923, 31024 a/b*, 31028
a/b*, 31321 a/b, 31432 a/b*, 31433 a/b*, 33314, 35579 a/b,
39368*.ElMontsec:BMNHV.41257*; G-421; LC-965-IEI*,
2901*; LP93-4043-IEI*, 4228; LP-491-IEI, 1593*, 4062;
LP-1281-P; MNHN.F.17717, 17719, 17720 a/b. Hand speci-
mens included in the metric analysis are marked by an asterisk.
Institutional abbreviations. —ADR-P, Armando Diaz
Romeral collection, this abbreviation corresponds to the holo-
type of Coniopteris laciniata and the specimen is lost. BMNH
V, Palaeobotany collection at the Natural History Museum,
London, U.K.; G, Gomez collection, and LC-IEI, LP-IEI
and LP-P El Montsec collection, all housed at the Institut
d’Estudis Ilerdençs, Lleida, Spain; MUPA-LH, Las Hoyas
Collection at the Museo de Las Ciencias de Castilla-La Man-
cha, Cuenca, Spain; MNHN.F, Palaeobotany collection at the
Muséum national d’Histoire naturelle, Paris, France.
Taphonomic analysis. —Taphonomy, herein, explores
two aspects: the preservation type, and fragment size. The
preservation type includes four categories: charred compres-
sions, impressions (imprints on the sediment), brownish com-
pressions, and calcite infillings. Shiny black compressions are
included within “brownish compressions”. The size of each
fragment was recorded as the maximum length of the frag-
ment. The proportion of each preservation type was revised
for each locality, and the size distribution was graphed on a
histogram. The significance of the difference in the distribu-
tion of fragment sizes per type of preservation was tested by
Mann-Whitney non-parametric by pairs in SPSS Statistics
v.27 software (IBM corporation).
Metric analysis. —A metric architecture analysis was im-
plemented to observe differences between lobed and filiform
pinnules, and to explore the variation within each type of pin-
nule. Nineteen fragments (18 specimens) from Las Hoyas
were measured: 1 filiform ultimate pinna attached to the rhi-
zome, 1 penultimate pinna, and 17 ultimate pinnae; 6 filiform,
and 11 lobed. Also, 6 fragments (5 specimens) from El Mon-
tsec: 1 lobed ultimate pinna attached to the rhizome, and 5
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isolated ultimate pinnae; 2 filiform, 3 lobed, and 1 showing
the transformation from lobed to filiform. The method of
branching algorithms adapted by Blanco-Moreno & al.
(2019) was herein applied to test the variation of three vari-
ables along the pinna: (1) the insertion angle (from now on
IA), measured as the smallest angle formed at the inter-
section between the pinna rachis and the pinnule petiolule;
(2) distance between pinnae (from now on DBP), measured
as the length between the adaxial side of one petiolule to the
next; and (3) first segment length (from now on FSL), mea-
sured as the length of the petiolule, up to the first lobe or
branch of the pinnule (Fig. 3). When the FSL was not observ-
able in completely fused lobed pinnules, pinnule length was
used. All visible pinnules along the rachis were measured,
and measurements from both the left and the right pinnules
of each specimen were recorded and included in the analyses.
Fig. 1. Coniopteris laciniata.A&B, BMNH V.41257, part and counterpart of the holotype of Sphenopteris wonnacottii, preserving lobed and
filiform pinnules (photographs provided by Trustees of the Natural History Museum, London): A, BMNH V.41257a; B, BMNH V.41257b.
C, Ultimate pinna with f iliform pinnules from Las Hoyas (MUPA-LH 31432). D, Ultimate pinna with long lobed pinnules from Las Hoyas
(MUPA-LH 30836). E, Ultimate pinna preserving the transition from lobed to reniform pinnules from El Montsec (LP-491-IEI). F, Ultimate pinna
with lobed pinnules from El Montsec (MNHN.F.17720). G&H, Penultimate pinna fragments from Las Hoyas: G, MUPA-LH 21028;
H, MUPA-LH 20016. —Scale bars = 5 mm.
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Measurements were taken on photographs using the software
ImageJ v.2 (Schneider & al., 2012).
The branching ratio (from now on BR), comparison be-
tween DBP and FSL, was observed by plotting these variables
on an xy graph and linear regressions were calculated for each
of the pinnule types. Additionally, a principal component
analysis (from now on PCA) was performed, using a correla-
tion matrix, and including IA, DBP and FSL. The results of
the BR and PCA were graphed distinguishing between the
types of pinnule and between localities. These analyses were
performed using PAST v.4 software (Hammer & al., 2001).
■RESULTS
Systematic Palaeontology
Order: Incertae sedis
Family: Incertae sedis
Genus: Coniopteris Brongn. in d’Orbigny, Dict. Univ. Hist.
Nat. 13: 75. 1849.
Coniopteris laciniata Diéguez & N.Meléndez in Palaeontol-
ogy 43: 1121. 2000 –Lectotype (designated here):
[illustration in] Palaeontology 43: 1123, t. 2, fig. 1 & 2.
2000.
=Sphenopteris wonnacottii Dilcher & C.R.Hill in Courier
Forschungsinst. Senckenberg 241: 112. 2003 –Holotype:
BMNH V.41257 [pictured in Courier Forschungsinst.
Senckenberg 241: 112, text-fig. 1; 117, t. 1, fig. 1 & 2].
Emended species diagnosis. –Creeping rhizome, bearing
roots in an abaxial position that dichotomise at least once.
Fronds once- or twice-pinnate, borne in an adaxial position,
crowded in thick areas of the rhizome. Pinnae catadromically
alternate bearing polymorphic, catadromically alternate or
rarely subopposite, pinnules. Three types of pinnules are pre-
sent: (1) deeply lobed pinnules, with up to 5 lobes; (2) filiform
Fig. 2. Specimens and corresponding drawings of Coniopteris laciniata preserving the rhizome. A&B, Specimen MUPA-LH 31433 from Las
Hoyas, presenting filiform pinnules; C&D, Specimen LC-965-IEI from El Montsec, presenting lobed pinnules. —Scale bars = 5 mm.
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pinnules, larger in size, presenting very reduced lamina; (3) re-
niform pinnules. A continuum of forms connects all three
types of pinnules.
Description. –Rhizome creeping, no clear branching is
observed. Width homogeneous in areas where few or no
fronds are borne, measuring up to 1.8 mm. Rhizome becomes
more massive (up to 3 mm thick) and irregular where leaf and
root insertions accumulate (Fig. 2). Roots arise from the abax-
ial part of the rhizome, measuring at least 8.5 mm long and
0.5 mm wide. Fronds twice-pinnate, emerging from the adax-
ial part of the rhizome at irregular intervals, tending to accu-
mulate in certain areas. Leaves are born singly or in pairs.
A crozier attached to the rhizome is observed (Fig. 2A,B),
evidencing circinate vernation. Penultimate rachis flexuous,
0.2 to 1.5 mm wide. Ultimate pinnae are generally alternate
and rarely subopposite, inserted at a wide angle (60°–80°),
and 1.9 to 6.8 mm apart from each other. Rachis width of
the ultimate pinnae 0.2 to 1 mm, bearing polymorphic sphe-
nopteroid pinnules inserted in catadromous disposition, sub-
opposite to alternate, and attached to the rachis by a short
petiolule or a very constricted base. Pinnules are generally in-
serted from 1 to 5 mm from each other, and at an angle of
50° to 70°, although basal most and apical most pinnules are
inserted at lower angles (35°–45°). Three main types of pin-
nules are identified, although a continuum between each type
is observed:
(1) Lobed pinnules (Figs. 1A,B,F–H,2C,D). Basal pin-
nules are deeply lobed, consist of up to 5 catadromous lobes,
and measure up to 5.7 mm long and 3.2 mm wide.
Intermediate pinnules generally present 3 lobes and measure
around 3 mm long and 3 mm wide. The smallest apical pin-
nules are 0.8 mm long and 0.9 mm wide and have 2 lobes.
Venation is open dichotomous and generally catadromous.
The main vein dichotomises into each of the lobes of the pin-
nule, and veins successively dichotomise inside the lobes,
from one to three times. The number of successive dichoto-
mies is related to the size of the pinnule.
(2) Filiform pinnules (Figs. 1C,D,2A,B). The widest ra-
chises are associated to areas bearing filiform pinnules. These
pinnules are inserted further apart than the other types of pin-
nules (up to 11 mm), and at a smaller angle (35°–55°). They
branch in catadromous, and rarely anadromous disposition,
and measure up to 12.6 mm. No fertile organs are observed.
(3) Reniform pinnules (Fig. 1E). These pinnules are ob-
served at the apical-most part of some pinnae bearing lobed
pinnules exclusively, they have a reniform morphology, and
venation is not observed. Size at Las Hoyas is from 1.4 to
2.2 mm long and 1.3 to 2 mm wide, the size at El Montsec
is smaller, from 0.8 to 1.8 mm long and 0.9 to 1.8 mm wide.
No fertile organs are observed.
Pinnae presenting a transition between types have been
observed but are very rare (Fig. 1A,B,D,E herein and
pl. 2 fig. 1 in Diéguez & Meléndez, 2000), and most speci-
mens present either filiform or lobed pinnules exclusively
(Figs. 1C,F–H,2). Pinnae attached to the rhizome, bearing ei-
ther lobed or filiform pinnules, have been observed (Fig. 2).
These two pinnule morphologies are independent of their po-
sition within the pinna. Reniform pinnules have only been ob-
served in a specific position, at the apex of pinnae bearing
lobed pinnules and not filiform pinnules.
Holotype. –ADR-0119-P. Pictured in plates 2 and 3, and
text-figure 4A,B in Diéguez & Meléndez (2000). Physical
specimen lost.
Type localities. –Santa Maria de Meià(La Pedrera),
Lleida (Spain), and Las Hoyas, Cuenca (Spain).
Stratigraphic occurrence. –La Pedrera de Rúbies Unit
(de Gibert & al, 2000), and La Huérguina Formation
(Fregenal-Martínez & al., 2017).
Age. –Barremian, Early Cretaceous.
Discussion. –The three types of pinnules herein observed
correspond to the “frond forms”described for Sphenopteris
wonnacottii (Dilcher & Hill, 2003). Based on the fragmentary
condition of most of the specimens herein analysed, the con-
tinuum of pinnule forms observed in them, and the variability
of their position in the frond, we prefer to note the hetero-
phylly as a pinnule-level trait and use types of pinnules, rather
than frond forms. Variability in ferns can be very high, where
the form is controlled during its growth, and it is generally
linked to the venation pattern during its development
Fig. 3. Criteria used for the metric analysis represented on lobed (green)
and filiform pinnules (blue), and twice-pinnate specimens (purple). IA,
insertion angle; DBP, distance between pinnae; FSL, first segment
length.
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(Zurakowski & Gifford, 1988). Different types of pinnules
could therefore be found in the same frond from a develop-
mental point of view and would not necessarily be conserved
along the same pinna or frond.
Our accurate study of all specimens analysed indicates
that Sphenopteris wonnacottii is indistinguishable from
Coniopteris laciniata (Diéguez & Meléndez, 2000), hence
these two species should be considered conspecific. Follow-
ing the rule of priority of the International Code of
Nomenclature for algae, fungi, and plants (Turland & al.,
2018), the name Coniopteris laciniata should be maintained
and Sphenopteris wonnacottii become its heterotypic syno-
nym. The holotype of Coniopteris laciniata (ADR-0119-P)
designated by Diéguez & Meléndez (2000) cannot be found
in the institution referenced by the authors, and they did not
designate paratypes, isotypes, or mention any other specimens
that could be assigned to this species in their work. Therefore,
an illustration of the holotype (ADR-0119-P) provided by
Diéguez & Meléndez (2000) in protologue of the species has
been designated as lectotype.
The filiform pinnules herein described are comparable to
Sphenopteris microclada Saporta (Saporta, 1894). However,
due to only filiform pinnules being described for this species,
the name Coniopteris laciniata is tentatively maintained for
the material herein presented, which shows three distinct pin-
nule forms, until more material can be revised. The generic
name Coniopteris is maintained here due to the impossibility
to assign this species with certainty to either Sphenopteris or
Fig. 4. Proportion of preservation
types and size distribution per pres-
ervation type for the 66 Coniopteris
laciniata fragments revised. A, Las
Hoyas; B, El Montsec. —Black,
charred compressions; grey, im-
pressions; brown, brownish com-
pressions; light brown, calcite
infillings.
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Coniopteris as no sori have been identified. Coniopteris fre-
quently presents both sterile-fertile and basal-apical pinnule
dimorphism, and finely dissected pinnules are frequent in
the genus (Harris, 1961; Taylor & al., 2009). As far as we
know, no fossil or extant fern with a comparable morphology
and variability in pinnule form and position within the plant
has been published to date.
Remarks. –This taxon was first discovered at Las Hoyas,
by Diéguez & Meléndez (2000). However, the frond dimor-
phism was underestimated, and it was not until Dilcher & Hill
(2003) described this same species as Sphenopteris wonnacot-
tii based on material from El Montsec that the degree of reduc-
tion of the pinnule lamina was ascertained. After comparison
with material from El Montsec, we have observed that the
specimens assigned to Sphenopteris fontanei and Coniopteris
cf. murrayana by Diéguez & Meléndez (2000) correspond to
two different pinnae forms of Coniopteris laciniata: the fili-
form pinnule area, and the form with typical lobed pinnules
respectively.
Taphonomy. —Fossil fragments from El Montsec are all
preserved as brownish compressions except for one impres-
sion (Fig. 4B). The mean size is 1.4 cm and the largest frag-
ments have filiform pinnules. At Las Hoyas, this species is
most frequently found preserved as brownish compressions,
consisting of 67% of the remains (Fig. 4A). Charred remains
are the second most frequent preservation type, corresponding
to 20% of the total sample. Four impressions have been recov-
ered (that is 10% of the total remains), and only one specimen
is preserved as a calcite infilling. The size distribution of the
charred compressions, brownish compressions, and impres-
sions (Fig. 4A) are significantly similar (Mann-Whitney tests
by pairs Sig. > 0.05). At Las Hoyas, the mean size of the frag-
ments is 3.16 cm, much larger than the material from El Mont-
sec, and the size distribution is signif icantly different between
the two localities (Mann-Whitney test Sig. = 0.001). Addi-
tionally, 53% of the specimens recovered from Las Hoyas
are incomplete and therefore the fragment would be longer
than observed (the hand specimen is broken, and the plant re-
main would have continued in the missing rock). Similarly to
El Montsec, fronds with filiform pinnules are all preserved as
brownish compressions and are larger in mean size than the
lobed remains (5.03 cm in mean).
Metric architecture analysis. —Both lobed and filiform
pinnules show metric differences (Figs. 5, 6). IA is smaller in
filiform pinnules, although they are very variable in both pin-
nule types, and there is no clear tendency along the pinna
(Fig. 5A). DBP and FSL both diminish towards the apex in
lobed pinnules. However, in the case of filiform pinnules,
FSL grows towards the apex, and the variation of DBP along
the pinna does not follow a clear pattern (Fig. 5B,C).
The BR analysis clearly separates the pinnule types, and
the general distributions of lobed and filiform pinnules
can be described by linear regressions (Fig. 6A; lobed:
y= 0.55x+ 0.09, R
2
= 0.57; filiform: y= 3.27x+ 0.21,
R
2
= 0.304) with a general positive correlation between DBP
Fig. 5. Mean and standard deviation of the measurements along the pin-
nae performed on Coniopteris laciniata from Las Hoyas. A, Insertion
angle (IA); B, Distance between pinnae (DBP); C, First segment length
(FSL). —Green, lobed pinnules; blue, filiform pinnules.
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and FSL, although it is not very robust, especially for the fili-
form pinnules.
In the PCA, the loadings of each variable in the two prin-
cipal components (from now on PCs) included in the graph
show that all of them contribute to the description of the frond
architecture separately (Table 1). The results show that in gen-
eral, filiform pinnules have a larger DBP, less variable and
generally smaller FSL, and much smaller IA, whereas lobed
pinnules have a larger range of FSL (Fig. 6B).
Notwithstanding, the specimen preserving the transition
between lobed and filiform pinnules (BMNH V.41257,
squares in Fig. 6A,B) shows very small pinnules and the three
variables do not follow the same distribution along the pinna
as the rest of the specimens studied. In this case, IA values
are constant along the pinna and FSL is longer in the filiform
pinnules. However, there is an increase in DBP towards the fi-
liform pinnules, similarly to what is observed in other speci-
mens. In both the BR and PCA analyses, the values of the
lobed pinnules in this specimen are grouped with the rhizome
bearing lobed pinnules (LC-965-IEI; green stars in Fig. 6A,B)
and the basal pinnae of the twice-pinnate specimen
(MUPA-LH 20016, purple dots in Fig. 6B). Interestingly,
the apical-most pinnae of twice-pinnate fronds, which are
fused into single pinnules (Fig. 1H), are grouped with the
lobed remains. The specimen preserving ultimate pinnae with
filiform pinnules attached to the rhizome (MUPA-LH 31433,
blue stars in Fig. 6B), shows a unique distribution in the PCA,
situated in between lobed and filiform remains.
■DISCUSSION
All the remains herein studied belong to a single species,
with a continuum of pinnule variation and two extreme mor-
phologies that are architecturally distinct. These results allow
for discussions and interpretations of the plant’s habit and aut-
ecology, exploring the two hypotheses for the presence of the
filiform morphology, fertile vs amphibious, in depth.
Fig. 6. Results of the metric analyses of specimens from Las Hoyas (filled-in shapes) and El Montsec (empty shapes). A, Branching ratio;
B, PCA. —Green, lobed pinnules; blue, filiform pinnules; purple, twice pinnate (MUPA-LH 20016). Squares, specimen that shows pinnule type
transition (BMNH V.41257); stars, pinnae attached to rhizome (MUPA-LH 31433, f illed-in blue stars; LC-965-IEI, empty green stars).
Table 1. Principal component loadings for principal component
analysis.
Component
12
Insertion angle (IA) −0.641 0.289
Distance between pinnae (DBP) 0.637 −0.318
First segment length (FSL) 0.429 0.903
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Plant habit and autecology. —Specimens displaying
both once-pinnate and twice-pinnate fronds are present in the
sample. Although Diéguez & Meléndez (2000) describe the
plant as tripinnate, no evidence of this has been observed in
the specimens herein studied. The two specimens preserving
the rhizome (LC-965-IEI, MUPA-LH 31433), bear fronds
that seem to be once pinnate, although the connection of
the pinnae and the rhizome is not always clear (Fig. 2). Other
studied specimens show clearly bipinnate fronds (G-421;
MUPA-LH 17262, 20016, 21028). The similarity in archi-
tecture observed between the penultimate pinnae and the
once-pinnate pinnae with lobed pinnules borne on the
rhizome (LC-965-IEI), suggest that although the pinnae
attached to the rhizome are once pinnate, the architecture is
closer to twice-pinnate fronds than to the isolated once-
pinnate ultimate pinnae. This could indicate that specimen
LC-965-IEI corresponds to a young sporophyte, where
fronds are once pinnate and would become twice pinnate
during maturation. This condition can be observed in extant
ferns such as Angiopteris evecta (G.Forst.) Hoffm. within the
family Marattiaceae. The small size of this specimen also
corroborates this hypothesis (Fig. 2). The unique architec-
ture observed in the once-pinnate pinnae bearing filiform
pinnules that are attached to the rhizome in this fern
Fig. 7. Drawings representing the variability in the leaf morphology of specimens. A–D,Coniopteris laciniata:A, The missing holotype
ADR-0119-P, figured by Diéguez & Meléndez (2000); B, BMNH V.41257; C, MUPA-LH 30451; D, MUPA-LH 21194. E, Fertile specimen
(IRSNB b 7856, housed at the Royal Belgian Institute of Natural Sciencies in Brussels, Belgium) of Coniopteris sp. from the Barremian-Aptian
locality of Bernissart (Mons Basin, Belgium). F, Sterile specimen of Coniopteris simplex redrawn from Harris (1961). G,Ranunculus flabellaris
Raf. based on specimens figured by Bostrack & Millington (1962).
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(MUPA-LH 31433) could also indicate a young sporophyte,
although it is larger in size than LC-965-IEI. As no bipinnate
fronds with filiform pinnules have been observed in the
current sample, this possibility cannot be ruled out.
The architectural differences identified between pinnae
bearing lobed pinnules and pinnae bearing filiform pinnules
in Coniopteris laciniata argue against the filiform pinnules be-
ing homologous to the fertile pinnae in some Coniopteris spe-
cies. Other Coniopteris taxa with skeletonised areas that bear
sori are clearly pinnate, and when the whole skeletonised area
corresponds to a lower-order pinna, the rachises are straight
(Fig. 7F). This is not the case for the filiform pinnules in Con-
iopteris laciniata, where the dichotomies follow the pattern of
the venation of the lobed pinnules, which is not pinnate but di-
chotomous. Filiform pinnules themselves are significantly
larger than lobed pinnules in Coniopteris laciniata and dichot-
omise many times (Fig. 7A–D). Skeletonised fertile pinnae of
other Coniopteris species do not dichotomise more than once
and are normally the same size as the pinnules preserving the
lamina (see Fig. 7E,F and Coniopteris species discussed in
Harris, 1961 for example). Additionally, no indusia comparable
to those interpreted by Diéguez & Meléndez (2000) were iden-
tified on the filiform pinnules. On the other hand, the morpho-
logical diversity of the submerged leaves of the extant aquatic
taxon Ranunculus flabellaris Raf. is more similar to that ob-
served in Coniopteris laciniata (Fig. 7A–D,G) as already men-
tioned by Dilcher & Hill (2003). The pinnules in Coniopteris
laciniata show a clear increase in the size and architectural com-
plexity of the pinnules as they become filiform, similarly to
what occurs in other submerged leaves (Fig. 7G).
There are clear differences between the architecture ob-
served in the specimen described by Dilcher & Hill (2003),
BMNH V.41257, which presents both lobed and filiform pin-
nules, and the general architecture of the rest of the specimens.
Lobed and filiform pinnules in this specimen are grouped with
intermediate forms, but the general tendency of the pinnule
architecture along the pinna is reversed due to the increase
in FSL and also large IA observed for the filiform pinnules.
The anomaly in the FSL trend, however, agrees with the gen-
eral tendency in pinnae bearing filiform pinnules, which
shows an increase towards de apex. IA is much conserved in
this specimen, with values in the lobed-pinnule range. As pin-
nule insertion angle is established before the pinna unfurls, the
large insertion angle in the range of lobed pinnules would sug-
gest this pinna initially developed out of water and was sub-
merged at a later stage of its development. Extant
amphibious plants that present heterophylly respond to differ-
ent environmental factors that are related to underwater condi-
tions during their development. For example, the fern
Marsilea L. grows aerial-type leaves, which are broader and
less dissected, in presence of blue light and high levels of
CO
2
(Lin & Yang, 1999). Additionally, the small size of the
pinna fragment and its pinnules, together with similarity of
the lobed pinnule segment of the specimen preserving both
types of pinnules (BMNH V.41257) with the architecture of
the pinnae attached to the rhizome from El Montsec (LC-
965-IEI) could suggest this specimen is also juvenile. In this
case, differences in architecture could also be due to the imma-
turity of the specimen.
Plant habitat. —The taphonomic analyses show that there
is a small proportion of charred remains of this species, indicat-
ing that it would not have been frequently affected by fires, and
that most of the material of this fern preserved at Las Hoyas and
El Montsec was produced by other agents. Fire is a very fre-
quent agent in the production of other fern species in these lo-
calities, for example Weichselia reticulata (Stokes & Webb)
Fontaine (Martín-Closas & al., 2016). Also, the remains of
Coniopteris laciniata at Las Hoyas show differences in size
and abundance in relation to other ferns from the locality, the
mean fragment size is significantly larger for this species, and
its remains are comparably not very abundant (see Blanco-
Moreno & al., 2018 for data on Weichselia reticulata as a
Fig. 8. Whole plant schematic re-
construction showing general habit
and pinnule morphological
diversity.
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comparison). This could be interpreted as evidence that the
plants lived at a larger distance from the depositional site, due
to the low abundance of remains, and the possibility to be trans-
ported during a longer period of time, as larger fragments take
more time to waterlog (Nichols & al., 2000). However, low
abundances of plant species can also occur due to a preservation
bias by selective decay, where taxa that are locally abundant and
live near the depositional environment are more readily de-
graded by detritivores, and hence more rarely preserved
(Spicer, 1991). In addition, the preservation of the rhizome
of the plant also suggests para-autochthony, and rhizomes
are very rare remains in both localities. Moreover, if the re-
mains were produced in lentic environments such as pools
and lakes, the size selection would be mainly influenced by
the architecture of the plant and necrobiotic agents instead
of transport in water (Blanco-Moreno & al., 2022), which
inthecaseofConiopteris laciniata might be different from
the other fern species from Las Hoyas, producing larger frag-
ments (Blanco-Moreno, 2020).
Plant reconstruction. —The results of the analyses herein
performed would indicate that Coniopteris laciniata was a
small fern with tufts of leaves arising at intervals from thin,
creeping rhizomes (Fig. 8). Fronds were twice pinnate in matu-
rity and once pinnate in young specimens. Pinnae bore filiform
pinnules when they developed underwater, and lobed pinnules
when they developed subaerially. The habitat of this plant was
probably alkaline soils at the margin of the pools and ponds of
Las Hoyas and El Montsec where the remains were deposited,
or on the margin of streams and creeks that flowed into those
water bodies.
Systematic importance. —The ferns of the families Ma-
toniaceae, Gleicheniaceae, Dicksoniaceae, and Osmundaceae
were relatively abundant during the Early Cretaceous (Vakhra-
meev, 1991; Coiffard & al., 2007). At the mid Early Cretaceous
the proportion of Osmundaceae and Matoniaceae decreased,
whereas the proportion of Dicksoniaceae and Polypodiales
rose towards the Albian. This replacement has been associated
with the radiation of angiosperms and niches becoming avail-
able for opportunistic fern taxa (Schneider & al., 2004; Coif-
fard & al., 2007). The absence of fertile material in both El
Montsec and Las Hoyas makes the assignment of this fern to
either group impossible. Dilcher & Hill (2003), place this spe-
cies close to Ceratopteris Brongn. or Eriosorus Fée, both in
Pteridaceae, and they also mention similarities with Marsilea-
ceae and Salviniaceae. Both El Montsec and Las Hoyas have
a fern taxa assemblage, which, in general, presents a typical Ju-
rassic to earliest Cretaceous structure. However, the presence
of Coniopteris laciniata, if related to Polypodiales as it has
been recently suggested for other Coniopteris species preserv-
ing fertile structures (Li & al., 2020), could indicate a more
modern fern assemblage in these localities, where early angio-
sperms have also been recovered, i.e., Montsechia vidalii (Zeil-
ler) C.Teixeira (Gomez & al., 2015), Ranunculus ferreri
(C.Teixeira) Blanc-Louvel (Barale & al., 1984), and Iterophyl-
lum lobatum Barral & al. at Las Hoyas (Barral & al., 2013).
This would support the diversification of Polypodiales during
the Late Cretaceous, related to the diversification of angio-
sperms as suggested by Schneider & al. (2004).
■CONCLUSION
The conspecifity of Coniopteris laciniata and Sphenop-
teris wonnacottii increases the range of distribution of the
taxon, and links it to depositional environments with alkaline
soils and presence of calm waters. The reconstruction of this
plant is made possible with the aid of the metric analyses per-
formed in this work, which permit a better understanding of
the architecture and habit of the plant. Additionally, they allow
for comparison with the architecture of other plants with lobed
and filiform pinnules. The unique morphology and variability
of the pinnules of Coniopteris laciniata sets it aside from other
species of this genus as a very well-defined species. Future
studies must be conducted to better understand the autecology
of Coniopteris laciniata as well as to corroborate the putative
assignment of this species to Polypodiales and its implications
in the evolution of the vegetation in the Early Cretaceous.
■ACKNOWLEDGMENTS
We would like to thank the following professionals for access to
specimens and collections: Antoni Lacasa and Jaume Miquel Orófor
the collection of El Montsec housed at the Institut d’Estudis Ilerdençs
(Lleida, Spain), Mercedes Llandres for the collection of Las Hoyas
housed at the Museo de Paleontología de Castilla-La Mancha, Peta
Hayes for the holotype of Sphenopteris wonnacottii (BMNH
V.41257) housed at the Palaeobotany collection at the Natural History
Museum (London, U.K.), and Dario de Francesci for the collection of
El Montsec housed at the Muséum national d’Histoire naturelle
(Paris, France), which was visited with support of a grant from the
SYNTHESYS Project (http://www.synthesys.info/), financed by the
European Community Research Infrastructure Action under the FP7 In-
tegrating Activities Program. Candela Blanco-Moreno is supported by
a Margarita Salas Postdoc CA1/RSUE/2021-00703 scholarship funded
by the Spanish Ministry of Universities and Universidad Autónoma de
Madrid. This work is part of the project PID2019-105546GB-I00 of the
Spanish Ministry of Science, Innovation and Universities.
■AUTHOR CONTRIBUTIONS
CB-M designed and performed the research, collected the data,
performed the analyses, and wrote the initial draft of the manuscript.
´
ADB collaborated in the design of the research, the interpretation,
and writing of the subsequent manuscript drafts. —CB-M, https://
orcid.org/0000-0001-6614-286X;´
ADB, https://orcid.org/0000-0003-
1598-7963
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