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On the taxonomic resolution of pollen and spore
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Mander, Luke and Punyasena, Surangi W. (2014). On the taxonomic resolution of pollen and spore records of
Earth’s vegetation. International Journal of Plant Sciences, 175(8) pp. 931–945.
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931
Int. J. Plant Sci. 175(8):931–945. 2014.
R
EVIEW
䉷 2014 by The University of Chicago. All rights reserved.
1058-5893/2014/17508-0004$15.00 DOI: 10.1086/677680
ON THE TAXONOMIC RESOLUTION OF POLLEN AND
SPORE RECORDS OF EAR TH’S VEGETATION
Luke Mander
1,
* and Surangi W. Punyasena†
*College of Life and Environmental Sciences, University of Exeter, Prince of Wales Road, Exeter, Devon EX4 4PS, United Kingdom; and
†Department of Plant Biology, University of Illinois, 505 South Goodwin Avenue, Urbana, Illinois 61801, USA
Editor: Patrick S. Herendeen
Premise of research. Pollen and spores (sporomorphs) are a valuable record of plant life and have provided
information on subjects ranging from the nature and timing of evolutionary events to the relationship between
vegetation and climate. However, sporomorphs can be morphologically similar at the species, genus, or family
level. Studies of extinct plant groups in pre-Quaternary time often include dispersed sporomorph taxa whose
parent plant is known only to the class level. Consequently, sporomorph records of vegetation suffer from
limited taxonomic resolution and typically record information about plant life at a taxonomic rank above
species.
Methodology. In this article, we review the causes of low taxonomic resolution, highlight examples where
this has hampered the study of vegetation, and discuss the strategies researchers have developed to overcome
the low taxonomic resolution of the sporomorph record. Based on this review, we offer our views on how
greater taxonomic precision might be attained in future work.
Pivotal results. Low taxonomic resolution results from a combination of several factors, including in-
adequate reference collections, the absence of sporomorphs in situ in fossilized reproductive structures, and
damage following fossilization. A primary cause is the difficulty of accurately describing the very small mor-
phological differences between species using descriptive terminology, which results in palynologists classifying
sporomorphs conservatively at the genus or family level to ensure that classifications are reproducible between
samples and between researchers.
Conclusions. In our view, the most promising approach to the problem of low taxonomic resolution is
a combination of high-resolution imaging and computational image analysis. In particular, we encourage
palynologists to explore the utility of microscopy techniques that aim to recover morphological information
from below the diffraction limit of light and to employ computational image analyses to consistently quantify
small morphological differences between species.
Keywords: palynology, paleoecology, taxonomy, vegetation history, plant evolution.
What Is Taxonomic Resolution?
Palynological research into the history of Earth’s vegetation
is underpinned by the classification of fossil sporomorphs (pol-
len and spores) into taxonomic groups (Birks and Birks 1980).
This allows researchers to investigate patterns of vegetation
diversity and composition on a variety of spatial and temporal
scales. The results of these investigations have provided val-
uable information on subjects ranging from the nature and
timing of major evolutionary events, such as the origin and
radiation of flowering plants (Heimhofer et al. 2007), to the
relationship between vegetation and climate (Jackson and Wil-
liams 2004). However, since the earliest attempts to use spo-
romorphs to reconstruct vegetation history, workers have
expressed concern about the taxonomic rank at which spo-
1
Author for correspondence; e-mail: luke.mander@gmail.com.
Manuscript received March 2014; revised manuscript received May 2014; elec-
tronically published September 19, 2014.
romorphs are classified. In his classic lecture, von Post re-
marked, “Although the pollen types enumerated can be iden-
tified generically, the species cannot be distinguished. Thus
Betula species, Alnus species, Salices etc. can unfortunately
only be treated collectively” (von Post [1916] 1967, p. 382).
The potential implications of failing to classify sporomorphs
at the species level were recognized by Cain, who commented
“Nearly all reports of pollen grains in peats and other sedi-
ments are based on generic determinations only, despite the
generally accepted fact that a knowledge of the species involved
would be advantageous in making climatic interpretations and
reconstructing vegetational history” (Cain 1940, p. 301).
These comments neatly express the concept of taxonomic
resolution in palynology, which is shown schematically in fig-
ure 1. In this example, the pollen of six plant species (fig. 1A)
has been classified on the basis of morphological criteria. The
classifications lie on a continuum from low to high taxonomic
resolution (fig. 1B). The classification with the lowest taxo-
nomic resolution in this example is based only on the coarsest
932 INTERNATIONAL JOURNAL OF PLANT SCIENCES
Fig. 1 Schematic diagram to show low and high taxonomic resolution of sporomorph (pollen and spore) classification. A, Species A (single
main stem with black opposite leaves) produces tricolpate pollen that is circular in polar view and lacks surface ornamentation. Species B (single
main stem with dark gray opposite leaves) produces tricolpate pollen that is circular in polar view and has sparse granulate surface ornamentation.
Species C (single main stem with pale gray opposite leaves) produces tricolpate pollen that is circular in polar view and has dense granulate
surface ornamentation. Species D (two dichotomously branching main stems with black terminal leaves) produces angulaperturate pollen that
is triangular in polar view and lacks surface ornamentation. Species E (two dichotomously branching main stems with dark gray terminal leaves)
produces angulaperturate pollen that is triangular in polar view and has granulate surface ornamentation. Species F (two dichotomously branching
main stems with pale gray terminal leaves) produces angulaperturate pollen that is triangular in polar view and has gemmate surface ornamentation.
Descriptive terminology for pollen grains from Punt et al. (2007). B, Continuum of taxonomic resolution shown schematically. C–E, Classification
of the pollen grains of these six species shown at low (C), intermediate (D), and high (E) taxonomic resolution. Scale bars in insets in E represent
100 nm. Thick solid lines encircling pollen grains represent morphologically delimited taxa. The pollen of species A and B is separated by the
shape of sculptural elements that are less than 100 nm in size (E). The pollen of species E and F is separated on the basis of sculptural element
size (E).
morphological features, aperture arrangement and polar out-
line, and results in the identification of two taxa, each con-
taining three species (fig. 1C). The classification with inter-
mediate taxonomic resolution incorporates an additional
character, the presence or absence of surface ornamentation,
and results in the identification of four taxa; two containing
one species and two containing two species (fig. 1D). The
classification with the highest taxonomic resolution in this ex-
ample includes subtle morphological features such as the shape
and size of sculptural elements on the pollen surface to dis-
tinguish each species (fig. 1E). The surface ornamentation of
species A and B to the left of the schematic is characterized
by individual sculptural elements that are less than 100 nm in
size (fig. 1E).
Studies of the morphology of sporomorphs contained within
flowers and reproductive structures of extant plants establish
the relationship between dispersed sporomorphs and their par-
ent plants. This allows sporomorphs found in modern sedi-
ments to be classified in terms of extant plants. For example,
an oak pollen grain found in the surface sediments of a modern
lake can be classified as a specimen of extant Quercus. Fossil
sporomorphs of Holocene age (∼12,000 yr ago to the present)
are also generally classified in terms of extant plants. In the
schematic classification shown in figure 1, the classifications
MANDER & PUNYASENA—PALYNOLOGY AND TAXONOMIC RESOLUTION 933
Fig. 2 Cladogram to highlight the difficulty of placing a fossil in
a phylogeny. The fossil is labeled 1. Apomorphies are labeled A–E. In
this example, apomorphies D and E, highlighted in gray, relate to plant
organs that were not preserved in the fossil record. Cladogram to-
pology and example based on Pirie and Doyle (2012).
could correspond to the rank of family (fig. 1C), genus (fig.
1D), and species (fig. 1E). Farther backward in time, the phy-
logenetic position of dispersed sporomorphs is often difficult
to establish, and it becomes increasingly unclear whether fossil
sporomorphs represent extant plant species, genera, or fami-
lies. This is partly because certain sporomorphs, such as the
pollen grains of seed plants, offer few characters that can be
used to place them in a phylogenetic tree and because the
flowers, fruits, and seeds of their parent plants, which contain
more phylogenetically informative characters, are relatively
rare in the fossil record (Pirie and Doyle 2012). This problem
is highlighted by an example from Pirie and Doyle (2012),
which explores the uncertain phylogenetic position of a fossil
that possesses apomorphies A and B, but in which the organs
bearing on apomorphies D and E are not preserved (fig. 2).
The fossil could represent either a stem relative in which apo-
morphies D and E had not evolved (as shown in fig. 2), a later
stem relative in which D and E had evolved, or a crown group
member lacking apomorphy C (fig. 2). Despite uncertainties
of this nature, it is thought that many Paleogene–Neogene
(∼65–2.6 Ma) sporomorphs can be classified in terms of extant
genera or families (Chaloner 1968), but this is not the case for
the sporomorphs produced by extinct lycophytes and seed-
ferns of the Carboniferous, for example (∼359–259 Ma). In
situations such as this, where sporomorphs cannot be classified
in terms of extant species, genera, or families, the relationship
between dispersed sporomorphs and their parent plants can
be established by studies of sporomorphs found in situ in fos-
silized reproductive structures (e.g., Balme 1995).
In this review, we define taxonomic resolution as the ability
to classify a sporomorph at the taxonomic rank of species. We
make the assumption that the vast majority of fossil sporo-
morphs found in sediments of Quaternary age (∼2.59 Ma to
the present day) were produced by plant species that are extant,
although there is evidence for plant species extinction (Jackson
and Weng 1999; Willis and Niklas 2004) and morphological
evolution (Birks and Birks 1980) during this period. Accord-
ingly, we acknowledge “Quaternary time,” in which our def-
inition implies that a fossil sporomorph has been classified as
an extant species (e.g., Punyasena et al. 2012). We also assume
that many fossil sporomorphs found in sediments older than
the Quaternary were produced by extinct plant species. Con-
sequently, we acknowledge “pre-Quaternary time,” in which
our definition of taxonomic resolution implies the recognition
of characters that are sufficient to classify a fossil sporomorph
as an extinct species.
Low taxonomic resolution, the classification of sporo-
morphs above the rank of species, remains a key obstacle in
both Quaternary and pre-Quaternary palynology (Birks and
Birks 2000; Jackson and Booth 2007; Mander 2011; Pun-
yasena et al. 2011, 2012; May and Lacourse 2012; Mander
et al. 2013). In this review, we aim to examine the factors that
can reduce taxonomic resolution and to appraise existing ways
in which researchers have approached the problem of low tax-
onomic resolution. We also offer our views on how greater
taxonomic precision may be attained in the future.
Factors That Reduce Taxonomic Resolution
There are several primary factors that, either singly or in
combination, prevent the classification of sporomorphs to the
species level and thus reduce the taxonomic resolution of spo-
romorph records of ancient vegetation. The most conspicuous
of these is the morphological similarity of sporomorphs among
many species within a single genus of plants and among many
genera within certain families (Jackson and Booth 2007). In
Quaternary time, the pollen of Pinus (pine) and Quercus (oak)
are examples of morphological similarity among species within
a genus (fig. 3A), and the pollen of Poaceae (grasses) is an
example of morphological similarity among genera within a
single family. Quaternary pollen diagrams typically report fluc-
tuations in the relative abundance of these three taxa through
time rather than fluctuations in the relative abundance of their
constituent species. Morphological similarity between taxa ei-
ther can result from a lack of morphological information on
which to base a classification, such as Poaceae (Wodehouse
1935; Beug 2004; Mander et al. 2013), or can occur when the
natural range of morphological variation within two or more
species overlaps considerably, such as the pollen of Palaua
(Malvaceae), a genus of plants endemic to the coastal deserts
of Chile and Peru (Schneider et al. 2009).
There are numerous similar cases of morphological similar-
ity among species of sporomorphs in pre-Quaternary time. In
these cases, a single sporomorph morphotaxon has been found
in situ in more than one taxon of fossilized reproductive struc-
ture and therefore has botanical affinities to more than one
parent plant (e.g., Mander 2011). Examples of this include
Punctatisporites, which has affinities to the Sphenophyllales
and the fern families Marratiaceae and Osmundaceae as well
as to certain progymnosperms and other Mesozoic gymno-
sperms of uncertain systematic position (Balme 1995; Traverse
2007; Mander 2011). Other examples of sporomorphs with
affinities to several higher plant taxa include the smooth trilete
spore Deltoidospora, Mesozoic bisaccate pollen of the Alis-
porites morphotype, and the smooth or scabrate “boat-
shaped” monocolpate pollen grains of the Cycadopites/Mono-
sulcites and Chasmatosporites morphotypes (Balme 1995;
Fig. 3 Pollen of four Quercus (oak) species, sampled from herbarium sheets at the Royal Botanic Gardens, Kew. These pollen grains highlight
morphological similarity among several species within a single genus. The species are Quercus englemannii (A
1
–C
1
), Quercus lobata (A
2
–C
2
),
Quercus macrocarpa (A
3
–C
3
), and Quercus virginiana (A
4
–C
4
). Specimens were imaged with bright-field (transmitted-light) microscopy (A),
confocal (reflected-light) microscopy (B), and SEM (C). A, Bright-field images show the outline of each specimen (scale bar p 10 mm), together
with two smaller insets showing the surface ornamentation at two different focal planes (scale bars p 5 mm). B, Confocal images show a
