Plant Ecol (2015) 216:1597–1609
DOI 10.1007/s11258-015-0543-z
Taxonomic, phylogenetic and functional diversities of ferns
and lycophytes along an elevational gradient depend
on taxonomic scales
Takayuki Tanaka . Toshiyuki Sato
Received: 17 August 2015 / Accepted: 14 November 2015 / Published online: 20 November 2015
Ó Springer Science+Business Media Dordrecht 2015
Abstract We evaluated the phylogenetic and func-
tional diversities of ferns and lycophytes along an
elevational gradient in central Japan and assessed the
influence of taxonomic scales on the aforementioned
diversities and support for the niche conservatism
hypothesis. Our dataset was based on herbarium spec-
imens and broad field sampling of ferns and lycophytes
integrated into 300-m intervals of elevational gradient.
Phylogenetic and functional diversities evaluated using
the standardised effect sizes of the Rao quadratic
entropy index depended on the phylogenetic scale,
particularly the inclusiveness of lycophytes. In ferns
only and polypods, phylogenetic diversity showed no
trends with elevation, and functional diversity at lower
and higher elevations showed over-dispersion and
Communicated by William E. Rogers.
Electronic supplementary material The online version of
this article (doi:10.1007/s11258-015-0543-z) contains supple-
mentary material, which is available to authorised users.
T. Tanaka (&)
Department of Mountain and Environmental Science,
Interdisciplinary Graduate School of Science and
Technology, Shinshu University, 3-1-1 Asahi, Nagano,
Matsumoto 390-8621, Japan
e-mail: tanakanaka8150@gmail.com
T. Sato
Department of Biology, Faculty of Science, Shinshu
University, 3-1-1 Asahi, Nagano, Matsumoto 390-8621,
Japan
clustering, respectively; however, those diversities of
ferns and lycophytes showed a contrasting pattern in
ferns only and polypods, although taxonomic diversity
showed similar patterns. These results suggest that
phylogenetic and functional diversities were affected by
the variable evolutionary history of included groups.
The patterns of functional diversities of ferns only and
polypods were supported by environmental filtering,
although phylogenetic diversity showed no trends. This
suggests that morphological and life-history traits
examined in the present study independently evolved
in various lineages. The decreasing pattern of the mean
family age in ferns only along an elevational gradient
supported the niche conservatism hypothesis; however,
the patterns in ferns and lycophytes and polypods did not
support this hypothesis. These results suggest that the
mean family age is susceptible to taxon-specific history
and focal taxonomic scale, although niche conservatism
may contribute to biodiversity patterns along eleva-
tional gradients.
Keywords Elevation
Ferns and lycophytes

Functional diversity
Phylogenetic diversity
Rao
quadratic entropy
Species richness
Introduction
Understanding the underlying drivers of the spatial
patterns of species diversity and community
123
1598
structure is the one of the central topics and
challenges within ecology (Gaston 2000; Kluge
and Kessler 2011). The latitudinal diversity pattern,
namely, the decreasing species richness from the
Equator towards the poles, is the most conspicuous
pattern represented in most taxa on Earth (Gaston
2000; Condamine et al. 2012). The elevational
diversity patterns can additionally provide insight
into the development of the general theory of
species diversity (Lomolino 2001) because of the
smaller spatial scales involved and independent
replication within field surveys (McCain 2007;
Sanders and Rahbek 2012). Numerous studies have
documented a hump-shaped species richness or
monotonic decreasing patterns along an elevational
gradient in many taxa and regions (Rahbek 1995,
2005). The recent meta-analyses of the patterns
within elevational species richness have enhanced
our understanding of the effect of climatic and
spatial factors on species richness along elevational
gradients (McCain 2007; Romdal and Grytnes 2007;
McCain 2010; Kessler et al. 2011). However, the
mechanisms driving biodiversity along an elevation
scale has remained unclear (Kessler et al. 2011)
because species richness implicitly assumes the
equivalence of the ecological and evolutionary
background (Swenson et al. 2012). Thus, the
informative criteria and recognition beyond simple
species richness is important to understand processes
driving the elevational diversity pattern (Kluge and
Kessler 2011; Dreiss et al. 2015).
An important approach for exploring the processes
affecting species diversity and assembly is the analysis
of phylogenetic and functional diversities within and
between communities or over varying scales (Webb
et al. 2002; Kraft et al. 2007), which contributes to the
understanding of the ecological and evolutionary
processes driving biodiversity (Webb et al. 2002;
Hoiss et al. 2012; Swenson et al. 2012). Recent
phylogenetic and functional approaches focus on two
main theories regarding the process, namely, habitat
filtering and biotic interaction (Kluge and Kessler
2011; de Bello 2012). The two processes lead to the
different prediction regarding phylogenetic and func-
tional diversities. For example, the phylogenetic
clustering and similar traits of co-occurring species
suggest that environmental filtering has acted on a
community, whereas the phylogenetic over-dispersion
and high functional diversity of co-occurring species
123
Plant Ecol (2015) 216:1597–1609
suggest that competitive exclusion has limited the
coexistence of closely related species (Dehling et al.
2014; Spasojevic et al. 2014; Dreiss et al. 2015).
However, these results depend on the spatial and
taxonomic scaling studied (Swenson et al. 2006). In
spatial scaling, phylogenetic over-dispersion is more
common within fine scales, whereas phylogenetic
clustering is more common within large scales
because of the difference in the relative importance
of biotic interactions and abiotic filtering (Cavender-
Bares et al. 2006; Swenson et al. 2006; Kraft and
Ackerly 2010; Swenson 2013). However, phyloge-
netic and functional diversities with taxonomic scaling
have received considerably less attention (Swenson,
2013; but see Cavender-Bares et al. 2006 and Swenson
et al. 2006).
In broad scales, an additional insightful hypoth-
esis using this approach to explain diversity patterns
is the niche conservatism hypothesis (Wiens 2004;
Qian et al. 2013; Qian 2014). Niche conservatism is
defined as the phylogenetic constraint of ecological
traits and difficulty of the adaptive shift to harsher
environments (Ricklefs 2006); thus, the communities
with younger and derived clades appear within a
harsh environment. According to the analysis of
phylogenetic structure in latitudinal gradients, the
regional assemblages of tree species at higher
latitudes with lower temperature tend to be more
phylogenetically clustered (Qian et al. 2013) and of
a younger family age than that of tree species at
lower latitudes (Hawkins et al. 2014; Qian 2014).
These results indicated that few groups have
recently been able to cross the adaptive barrier to
high latitudes and that these evolutionary and
ecological processes may have produced the latitu-
dinal diversity pattern, thereby supporting the niche
conservatism hypothesis (Wiens and Donoghue
2004; Wiens et al. 2010; Qian et al. 2013; Hawkins
et al. 2014; Qian 2014). Qian et al. (2014) tested
this hypothesis in an elevational gradient by exam-
ining the relationship between the elevation and
mean family age of communities; however, the
results along an elevational gradient did not support
the prediction of the niche conservatism hypothesis
and evidence for niche conservatism in elevational
plant diversity remains controversial. Thus, Qian
et al. (2014) suggested the necessity of further
studies to assess the generality of this hypothesis for
elevational biodiversity patterns.
Plant Ecol (2015) 216:1597–1609
In the present study, we assessed the taxonomic,
phylogenetic and functional diversities of ferns and
lycophytes along an elevational gradient within three
taxonomic scales to evaluate evolutionary and eco-
logical processes driving biodiversity along an eleva-
tional gradient and to test the niche conservatism
hypothesis along an elevational gradient regarding
phylogenetic diversity and mean family age. Most
studies on phylogenetic and functional diversities of
plants have focused on angiosperms, whereas ferns
and lycophytes have received little attention (but see
Kluge and Kessler 2011), although ferns and lyco-
phytes are the second largest group in vascular plants
(Schneider et al. 2004) and have developed a broad
range of morphological and physiological strategies
(Kessler et al. 2007). In central Japan, the species
richness of ferns and lycophytes show decreasing or
low-plateau patterns along elevational gradients
(Tanaka and Sato 2013, 2014); however, the evolu-
tionary and ecological processes driving these patterns
remain unclear. The aim of the present study was as
follows: (1) to evaluate the phylogenetic and func-
tional diversities of regional assemblages of ferns and
lycophytes along elevational gradients, (2) to assess
the influence of taxonomic scales on phylogenetic and
functional diversities and (3) to test the niche conser-
vatism hypothesis for elevational biodiversity.
Methods
Dataset of species and taxonomic diversities
We surveyed the flora of central Japan, Nagano
Prefecture (35.20°N–37.03°N, 137.3°E–138.7°E),
which is located in the temperate zone. The study
area covers approximately 13,000 km2, and the
elevational span of the study area ranges from 300 to
3190 m (Tanaka and Sato 2014).
To represent a plausible regional species assem-
blage of ferns and lycophytes along an elevational
gradient in this region, we integrated two types of
information of species distribution, a flora database
based on herbarium specimens (Tanaka and Sato
2014) and sampling-based dataset (Tanaka et al.
2014). We used the Nagano Flora database (Kanai
and Shimizu 2006) based on Shimizu (1997). This
database contains over 400,000 data points for vascu-
lar plants in this region, including herbarium
1599
specimens sampled until 2004 and personal observa-
tions. We extracted herbarium data for ferns and
lycophytes containing elevational records, resulting in
information for a total of 11,776 herbarium specimens.
For the sampling-based dataset, we conducted our
field surveys in 2,310 quadrats (approximately 1 ha:
100 m 9 100 m or 20 m 9 500 m based on mea-
surement by pace) from 2000 to 2011 in central Japan.
To achieve even sampling intensity in a horizontal
area, we used a topographic map of Japan (scale,
1:50,000) showing a 20 km 9 20 km section and
further divided each section into 64 equal-sized grids
of 2.5 km 9 2.5 km. In each cell, we established at
least one survey quadrat in the forest along a road.
Within this sampling, we obtained 21,132 records of
species distribution. By combining data from the two
resources, we obtained 32,908 records in total, which
comprised 253 species of ferns and lycophytes.
We divided the elevational gradient between 300
and 3100 m into 29 bands, each of which covered
100 m of elevation (for example, the 300-m eleva-
tional band was located between 300 and 399 m) and
integrated these two types of information of species
distribution into 100-m intervals of elevation. To test
the saturation of the sampling in each elevation, we
used the mean slope of the last 10 % of the individual-
based rarefaction curve as the proxy for inventory
incompleteness (Yang et al. 2013). The values of slope
close to zero indicate saturation in the sampling,
whereas those close to one indicate high levels of
incompleteness of sampling. This analysis found the
higher level of incompleteness of sampling in 100-m
intervals of elevation, and thus, we integrated the data
into 200-, 300- and 400-m intervals of elevation, with
some departure from this interval rule only in the
highest elevation (Online Resource, Appendix 1).
From the integration of 200- to 300-m intervals, the
inventory incompleteness was greatly improved,
whereas the inventory incompleteness only slightly
improved from the integration of 300- to 400-m
intervals. We therefore used the dataset of integrated
information of species distribution into 300-m inter-
vals of elevation (henceforth 300 m elevation means
the elevational band located between 300 and 599 m)
and converted to incident data. The rarefaction curves
were computed with Estimate S9 (Colwell 2013).
To investigate the effect of taxonomic scale on
phylogenetic and functional diversities, we performed
phylogenetic and functional analyses in three different
123
1600
taxonomic scales: (1) ferns and lycophytes, (2) ferns
only and (3) polypods. Ferns and lycophytes were
traditionally lumped as ‘pteridophytes’ because of
spore bearing, uniting the paraphyletic assemblages of
plants (Mehltreter et al. 2010). Within vascular plants,
the deep split, estimated to have occurred 400 million
years ago, separated lycophytes from the euphyllo-
phytes containing seed plants and ferns (Kenrick and
Crane 1997; Wikström and Kenrick 2001). Ferns are
monophyletic if excluding lycophytes from pterido-
phytes and are composed of nine orders in central
Japan. Polypods are the most divergent group in ferns
diversified in the Cretaceous (Schneider et al. 2004)
and are composed of one order, Polypodiales.
Phylogeny of ferns and lycophytes
We explored a phylogenetic tree using rbcL sequences
(1205 base pairs) of the DNA barcoding data (Ebihara
et al. 2010) and reconstructed a Bayesian phylogenetic
tree with the estimates of divergence time using
BEAST v. 1.8.0 (Drummond and Rambaut 2007). We
manually aligned this rbcL dataset in ClustalW
(Thompson et al. 1994) and identified the best-fit
models of nucleotide substitution, GTR ? I ? C
substitution model, using Kakusan 4 (Tanabe 2011).
We employed a relaxed lognormal clock, death–birth
speciation process and calibration of fossil age con-
straints with a lognormal distribution obtained from
Pryer et al. (2004) and Schuettpelz and Pryer (2009).
The age of the root node was assumed using an
exponential prior with a mean of 10 and minimum age
of 408 (Wikström and Kenrick 2001) as the offset.
Fossil age constraints and associated lognormal dis-
tribution parameters were arranged on Online
Resource (Appendix 2). We enforced some order-
and family-level topological constraints based on
well-supported phylogenetic relationships identified
in previous studies (Pryer et al. 2004; Schuettpelz et al.
2007; Lehtonen 2011; Rothfels et al. 2012) because
the use of the rbcL sequence alone is insufficient
(Ebihara 2011). Tree posterior distributions for each
parameter were obtained using Markov chain Monte
Carlo analysis runs for 100 million generations and
sampled every 10,000 generations. Topologies in the
first 10 % of the posterior distribution were discarded
as burn-in with resampling trees every 20,000 gener-
ations using LogCombiner v. 1.8.0 (the BEAST
123
Plant Ecol (2015) 216:1597–1609
package), and convergence was checked using Tracer
v. 1.6 (the BEAST package). We used TreeAnnotator
v. 1.8.0 (the BEAST package) to produce maximum
clade credibility trees from the post-burn-in trees. On
the basis of this phylogenetic tree, we manually
reconstructed the phylogenetic tree in three different
taxonomic scales (Fig. 1).
Trait data of ferns and lycophytes
We focused on the morphological traits of frond
length, frond thickness, frond dissection, frond dimor-
phism, rhizome type and indusium (Kessler et al.
2007; Kluge and Kessler 2007, 2011) as well as two
life-history traits, namely phenology and reproductive
type (Table 1). The morphological characteristics and
life-history traits of ferns and lycophytes were com-
piled using literature data (Iwatsuki et al. 1995;
Takamiya 1996; Shimizu 1997). Frond length was
based on the maximum length within the literature
because smaller individuals may be favoured by
collectors for a herbarium specimen (Kessler et al.
2007). In the species without a documentation of frond
length within literature (5 species), we measured the
maximum frond length using all available herbarium
specimens (at least three herbarium specimens) of 5
species deposited in the Shinshu University herbar-
ium. Unknown data in frond dissection (30 species),
phenology (three species) and reproductive type (34
species) in a total of 253 species of ferns and
lycophytes were labelled as ‘Na’ (not available)
within the analysis; however, the unknown data of
frond dissection and reproductive type biased in
lycophytes, 22/24 lycophytes species and 13/24 lyco-
phytes species were unknown, respectively. Thus, to
assess the effect of unknown data of the morphological
and life-history traits, we also analysed the functional
diversity mentioned below without frond dissection
and reproductive type.
Analysis of taxonomic, phylogenetic
and functional diversities
In each taxonomic scale, we estimated the taxonomic
diversity based on species richness using the method
of linked individual-based rarefaction and extrapola-
tion curves (Colwell et al. 2012) with Estimate S9
(Colwell 2013) to adjust for the differences in the
numbers of herbarium specimens. The linked
Plant Ecol (2015) 216:1597–1609
Fig. 1 A time-calibrated
phylogeny of ferns and
lycophytes in central Japan
over three taxonomic scales.
Orders of ferns and
lycophytes abbreviations:
Lyc Lycophytes; Oph
Ophioglossales; Equ
Equisetales; Osm
Osmundales; Gle
Gleicheniales; Hym
Hymenophyllales; Sch
Schizaeales; Sal Salviniales;
Cya Cyatheales; Pol
Polypodiales
rarefaction and extrapolation curves do not discard
data for larger samples, in contrast to the previous
rarefaction method that required an adjustment of the
sample size to that of the smallest reference when
rarefied species richness was compared. We estimated
taxonomic diversity using the linked rarefaction and
extrapolation curves up to a sample size of the
elevation with the maximum individuals.
To evaluate the phylogenetic and functional diver-
sities along the elevational gradient, we used the Rao
quadratic entropy index of diversity (RaoQ) (Rao
1982; Botta-Dukát 2005) in each elevation (Dainese
et al. 2015; Dreiss et al. 2015). To determine if the
phylogenetic and functional diversities differed from
randomness, we calculated standardised effect sizes
(SES) to compare the observed value of the RaoQ
index of phylogenetic and functional diversities rela-
tive to that of the null assemblage, which is defined as
SES.RaoQ = (observed value of RaoQ - mean value
of RaoQ of null assemblage)/standard deviation of
null assemblage in phylogenetic and functional diver-
sities. The null model was generated by the randomi-
sation of the species-elevation matrix by maintaining
not only the number of species in the elevation but also
the frequency of species occurrence across elevations
1601
using the independent swap algorithm (Gotelli and
Entsminger 2001). We evaluated the relationship
between phylogenetic/functional diversity and eleva-
tion using linear and second-order polynomial regres-
sion analysis.
To test the relationship between clade age and
elevation, we used the family age, as in Qian (2014)
and Hawkins et al. (2014) within three different
taxonomic scales. The family age of ferns and
lycophytes were obtained from the previous works
of divergence time in lycophytes (Wikström and
Kenrick 2001) and ferns (Pryer et al. 2004; Schuett-
pelz and Pryer 2009). Only one family with one
species, namely Rhachidosoraceae, was excluded
from the analysis because of no data available from
previous works. We calculated the mean family age
(MFA) for each elevation as the sum of the family ages
of species divided by the number of species in an
elevation (Qian 2014). We evaluated the relationship
between MFA and elevation using linear regression
analysis and Spearman’s rank correlation.
For all statistical analyses, we used R ver 3.1.2 (R
Development Core Team 2009) and the packages
Picante (Kembel et al. 2010) and FD (Laliberté and
Shipley 2014).
123
1602 Plant Ecol (2015) 216:1597–1609

Table 1 Morphological Trait Trait values Class

and life-history traits of
ferns and lycophytes in the Morphological
present study
Frond length Maximum length of herbarium specimen Continuous
and literature
Frond thickness Thin (membranaceous to thin herbaceous) 1
Medium (herbaceous to paper-like) 2
Thick (thick paper-line to very leathery) 3
Frond dissection Unknown Na
Entire 0
Once-pinnate (to once-pinnate-pinnatifid) 1
Twice-pinnate 2
More-pinnate 3
Frond dimorphism Monomorphic 1
Slightly dimorphic 2
Dimorphic (including heterophyllous) 3
Rhizome type Upright to short-creeping 1
Creeping 2
Indusium Absent 0
Present 1
Life history
Phenology Unknown Na
Evergreen E (Categorical)
Summergreen S (Categorical)
Wintergreen W (Categorical)
Reproductive type Unknown Na
Focal traits and category of Sexual S (Categorical)
trait values were inferred to Apogamous A (Categorical)
a previous work by Kluge (including Apogamous ? Sexual)
and Kessler (2011)

Results occurred at lower elevations. All the values of the

The patterns of phylogenetic and functional diversities
along elevational gradients varied among different
taxonomic scales, although the taxonomic diversities
along elevational gradients showed similar decreasing
patterns (Fig. 2). In ferns and lycophytes, the phylo-
genetic SES.RaoQ showed a monotonic increasing
pattern (Fig. 3). The phylogenetic SES.RaoQs over
2500 m in elevation were significantly higher than
would be expected by random chance (over-disper-
sion) and those of 300 and 900 m elevations were
significantly lower than would be expected by random
chance (clustering). In ferns only and polypods, the
phylogenetic SES.RaoQ showed no trends along
elevational gradients; however, the highest values
phylogenetic SES.RaoQs along the elevational gradi-
ents fitted within the range of values expected under
the null model.
The functional SES.RaoQ in ferns and lycophytes
showed a bowl-shaped pattern with the highest values
within the 2700 m elevation, which was significantly
higher than would be expected by random chance (over-
dispersion) (Fig. 4). The functional SES.RaoQ in ferns
and lycophytes without frond dissection and reproduc-
tive type showed a monotonic increasing pattern (Online
Resource, Appendix 3). Although the trend lines of
functional SES.RaoQ in ferns and lycophytes showed
different patterns between with frond dissection and
reproductive type and without these traits, each value of
the functional SES.RaoQ within the 2700 m elevation

123
Plant Ecol (2015) 216:1597–1609
b Fig. 2 Taxonomic diversity based on species richness in a ferns
was significantly higher than would be expected by
random chance (over-dispersion). Thus, we discussed
the results of the functional SES.RaoQ in ferns and
1603
and lycophytes, b ferns only and c polypods, estimated using the
method of linked individual-based rarefaction and extrapolation
curves up to a sample size of the elevation with maximum
individuals. The error bars represent 95 % unconditional
confidence intervals for estimated species richness. Trend lines
were fitted using linear and second-order polynomial regression
analysis with statistical significance at the P \ 0.05 level
lycophytes focused on the over-dispersion within the
2700 m elevation. The functional SES.RaoQ in ferns
only and polypods showed the bowl-shaped patterns
with the highest values at 300 m elevation. The
functional SES.RaoQ in the 300 m elevation was
significantly higher than would be expected by random
chance (over-dispersion) and that at 1500 and 1800 m
elevations in ferns only as well as at 1800 m in polypods
was significantly lower than would be expected by
random chance (clustering).
The patterns of MFA along elevation varied among
taxonomic scales (Fig. 5). In ferns and lycophytes,
MFA increased towards high elevation (r = 0.933,
P \ 0.001 in Spearman’s rank correlation); however,
MFA in ferns only decreased towards high elevation
(r = - 0.717, P \ 0.05 in Spearman’s rank correla-
tion). In polypods, MFA showed no trend along
elevational gradients (r = 0.133, N.S in Spearman’s
rank correlation).
Discussion
We found different patterns of phylogenetic and
functional diversities along elevational gradients
among taxonomic scales. In the broadest taxonomic
scale, namely ferns and lycophytes, the results of
phylogenetic and functional diversities showed a
contrasting pattern to ferns only and polypods. This
result suggested that the interpretation of evolutionary
and ecological processes for biodiversity along eleva-
tional gradients was influenced by the broadness of the
included taxonomic scale. The previous studies in
tropical forests and north central Florida suggested the
dependence of phylogenetic scale or the inclusiveness
of taxa on phylogenetic structure, where communities
defined on a finer taxonomic scale showed more
phylogenetic over-dispersion, whereas those defined
on a broad taxonomic scale showed more clustering
(Cavender-Bares et al. 2006; Swenson et al. 2006). In
123
1604
Fig. 3 Elevational pattern of SES.RaoQ and observed RaoQ in
phylogenetic diversity of a, b ferns and lycophytes, c, d ferns
only and e, f polypods. In SES.RaoQ, trend lines were fitted
using linear and second-order polynomial regression analysis
with statistical significance at the P \ 0.05 level. In observed
RaoQ, black circles indicate the value of RaoQ in observed
the present study, the pattern of phylogenetic and
functional diversities along elevation differed because
of the inclusiveness of lycophytes. Lycophytes have a
123
Plant Ecol (2015) 216:1597–1609
species assemblages, and grey circles indicate the mean value of
RaoQ in the null assemblage. The dotted lines and asterisk
indicate the 95 % confidence interval of values obtained in the
null assemblage and significant clustering or over-dispersion
that deviated from the 95 % confidence interval, respectively
long history and first appeared in the Paleozoic
(Wikström and Kenrick 2001) and phylogenetically
differ from ferns (paraphyly). In addition,
Plant Ecol (2015) 216:1597–1609
Fig. 4 Elevational pattern of SES.RaoQ and observed RaoQ in
functional diversity of a, b ferns and lycophytes, c, d ferns only
and e, f polypods. In SES.RaoQ, trend lines were fitted using
linear and second-order polynomial regression analysis with
statistical significance at the P \ 0.05 level. In observed RaoQ,
black circles indicate the value of RaoQ in observed species
assemblages, and grey circles indicate the mean value of RaoQ
Lycopodiaceae, the main family of lycophytes, are
almost all cosmopolitan in distribution (Xiang et al.
2015). In contrast to ferns taxonomic diversity,
1605
in the null assemblage. The dotted lines indicate the 95 %
confidence interval of values obtained in the null assemblage.
The dotted lines and asterisk indicate the 95 % confidence
interval of values obtained in the null assemblage and significant
clustering or over-dispersion that deviated from the 95 %
confidence interval, respectively
lycophytes taxonomic diversity showed a hump-
shaped pattern with mid-elevational peaks, and the
proportion of lycophytes increased towards high
123
1606
Fig. 5 Mean family age (MFA) along elevational gradient in
a ferns and lycophytes, b ferns only and c polypods. Trend lines
were fitted by linear regression analysis with statistical
significance at the P \ 0.05 level
123
Plant Ecol (2015) 216:1597–1609
elevations (Online Resource, Appendix 4), which
resulted in a large amount of phylogenetic distance
among co-occurring ferns species. In addition, the leaf
morphological traits of lycophytes considerably differ
from those of ferns. For example, at high elevation,
lycophytes have evergreen, hard, needle-like or acic-
ular-lanceolate trophophylls similar to a conifer. In
contrast, ferns occurring at higher elevations have
summergreen and not hard leaves. Thus, it is more
reasonable that the cause of the over-dispersion of
phylogenetic and functional diversities at higher
elevations in ferns and lycophytes is because of the
extreme difference of evolutionary history or strategic
differences between lycophytes and ferns rather than
the conclusions of the influence of biotic interaction
(Ghosh-Harihar 2014) and convergence (Culmsee and
Leuschner 2013) arrived at by previous studies that
identified phylogenetic dispersion at high elevation. In
support of the aforementioned assertion of the present
study, phylogenetic and functional diversities did not
show over-dispersion at high elevations only for ferns
or polypods. These results suggested that phylogenetic
and functional diversities along elevational gradients
were considerably affected by the variable evolution-
ary history of included groups (ferns and lycophytes in
the present study). In addition, taxonomic diversity
showed similar patterns among the included taxo-
nomic scales, although the patterns of phylogenetic
and functional diversities differed. This suggested that
the taxonomic diversity index masked the evidence for
understanding evolutionary and ecological process
driving biodiversity and for facilitating conservation
and management (Dreiss et al. 2015) because the
features of the majority group (ferns in the current
study) masked those of the minority group (lycophytes
in the current study). Thus, the present study con-
firmed that evaluating taxonomic diversity alone is
insufficient for understanding any aspects of
biodiversity.
In ferns and polypods, functional diversities at low
and middle/high elevations exhibited higher (over-
dispersion) and lower (clustered) values, respectively,
than the null model, which corresponded to patterns
along the elevational gradient of previous studies in
any taxon (Graham et al. 2009; Machac et al. 2011;
Dehling et al. 2014; Qian et al. 2014; Dreiss et al.
2015). In central Japan, forest vegetation changes
from evergreen broad-leaved to deciduous broad-
Plant Ecol (2015) 216:1597–1609
leaved trees at approximately 800 m in elevation
because of temperature limitation (Ohsawa 1990,
1995). At around this threshold, functional SES.-
RaoQs in ferns only and polypods changed from
positive to negative values, suggesting that different
mechanisms contribute to ferns only and polypods
assemblages along elevational gradients (Dreiss et al.
2015). The pattern of functional diversity, dispersion
in moderate environments at lower elevations and
clustering in harsh environments at higher elevations,
was supported by environmental filtering, and niche
conservatism hypothesis supported these patterns
considering the decreasing of MFA along elevation
(derivative ferns occurred at high elevation). How-
ever, the trends of phylogenetic diversity in ferns only
and polypods were not statistically significant along
elevational gradients. This random pattern of phylo-
genetic diversity indicated that morphological and
life-history traits evident in the present study inde-
pendently evolved in various lineages (Kluge and
Kessler 2011).
Like the result of Qian (2014), MFA increased
along elevational gradients in ferns and lycophytes,
which did not support the niche conservatism hypoth-
esis. This may be because the proportion of lycophyte
species with considerably old family age increased
towards high elevations, as mentioned above. Qian
(2014) discussed a similar point in angiosperms that
many species at high elevations may belong to old
Gondwanan clades adapted to cold temperatures.
These results implied that the mean family age along
elevational gradient is susceptible to taxon-specific
history. In addition, MFA in ferns only decreased
along elevational gradients, suggesting that the fern
species occurring at higher elevations are composed of
relatively younger families and supported the niche
conservatism hypothesis; however, MFA in polypods
showed no trend, which does not support this hypoth-
esis. These results additionally suggest that the mean
family age along elevation is susceptible to not only
taxon-specific history but also focused taxonomic
scale, although niche conservatism may contribute to
biodiversity patterns along elevational gradients.
In summary, the inclusion of taxon affected the
phylogenetic and functional diversities of ferns and
lycophytes along elevational gradients. This suggests
that the depth of evolutionary history contributed to
these diversity patterns. In particular, the deeper
taxonomic split between ferns and lycophytes
1607
emphasised the differences in patterns of phylogenetic
and functional diversities. In turn, species richness as
taxonomic diversity showed a similar trend, although
phylogenetic and functional diversity indices showed
different patterns. Thus, taxonomic diversity masked
the ecological and evolutionary background of focal
taxon and was incomplete for understanding any
aspects of biodiversity.
Acknowledgments We greatly appreciate many local
botanists and the botanical society of Nagano for contributing
to the Nagano Flora Database. We would like to thank Enago
(www.enago.jp) for English language review. We are very
grateful to the handling editor and anonymous reviewer for their
valuable comments on the manuscript. Financial support was
provided by Research Fellow of Japan Society for the Promotion
of Science.
References
Botta-Dukát Z (2005) Rao’s quadratic entropy as a measure of
functional diversity based on multiple traits. J Veg Sci
16:533–540
Cavender-Bares J, Keen A, Miles B (2006) Phylogenetic
structure of Floridian plant communities depends on tax-
onomic and spatial scale. Ecology 87:S109–S122
Colwell R (2013) Estimate S: statistical estimation of species
richness and shared species from samples. Version 9 and
earlier. User’s Guide and application
Colwell RK, Chao A, Gotelli NJ, Lin S-Y, Mao CX, Chazdon
RL, Longino JT (2012) Models and estimators linking
individual-based and sample-based rarefaction, extrapola-
tion and comparison of assemblages. J Plant Ecol 5:3–21
Condamine FL, Sperling FA, Wahlberg N, Rasplus JY, Kergoat
GJ (2012) What causes latitudinal gradients in species
diversity? Evolutionary processes and ecological con-
straints on swallowtail biodiversity. Ecol Lett 15:267–277
Culmsee H, Leuschner C (2013) Consistent patterns of eleva-
tional change in tree taxonomic and phylogenetic diversity
across Malesian mountain forests. J Biogeogr 40:1997–
2010
Dainese M, Lepš J, de Bello F (2015) Different effects of ele-
vation, habitat fragmentation and grazing management on
the functional, phylogenetic and taxonomic structure of
mountain grasslands. Perspect Plant Ecol Evol Syst
17:44–53
de Bello F (2012) The quest for trait convergence and diver-
gence in community assembly: are null-models the magic
wand? Global Ecol Biogeogr 21:312–317
Dehling DM, Fritz SA, Töpfer T, Päckert M, Estler P, Böhning-
Gaese K, Schleuning M (2014) Functional and phyloge-
netic diversity and assemblage structure of frugivorous
birds along an elevational gradient in the tropical Andes.
Ecography 37:1047–1055
Dreiss LM, Burgio KR, Cisneros LM, Klingbeil BT, Patterson
BD, Presley SJ, Willig MR (2015) Taxonomic, functional,
123
1608
and phylogenetic dimensions of rodent biodiversity along
an extensive tropical elevational gradient. Ecography.
doi:10.1111/ecog.00971
Drummond AJ, Rambaut A (2007) BEAST: Bayesian evolu-
tionary analysis by sampling trees. BMC Evol Biol 7:214
Ebihara A (2011) RbcL phylogeny of Japanese pteridophyte
flora and implications on infrafamilial systematics. Bull
Natl Mus Nat Sci Ser B 37:63–74
Ebihara A, Nitta JH, Ito M (2010) Molecular species identifi-
cation with rich floristic sampling: DNA barcoding the
pteridophyte flora of Japan. PLoS ONE 5:e15136
Gaston KJ (2000) Global patterns in biodiversity. Nature
405:220–227
Ghosh-Harihar M (2014) Phylogenetic and ecomorphological
structure of assemblages of breeding leaf warblers (Phyl-
loscopidae) along Himalayan elevational gradients. J Bio-
geogr 41:1193–1203
Gotelli NJ, Entsminger GL (2001) Swap and fill algorithms in
null model analysis: rethinking the knight’s tour. Oecolo-
gia 129:281–291
Graham CH, Parra JL, Rahbek C, McGuire JA (2009) Phylo-
genetic structure in tropical hummingbird communities.
PNAS 106:19673–19678
Hawkins BA, Rueda M, Rangel TF, Field R, Diniz-Filho JAF
(2014) Community phylogenetics at the biogeographical
scale: cold tolerance, niche conservatism and the structure
of North American forests. J Biogeogr 41:23–38
Hoiss B, Krauss J, Potts SG, Roberts S, Steffan-Dewenter I
(2012) Altitude acts as an environmental filter on phylo-
genetic composition, traits and diversity in bee communi-
ties. Proc R Soc B 279:4447–4456
Iwatsuki K, Yamazaki T, Boufford D, Ohba H (1995) Flora of Japan
vol. I. Pteridophyta and Gymnospermae. Kodansha, Tokyo
Kanai H, Shimizu T (2006) CD-ROM Flora of Nagano Pre-
fecture, popular edition. A medium to publish a volumi-
nous data set. J Jpn Bot 81:54–62
Kembel SW, Cowan PD, Helmus MR, Cornwell WK, Morlon H,
Ackerly DD, Blomberg SP, Webb CO (2010) Picante: R
tools for integrating phylogenies and ecology. Bioinfor-
matics 26:1463–1464
Kenrick P, Crane PR (1997) The origin and early evolution of
plants on land. Nature 389:33–39
Kessler M, Siorak Y, Wunderlich M, Wegner C (2007) Patterns
of morphological leaf traits among pteridophytes along
humidity and temperature gradients in the Bolivian Andes.
Funct Plant Biol 34:963–971
Kessler M, Kluge J, Hemp A, Ohlemüller R (2011) A global
comparative analysis of elevational species richness pat-
terns of ferns. Global Ecol Biogeogr 20:868–880
Kluge J, Kessler M (2007) Morphological characteristics of fern
assemblages along an elevational gradient: patterns and
causes. Ecotropica 13:27–43
Kluge J, Kessler M (2011) Phylogenetic diversity, trait diversity
and niches: species assembly of ferns along a tropical
elevational gradient. J Biogeogr 38:394–405
Kraft NJ, Ackerly DD (2010) Functional trait and phylogenetic
tests of community assembly across spatial scales in an
Amazonian forest. Ecol Monogr 80:401–422
Kraft NJ, Cornwell WK, Webb CO, Ackerly DD (2007) Trait
evolution, community assembly, and the phylogenetic
structure of ecological communities. Am Nat 170:271–283
123
Plant Ecol (2015) 216:1597–1609
Laliberté E, Shipley B (2014) FD: measuring functional diver-
sity from multiple traits, and other tools for functional
ecology. R package version 1.0-12. Available at: http://
cran.r-project.org/web/packages/FD/FD.pdf
Lehtonen S (2011) Towards resolving the complete fern tree of
life. PLoS ONE 6:e24851
Lomolino M (2001) Elevation gradients of species-density:
historical and prospective views. Global Ecol Biogeogr
10:3–13
Machac A, Janda M, Dunn RR, Sanders NJ (2011) Elevational
gradients in phylogenetic structure of ant communities
reveal the interplay of biotic and abiotic constraints on
diversity. Ecography 34:364–371
McCain CM (2007) Could temperature and water availability
drive elevational species richness patterns? A global case
study for bats. Global Ecol Biogeogr 16:1–13
McCain CM (2010) Global analysis of reptile elevational
diversity. Global Ecol Biogeogr 19:541–553
Mehltreter K, Walker LR, Sharpe JM (2010) Fern ecology.
Cambridge University Press, Cambridge
Ohsawa M (1990) An interpretation of latitudinal patterns of
forest limits in south and east Asian mountains. J Ecol
78:326–339
Ohsawa M (1995) Latitudinal comparison of altitudinal changes
in forest structure, leaf-type, and species richness in humid
monsoon Asia. Vegetatio 121:3–10
Pryer KM, Schuettpelz E, Wolf PG, Schneider H, Smith AR,
Cranfill R (2004) Phylogeny and evolution of ferns
(monilophytes) with a focus on the early leptosporangiate
divergences. Am J Bot 91:1582–1598
Qian H (2014) Contrasting relationships between clade age and
temperature along latitudinal versus elevational gradients
for woody angiosperms in forests of South America. J Veg
Sci 25:1208–1215
Qian H, Zhang Y, Zhang J, Wang X (2013) Latitudinal gradients
in phylogenetic relatedness of angiosperm trees in North
America. Global Ecol Biogeogr 22:1183–1191
Qian H, Hao Z, Zhang J (2014) Phylogenetic structure and
phylogenetic diversity of angiosperm assemblages in for-
ests along an elevational gradient in Changbaishan, China.
J Plant Ecol 7:154–165
R Development Core Team (2009) R: a language and environ-
ment for statistical computing. R Foundation for Statistical
Computing, Vienna, Austria. http://www.R-project.org
Rahbek C (1995) The elevational gradient of species richness: a
uniform pattern? Ecography 18:200–205
Rahbek C (2005) The role of spatial scale and the perception of
large-scale species-richness patterns. Ecol Lett 8:224–239
Rao CR (1982) Diversity and dissimilarity coefficients: a unified
approach. Theor Popul Biol 21:24–43
Ricklefs RE (2006) Evolutionary diversification and the origin
of the diversity–environment relationship. Ecology 87:S3–
S13
Romdal TS, Grytnes JA (2007) An indirect area effect on ele-
vational species richness patterns. Ecography 30:440–448
Rothfels CJ, Sundue MA, Kuo L-Y, Larsson A, Kato M,
Schuettpelz E, Pryer KM (2012) A revised family-level
classification for eupolypod II ferns (Polypodiidae: Poly-
podiales). Taxon 61:515–533
Sanders NJ, Rahbek C (2012) The patterns and causes of ele-
vational diversity gradients. Ecography 35:1–3
Plant Ecol (2015) 216:1597–1609
Schneider H, Schuettpelz E, Pryer KM, Cranfill R, Magallón S,
Lupia R (2004) Ferns diversified in the shadow of
angiosperms. Nature 428:553–557
Schuettpelz E, Pryer KM (2009) Evidence for a Cenozoic
radiation of ferns in an angiosperm-dominated canopy.
PNAS 106:11200–11205
Schuettpelz E, Schneider H, Huiet L, Windham MD, Pryer KM
(2007) A molecular phylogeny of the fern family Pteri-
daceae: assessing overall relationships and the affinities of
previously unsampled genera. Mol Phylogenet Evol
44:1172–1185
Shimizu T (1997) Flora of Nagano Prefecture (in Japanese).
Shinano Mainichi Shimbun, Nagano
Spasojevic MJ, Grace JB, Harrison S, Damschen EI (2014)
Functional diversity supports the physiological tolerance
hypothesis for plant species richness along climatic gra-
dients. J Ecol 102:447–455
Swenson NG (2013) The assembly of tropical tree communi-
ties–the advances and shortcomings of phylogenetic and
functional trait analyses. Ecography 36:264–276
Swenson NG, Enquist BJ, Pither J, Thompson J, Zimmerman JK
(2006) The problem and promise of scale dependency in
community phylogenetics. Ecology 87:2418–2424
Swenson NG, Erickson DL, Mi X, Bourg NA, Forero-Montaña
J, Ge X, Howe R, Lake JK, Liu X, Ma K (2012) Phylo-
genetic and functional alpha and beta diversity in temper-
ate and tropical tree communities. Ecology 93:S112–S125
Takamiya M (1996) Index to chromosomes of Japanese Pteri-
dophyta. Nippon Print Center, Tokyo
Tanabe AS (2011) Kakusan4 and Aminosan: two programs for
comparing nonpartitioned, proportional and separate
models for combined molecular phylogenetic analyses of
multilocus sequence data. Mol Ecol Resour 11:914–921
Tanaka T, Sato T (2013) Elevational patterns of fern species
assemblages and richness in central Japan. Plant Ecol
214:1189–1197
1609
Tanaka T, Sato T (2014) Species richness of seed plants and
ferns along a temperate elevational gradient in central
Japan. Plant Ecol 215:1299–1311
Tanaka T, Isaka Y, Hattori M, Sato T (2014) Ecological and
phylogenetic approaches for diversification of apogamous
ferns in Japan. Plant Syst Evol 300:2041–2050
Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W:
improving the sensitivity of progressive multiple sequence
alignment through sequence weighting, position-specific
gap penalties and weight matrix choice. Nucleic Acids Res
22:4673–4680
Webb CO, Ackerly DD, McPeek MA, Donoghue MJ (2002)
Phylogenies and community ecology. Annu Rev Ecol Syst
33:475–505
Wiens JJ (2004) Speciation and ecology revisited: phylogenetic
niche conservatism and the origin of species. Evolution
58:193–197
Wiens JJ, Donoghue MJ (2004) Historical biogeography, ecol-
ogy and species richness. Trends Ecol Evol 19:639–644
Wiens JJ, Ackerly DD, Allen AP, Anacker BL, Buckley LB,
Cornell HV, Damschen EI, Jonathan Davies T, Grytnes JA,
Harrison SP (2010) Niche conservatism as an emerging
principle in ecology and conservation biology. Ecol Lett
13:1310–1324
Wikström N, Kenrick P (2001) Evolution of Lycopodiaceae
(Lycopsida): estimating divergence times from rbcL gene
sequences by use of nonparametric rate smoothing. Mol
Phylogen Evol 19:177–186
Xiang JY, Wen J, Peng H (2015) Evolution of the eastern Asian-
North American biogeographic disjunctions in ferns and
lycophytes. J Syst Evol 53:2–32
Yang W, Ma K, Kreft H (2013) Geographical sampling bias in a
large distributional database and its effects on species
richness—environment models. J Biogeogr 40:1415–1426
123