Journal of Biogeography (J. Biogeogr.

) (2011) 38, 394–405

ORIGINAL Phylogenetic diversity, trait diversity and

ARTICLE
niches: species assembly of ferns along a
tropical elevational gradient
Jürgen Kluge1,2* and Michael Kessler1

1
Systematic Botany, University of Zurich,
Zollikerstrasse 107, CH-8008 Zurich,
Switzerland, 2Faculty of Geography, University
of Marburg, Deutschhausstrasse 10, D-35032
Marburg, Germany
*Correspondence: Jürgen Kluge, Faculty of
Geography, University of Marburg,
Deutschhausstrasse 10, D-35032 Marburg,
Germany.
E-mail: klugejuergen@gmx.de
ABSTRACT
Aim To analyse the structure of pteridophyte assemblages, based on phylogenetic
relatedness and trait properties, along an elevational gradient. Ecological theory
predicts that co-occurring species may be: randomly selected from a regional
pool; ecologically sorted so that they are functionally different hence resulting in
reduced competition (overdispersion); or functionally similar as an adaptation to
specific ecological conditions (clustering).
Location Braulio Carrillo National Park and Cerro de la Muerte, Costa Rica,
Central America.
Methods We used an empirical dataset of the quantitative pattern of species
occurrences and individual numbers of ferns within 156 plots along a tropical
elevational gradient to test whether directed ecological sorting might cause
deviations in patterns of trait and phylogenetic diversity. Mean pairwise distances
of species based on phylogenetic and trait properties were compared with two
different sets of null assemblages, one maintaining species frequency distributions
(constrained) and one not (unconstrained).
Results Applying different null models resulted in varying degrees of
overdispersion and clustering, but overall patterns of deviation from random
expectations remained the same. Contrary to theoretical predictions, phylogenetic
and trait diversity were relatively independent from one another. Phylogenetic
diversity showed no patterns along the elevational gradient, whereas trait diversity
showed significant trends for epiphytes.
Main conclusions Under stressful environmental conditions (drought at low
elevations and frost at high elevations), epiphytic fern assemblages tended to be
clustered with respect to trait characteristics, which suggests environmental
filtering. Conversely, under less extreme environmental conditions (middle of the
transect), the sorting was biased towards high differentiation (overdispersion),
presumably because of interspecific competition and trait shifts among closely
related species (character displacement).
Keywords
Adaptation, Costa Rica, environmental filtering, ferns, niche, phylogenetic
diversity, species assemblage, trait diversity, tropical forest.

and composition brought about by global change (Fargione

INTRODUCTION
Understanding how the diversity of ecological communities
has evolved and how this diversity influences ecosystem
functionality is one of the central topics of ecological research,
especially with regard to the changes in assemblage diversity
et al., 2007). Biological diversity includes a wide range of
attributes, ranging from genetic diversity within populations to
ecosystem diversity on a global scale (Magurran, 1988).
Because species are the most readily sampled entities, the vast
majority of studies on the diversity and structure of species

394 www.blackwellpublishing.com/jbi ª 2010 Blackwell Publishing Ltd

doi:10.1111/j.1365-2699.2010.02433.x

assemblages have used species as focal units (Lomolino et al.,
2006). However, understanding processes that generate vari-
ation in diversity requires criteria to measure diversity that go
beyond simple species richness. As newly evolved taxa tend to
be ecologically similar (Wiens & Graham, 2005), there may be
a link between the phylogenetic relatedness of species within an
assemblage, traits of these species, and the ecological processes
that determine their co-occurrence (Kraft et al., 2007). Along
this line of thought, species assemblages may show non-
random patterns of species co-occurrences (reviewed by Webb
et al., 2002), and the degree of relatedness between co-
occurring species in terms of phylogenetic and trait similarity
may shed light on prevailing ecological processes such as
environmental filtering (Weiher & Keddy, 1995) and niche
differentiation (Stubbs & Wilson, 2004).
As species usually differ from each other with respect to
their position in the phylogenetic tree, as well as in their
morphological and thus functional characters, the range of
species properties tends to increase with species richness
(Janzen, 1985; Sax et al., 2007) (Fig. 1). This relationship is not
linear but asymptotic because, as new species are added to an
assemblage, the probability of their carrying new characteris-
tics declines as the number of species increases. The shape of
this asymptotic curve might be modified by two contrasting
processes (Weiher & Keddy, 1995).
First, the probability of a species persisting may increase if
it is distinct from other species in an assemblage. This will
result in a more efficient exploitation of the available
resources, which in turn will reduce competitive interactions
(MacArthur, 1958; Diáz & Cabido, 1997; Fridley, 2001;
Hooper et al., 2005). Under such a regime, competition
should favour species with different characters and thus from
different lineages, resulting in a level of diversity above that
of randomly selected assemblages with the same species
Figure 1 Theoretical curves showing the hypothetical relation-
ships between local species richness and trait diversity. The con-
tinuous line shows random sorting from a regional pool; the upper
dashed line represents a sorting towards higher niche differentia-
tion and reduced competition, the lower dashed line a sorting
towards adaptation and convergence.
Journal of Biogeography 38, 394–405
ª 2010 Blackwell Publishing Ltd
Phylogenetic and trait diversity of ferns
number, a pattern called ‘overdispersion’ (Moulton & Pimm,
1987) (Fig. 1).
Second, the environment may set limits on the occurrence
of species unsuited to these ambient conditions. Such
‘environmental filters’ might constrain species composition
to a restricted set of possible characteristics (Box, 1981;
Keddy, 1992; Weiher & Keddy, 1995; de Bello et al., 2006)
and admit only species that are viable under the given
environmental conditions (e.g. climate, disturbance regimes)
and biotic interactions (e.g. competitive exclusion) (Smith
et al., 1994). In this way, the diversity of characters is
limited by the local niche space (Dı́az & Cabido, 2001;
Grime, 2002; Lavorel & Garnier, 2002). This process might
thus result in trait diversity levels lower than those of
random assemblages, a pattern called ‘clustering’ (Weiher &
Keddy, 1995) (Fig. 1).
Accordingly, if there is directional ecological sorting (sensu
Ackerly, 2003), the direction itself may shed light on the
mechanism of species assembly (Fridley, 2001; Mouquet et al.,
2002). In general, both types of sorting are well supported by
both theoretical and empirical studies, but it has not yet been
explored how they affect the relationship of species richness
and phylogenetic/trait diversity along natural diversity gradi-
ents. A priori, one might expect competition to be stronger in
species-rich assemblages, and environmental filtering to be
more prevalent in species-poor assemblages under extreme
environmental conditions. Alternatively, however, species-rich
assemblages may contain a higher proportion of functionally
redundant (and hence similar) species, whereas species-poor
ones may contain distinct species exploiting different niches
(Yachi & Loreau, 2007). Thus there are various reasons to
expect that the phylogenetic/trait diversity–species richness
relationship might differ from randomness (Weiher & Keddy,
1995).
On the assumption that traits are conserved within lineages,
phylogenetic and trait diversity patterns should vary simulta-
neously. Disagreements of patterns along gradients may give
further insight into assembling processes beyond competition
and filtering (Webb et al., 2002). Species not only may be
selected into assemblages, but also may evolve while persisting
within an assemblage, thus altering phylogenetic and trait
structures in different ways (Cavender-Bares et al., 2009).
In the present study we assess the structure of fern
assemblages with respect to phylogenetic relatedness and trait
characteristics of co-occurring species using the species-
abundance distribution of ferns and lycophytes along a
tropical elevational gradient with a strong species-richness
pattern. Species richness was highest at mid-elevations, creat-
ing a symmetrical hump along the elevational gradient, as also
found at the same study site by Cardelús et al. (2006) and
Watkins et al. (2006). Because the major life forms of ferns,
terrestrials and epiphytes not only differ in their elevational
and morphological diversity patterns (Kessler, 2001; Kluge &
Kessler, 2007), but also occupy different realms within the
vegetation assemblages, we conducted our analyses separately
for each life form.
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J. Kluge and M. Kessler
MATERIALS AND METHODS
Vegetation sampling
Our analyses are based on distributional data for 477 fern species
along an elevational gradient (100–3400 m a.s.l.) with strong
associated changes in environmental conditions in undisturbed
tropical rain forest in Costa Rica, Central America. Species
assemblages were sampled within 156 plots with a regular square
shape of 20 · 20 m2. Two study sites were combined: Volcan
Barva (100–2800 m) and Cerro de la Muerte (2700–3400 m).
Although these two gradients are c. 50 km apart, previous
analysis revealed that there is no abrupt change in species
compositions between these sites (Kluge et al., 2008), so both
can be treated in combination. All species were counted
separately for terrestrials and epiphytes. For terrestrial species,
we avoided special substrates such as dead wood and stones to
minimize the possible influence of habitat heterogeneity. The
species-richness pattern is strongly hump-shaped with the
highest values at mid-elevations, reaching a maximum of 68
species per 400 m2 plot, and falling to 10 and 15 species per plot
at the upper and lower ends of the gradient, respectively (for
further details see Kluge et al., 2006).
General analysis procedure
Species-assembly patterns were assessed by plot-wide phylo-
genetic and trait relationships between the species present in
the respective assemblages. Assemblages were defined as the
species co-occurring in each study plot. This calculation is
based on distance matrices, where each pair of species present
in all assemblages found within this study (species pool) was
assigned a distance value (Euclidean) with respect to their
phylogenetic and trait similarity.
From the whole set of pairwise distances, we calculated the
mean of all pair values for those species that were members of
the respective assemblage (mean distance). To account for
abundance distributions within the assemblages and to give
lower weight to rare and possibly ‘erratic’ species, the distance
values were weighted according to the abundance of the
respective species. In this way, each assemblage was assigned a
value of its mean phylogenetic distance (MPDemp) and mean
trait distance (MTDemp), respectively. As this distance is a
measure for the phylogenetic/trait diversity of an assemblage,
MPD and MTD may also be read as ‘mean phylogenetic
diversity’ and ‘mean trait diversity’, respectively.
To assess whether such empirical assemblage patterns along
the elevational gradient of both phylogenetic and trait
relationships differed significantly from random assemblages,
we tested the empirical values against the values of 1000
randomly constructed assemblages.
Phylogenetic data
We constructed the phylogenetic tree by using data on
phylogenetic relationships provided by the Tree of Life web
396
project (http://www.tolweb.org), a regularly updated collabo-
rative effort of taxonomic specialists on the respective groups
of organisms.
For the assessment of the phylogenetic relationships among
species, several authors have suggested taking the length of the
branches of a taxonomic cladogram (e.g. Vane-Wright et al.,
1991; Faith, 1992, 1995), but unfortunately such fully resolved
cladograms are rarely available (Crozier, 1992; Izsák & Papp,
2000; Ricotta, 2005; Schweiger et al., 2008). To compensate for
the lack of such phylogenetic information, here we used the
topological distance of species within the phylogenetic tree of
the whole species pool by counting the nodes separating each
two species within an assemblage (mean pairwise distance:
Izsák & Papp, 2000; Webb, 2000; Ricotta, 2002), leading to the
distance matrix mentioned above, by using the R package
‘picante’ (Kembel et al., 2009). Note that this measure does not
consider the true length of cladogram branches, therefore this
calculation is an oversimplification.
Trait data
In the same manner, the structure of assemblages can be
analysed by replacing the phylogenetic distance matrix by a
species distance matrix based on trait properties of the species.
Morphological characteristics of the species were compiled
from the literature (Moran & Riba, 1995; Rojas, 1996, 1997,
2001a,b, 2002a,b) complemented by the study of herbarium
material. The traits, their scale of measurement, and their
presumed functional importance are listed in Table 1. Some of
these characteristics, especially indument density values and
laminar thickness, were rather subjective and variable; to avoid
a pretence to accuracy, we used an ample class division (see
further details in Kluge & Kessler, 2007). Because traits are
usually expressed on different scales, trait data needed to be
standardized to avoid traits with higher numeric values
overriding traits with lower values. We standardized the trait
values to means of 0 and a standard deviation of 1 so that all
traits had the same weight.
Null assemblages
The choice of a null model is essential for interpretation of the
comparison of empirical and randomized species assemblages
(Gotelli & Graves, 1996; Webb et al., 2002; Kembel & Hubbell,
2006; Swenson, 2009). We contrast the patterns gained from
two different null models that imply different assumptions
about the ability of species to occur at a certain site.
The first null model had fewer restrictions, and rests on the
assumption that each species is able to colonize a given plot
with equal probability. In the construction of these null
assemblages, the species were chosen randomly without
replacement from the whole species pool, so the species
richness of each plot and the total abundance of all species
across all plots were kept constant, but not the abundance of
each species in each plot. As species occurrence frequencies in
the randomized assemblages were not forced to be equal to the
Journal of Biogeography 38, 394–405
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 Table 1 Morphological traits of ferns used in this study according to information from Moran & Riba (1995), Rojas (1996, 1997, 2001a,b, 2002a,b) and herbarium studies, and their assignment
into classes.

Trait Scale of measurement Description Class Source* Functional importance

Rhizome type Ordinal Absent/unknown 0 a Competition for space/light, especially in

ª 2010 Blackwell Publishing Ltd

Upright to short-creeping 1 a dense communities (Kluge & Kessler, 2007)
Creeping 2 a

Journal of Biogeography 38, 394–405

(Stout) tree-like 3 a
Laminar dissection Ordinal Entire 0 a Adaptations to harsh environments,
Once-pinnate (to once-pinnate-pinnatifid) 1 a especially marked temperature and
Twice- or more-pinnate 2 a humidity oscillations (Kramer et al., 1995;
Halloy & Mark, 1996)
Laminar morphology Ordinal Monomorphic 1 a Dimorphism facilitates spore dispersal
Slightly dimorphic 2 a (Kramer et al., 1995)
Dimorphic (including heterophyllous) 3 a
Laminar thickness Ordinal Thin (membranaceous to thin herbaceous) 1 a Thick leaves against harsh environments e.g.
Medium (herbaceous to paper-like) 2 a frost, drought (Dubuisson et al., 2003)
Thick (thick paper-like to very coriaceous, 3 a
stiff)
Scale and hair density Ordinal Absent (0%) 0 b Dense indument as protection against
Very sparse/weak (> 0–1%) 1 b desiccation, solar radiation, herbivory or
Sparse (1–10%) 2 b gas exchange blocking water films
Numerous (10–50%) 3 b (Ehleringer & Mooney, 1978; Smith &
Very numerous to covering surface (> 50%) 4 b McClean, 1989; Halloy & Mark, 1996)
Hydathodes Binary Absent 0 a Hydathodes facilitate effective water
Present 1 a transport and secretion of surplus
minerals (Kramer et al., 1995)
Indusium Binary Absent 0 a Indusia as mechanical defence against high
Present 1 a amounts of falling and running water,
protection of spores (Kramer et al., 1995)
Buds Binary Absent 0 a Buds as vegetative reproduction mode,
Present 1 a especially in wet environments (Mickel,
1976; Koptur & Lee, 1993)

*Source of information: a, literature information verified by personal observations; b, personal observations.

Phylogenetic and trait diversity of ferns

397
J. Kluge and M. Kessler
empirical frequencies, we called this null model the ‘uncon-
strained null model’.
The second model kept constant not only the species
richness of each plot, but also the abundance of each species
across all plots. This model assumes that the ability of
species to colonize a plot is a direct function of its frequency in
the whole dataset (Kembel & Hubbell, 2006). This was
achieved using the independent swap algorithm (Gotelli,
2000; Gotelli & Entsminger, 2001), also called the ‘checker-
board swap’. This algorithm searches for submatrices within
the original species · plot matrix of the form (0,1)(1,0) (where
0 and 1 represent absent and present species, respectively; note
that the respective cells of the submatrix need not be adjacent
in the original matrix), and swaps the entries of these cells so
that species richness of each plot and total frequency of the
species across all plots are maintained. The number of such
swappings for each generated null assemblage (30,000) exceeds
the number of filled cells within the original matrices (c. 2000
for terrestrial species, c. 4200 for epiphytic species), in order to
ensure that the resulting randomized matrix is sufficiently
different from the empirical one (Lehsten & Harmand, 2006).
As this model contrasts with the assumptions of the former
model concerning species frequency distributions, hereafter we
call it the ‘constrained null model’.
Structure of assemblages
We calculated the mean pairwise phylogenetic and trait
distance of all species pairs occurring in an assemblage based
on the empirical data (MPDemp, MTDemp). To determine if
the composition differed from randomness, we compared the
observed empirical assemblage values with values of ran-
domly generated null assemblages (Gotelli & Graves, 1996).
For 1000 such null assemblages, we calculated the mean
and standard deviation (MPDnull, sdMPDnull, MTDnull,
sdMTDnull).
The phylogenetic and trait diversity measured with this
method is, to a certain degree, correlated with species richness
(for assessment of the performance of several phylogenetic
diversity indices, see Schweiger et al., 2008). We were inter-
ested to determine whether an empirical assemblage value
differed from random expectation given the species richness of
an assemblage. Thus we calculated the standardized effect size
(Gotelli & Rohde, 2002) of the empirical phylogenetic
distances relative to the phylogenetic distances of the null
assemblages (MPDstand and MTDstand, respectively), which is
defined as

Applying SAR models to correct linear models for spatial
Metricstand ¼ Metricemp  Metricnull =sd Metricnull
This measure is equivalent to )1 times the net relatedness
index (NRI, Kembel et al., 2009), which has been proposed as
a measure for tree-wide phylogenetic clustering and overdi-
spersion of species within an assemblage (Webb, 2000; Kembel
& Hubbell, 2006), and is independent of species richness
(Swenson, 2009). Negative MPDstand and MTDstand values and
low quantiles (P < 0.05) indicate species assemblages where
398
the co-occurring species are more closely related than expected
by chance (clustering), whereas positive values and high
quantiles (P > 0.95) indicate species assemblages where the
co-occurring species are less closely related than expected by
chance (overdispersion). Values close to zero thus indicate
random assemblages.
Pseudoreplication and spatial autocorrelation
Each plot is assigned a significance value stating whether its
phylogenetic structure differs from that of the 1000 random
assemblages. However, when considering a set of such
statistical inferences simultaneously, hypothesis tests that
incorrectly reject the null hypothesis are more likely to occur
(that is, a form of pseudoreplication occurs; Benjamini &
Yekutieli, 2001). To cope with this, a stronger level of evidence
is required for an individual test to be stated as significant, to
compensate for the number of tests being made. We applied
the false discovery rate (FDR) analysis to correct for such
pseudoreplicated comparisons by computation of a P value
cut-off (Storey, 2002).
Additionally, spatial autocorrelation may affect the percep-
tion of species distribution data along spatial or other
gradients, because these distributions are inherently spatially
structured, thus adjacent locations tend to be more similar in
terms of ecological properties and processes than expected by
chance (Legendre, 1993). We used simultaneous autoregressive
(SAR; Bivand et al., 2008) models to expand traditional linear
models (e.g. based on ordinary least squares, OLS) with an
additional spatial term (spatial weight matrix), which incor-
porates the spatial autocorrelation structure of the data.
Neighbourhood weights for the construction of the spatial
weight matrix need to be defined, with the aim of reducing the
Moran’s I of the OLS models to almost zero and not significant
in the SAR models (Dormann et al., 2007). The resulting SAR
models are able to reduce the spatial pattern of model residuals
with independently distributed errors in regression models
(Kissling & Carl, 2008).
All calculations were performed using R (R Development
Core Team, 2009), with package picante (Kembel et al., 2009)
for the analysis of phylogenetic and trait structures; package
qvalue (Dabney et al., 2009) for performing the FDR; and
package spdep (Bivand, 2006) to run the simultaneous
autoregressive models.
RESULTS
autocorrelation eliminated the error terms in Moran’s I
present in the OLS analyses (see Appendix S1 in Supporting
Information). Hereafter, all reports on explained variances and
the respective significances result from the SAR models only.
Patterns of phylogenetic and trait diversity (MPD, MTD)
were significantly correlated, more strongly so for terrestrial
species (R = 0.66, P < 0.001) than for epiphytic species
(R = 0.34, P < 0.001).
Journal of Biogeography 38, 394–405
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 Phylogenetic and trait diversity of ferns

Figure 2 Mean phylogenetic diversity (MPD) and mean trait diversity (MTD) of fern assemblages along an elevational gradient in Costa
Rica, sorted by plot species richness. Each dot marks an individual plot (terrestrials, n = 156; epiphytes, n = 155). Regression lines with
logarithmic term and R2 are given; **P < 0.01; ***P < 0.001.

The arrangement of MPD and MTD values by species
richness (Fig. 2) showed that these relationships were not
linear, but asymptotically reached a plateau at high levels of
species richness. All relationships were significant (P < 0.01),
and R2 values of the regression models ranged from 0.30 to
0.54, emphasizing the asymptotic fit for the model curves. R2
values were higher for epiphytic than for terrestrial species.
Standardized values of phylogenetic and trait diversity
(MPDstand, MTDstand) were largely independent from variation
in species richness (Table 2) for both randomization proce-
dures, with the exception of values based on MTD of
epiphytes, in which relationships were significant but rather
weak (R2 < 0.15). Therefore we relied on these standardized
values as an independent measure of species assembly.
Mean standardized values obtained using the unconstrained
null model differed more strongly from zero than those
obtained using the constrained null model (Table 2). Com-
Table 2 Results of regression analyses of standardized values of
mean phylogenetic diversity (MPDstand) and mean trait diversity
(MTDstand) and fern species richness in 156 forest plots in Costa
Rica, separated for terrestrial and epiphytic species.
Randomization Diversity Species Mean
procedure measure group Slope R2 P value
paring the empirical with the simulated values of random
species distributions showed that phylogenetic and trait
structure were highly variable among plots (Fig. 3). Most
values fell within the 90% confidence intervals of the null
models, but the standardized values indicate clustering (neg-
ative) or overdispersion (positive) of assemblages with respect
to phylogenetic and trait variation. As expected, the uncon-
strained null model had higher proportions of plots tending
towards clustering or overdispersion than the constrained null
model (Fig. 3).
When the elevational trends of MPDstand and MTDstand were
analysed for all plots together, the significance level had to be
corrected due to multiple hypothesis testing (pseudoreplica-
tion). While a considerable number of plots showed significant
deviations from null expectations (dark grey columns in
Fig. 3), applying FDR left no significant deviations for any
assemblage. Along the elevational gradient, clear and signifi-
cant trends were found only for epiphytes with respect to
MTDstand (Fig. 4). Trends in MTDstand of epiphytes were
hump-shaped in both randomization procedures, indicating
that epiphytic assemblages had higher trait diversity than
random assemblages at the middle of the gradient (1000–
2000 m), and correspondingly lower trait diversity at the ends
towards lowlands and the mountain tops.

Unconstrained MPD Terrestrial 0.008 0.00 0.591 )0.18 DISCUSSION

Epiphytic 0.006 0.01 0.261 )0.56
MTD Terrestrial 0.033 0.02 0.110 0.14 Our study compares the phylogenetic and trait structure of
Epiphytic 0.060 0.15 < 0.001 1.05 ferns within the same assemblages to distinguish between
Constrained MPD Terrestrial 0.008 0.00 0.630 )0.06 ecological sorting of species based on their traits or their
Epiphytic 0.012 0.01 0.144 )0.09 evolutionary legacies. Because phylogenetic groups are gener-
MTD Terrestrial 0.009 0.00 0.638 )0.03 ally characterized by suites of traits, a close relationship of MPD
Epiphytic 0.027 0.07 0.001 0.11 and MTD is to be expected (Tilman et al., 1997; Lawton et al.,
Standardized values of mean phylogenetic diversity (MPDstand) and
1998; Prinzing et al., 2001). In our case, this relationship was
mean trait diversity (MTDstand) are based on comparisons of empirical significant, but rather weak, especially for epiphytes. Part of this
values with 1000 random assemblages, with two underlying random- mismatch can certainly be explained by the ‘diffuse nature’ of
ization procedures (unconstrained and constrained; see Materials and large datasets, especially the lack of finely resolved phylogenies.
Methods for details). Another explanation must also be taken into account: clades are

Journal of Biogeography 38, 394–405 399

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J. Kluge and M. Kessler

(a)

(b)

Figure 3 Histograms of standardized values for mean phylogenetic diversity (MPDstand) and mean trait diversity (MTDstand) of species
within 156 fern assemblages along an elevational gradient in Costa Rica (a) for the unconstrained model and (b) for the constrained model.
A negative value indicates that phylogeny and traits of the species within the assemblage are more related than expected by chance
(clustering), while a positive value indicates that species are more diverse than expected by chance (overdispersion). Values of most
assemblages fall within the range [)2; 2], indicating that there are no significant deviations from 999 random assemblages and hence falling
within the 90% confidence interval of the models. Dark bars and dashed lines mark the limit of significant deviations. Applying correction
for multiple hypotheses testing (false discovery rate, see Materials and Methods) diminishes all cases of significant deviations.

phenotypically plastic, and similar traits may have evolved
independently in phylogenetically distant groups. This is
especially interesting if phylogenetic and trait structures of
species assemblages show different trends along environmental
gradients. However, contrary observations exist as well. For
example, de Bello et al. (2006) reported no consistent effect of
increased richness on trait diversity in grassland assemblages
along humidity and grazing gradients: while species richness
varied considerably, the variety of traits did not differ between
samples of high and low species richness.
The crucial question now is whether the assembly of species
from a regional pool and their addition to the local pool are
random processes, or whether species with a certain set of
traits or from certain lineages are selectively favoured.
Structure of assemblages
Within the study area, fern assemblages were outstandingly
species-rich at mid-elevations and relatively species-poor at
both extremes of the elevational gradient, creating a symmet-
rical hump pattern in response to the environmental setting
(Kluge et al., 2006). It has often been stated that elevational
transects form a natural gradient of rapidly changing environ-
mental shifts, especially in temperature and humidity regimes,
and that particularly these factors govern species-richness
patterns (Hawkins et al., 2003; Currie et al., 2004). Dispersal
limitation is not likely additionally to influence this pattern
because of the compact nature of our study area and the
efficient spore dispersal of ferns (Barrington, 1993). Thus the
presence or absence of a phylogenetic fern group from a given
elevation along our study transect is determined rather by
selection operating on the entire suite of physiological and
morphological traits of the taxa (Duckworth et al., 2000).
Values of the MPDstand and MTDstand structure of the fern
assemblages were close to zero on average (Table 2), and after
correction for multiple hypothesis testing, none of the plots
showed significant deviations from random expectations
(although individually considered plots did so; Fig. 3). How-
ever, this does not imply that no such patterns exist, as they
might occur among morphological or physiological traits not
studied by us, or with respect to ecological conditions we did
not include, such as microhabitat differentiation.

400 Journal of Biogeography 38, 394–405

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 Phylogenetic and trait diversity of ferns

(a)

(b)

Figure 4 Standardized values for mean phylogenetic diversity (MPDstand) and mean trait diversity (MTDstand) of 156 fern assemblages
based on comparisons of empirical MPD and MTD values with values from 999 random assemblages along an elevational gradient in Costa
Rica (a) for the unconstrained model and (b) for the constrained model. Each dot marks a plot; in contrast to Fig. 3, here we applied false
discovery rate to account for multiple hypotheses testing, leaving no individual plot with significant deviation from random assemblages.
However, trend lines across all data points combined were significant, and lines depict second-order polynomial regressions with *P < 0.05;
**P < 0.01; ***P < 0.001. Regressions and associated P values were corrected for spatial autocorrelation by applying simultaneous auto-
regressive models.

In any case, along the elevational gradient MPDstand and
MTDstand we documented various, but mainly very weak and
above all insignificant, trends. The only exception, trait
diversity patterns of epiphytes, raises two issues: the mismatch
between elevational trends of phylogenetic and trait diversity
in epiphytes, and the difference between both life forms in
general.
The humped trend of epiphytic trait richness may imply
that the selection of species from the regional pool in these
highly species-rich assemblages favours species that are more
distinct in terms of morphological features than a random
selection would be, and that are thus able to fill the available
microhabitats more effectively. As proposed by Kessler
(2001), Hemp (2002), Bhattarai et al. (2004), Kluge et al.
(2006) and others, the very humid conditions at mid-
elevations in tropical mountains represent optimal growing
conditions for ferns, so climate is unlikely to act as a filter
excluding ill-adapted taxa. Under these conditions, compet-
itive interactions may favour species with sets of traits
different from those already represented. Similar results were
recently found by Graham et al. (2009) for Andean hum-
mingbird assemblages, where sites without ecologically stress-
ful factors showed overdispersion and hence interspecific
competition.
Although trait conservation has frequently been docu-
mented across most plant groups (Prinzing et al., 2001;
Silvertown et al., 2006), the distribution of epiphytic taxa
along this elevational gradient is close to random and constant,
thus being somewhat decoupled from the distribution of traits.
It seems that an overdispersed epiphytic trait structure at mid-
elevations is the product not only of specific processes of how
species may enter an assemblage, but also of how they might
evolve while persisting within the assemblage. As the taxa are
able to occur almost everywhere (random phylogenetic
dispersion) and may be evolutionarily plastic, closely related
species coexisting at certain sites may undergo trait shifts
(‘character displacement’; Schluter, 2000) that reduce niche
overlap. For example, Grant & Grant (2006) found this pattern
for finches on the Galápagos Islands, where closely related
species rapidly developed different traits, thus enhancing trait
richness while maintaining phylogenetic richness. Additionally,
the mid-elevations host not only the highest species richness,
but also the highest number of individuals, suggesting that this
is the zone of highest productivity for ferns. It has been

Journal of Biogeography 38, 394–405 401

ª 2010 Blackwell Publishing Ltd
J. Kluge and M. Kessler
proposed that generation times are shorter in highly produc-
tive environments, resulting in higher diversification rates
(Cardillo, 1999).
Conversely, elevations with tendencies to trait clustering also
have low species richness. Here, species are apparently selected
for specific sets of traits that pass the filters dictated by the
local environmental conditions. Climatic conditions, distur-
bance regimes or biotic interactions have been suggested as the
main environmental filters removing species that lack appro-
priate traits for persistence under particular conditions
(‘assembly rules’ sensu Keddy, 1992; see also Dı́az et al.,
1998; Duckworth et al., 2000). Likewise, convergent evolution
across the whole species pool may force species towards a
suitable set of traits to cope with ambient conditions (e.g.
entire and stiff leaves to enhance frost or drought resistance;
Kluge & Kessler, 2007). Again, phylogenetic relatedness still
may be random as these traits have evolved independently in
different lineages (Cavender-Bares et al., 2004; Kraft et al.,
2007).
In contrast to epiphytes, assemblages of terrestrial species
were found to stay almost random throughout the gradient.
Whatever the driving factor of assembly might be, the
epiphytic life-form seems to be more subject to selecting
processes. There are two possible explanations. First, the
microhabitat diversity among height gradients within host
trees (from tree base to outer canopy) is certainly higher by far
than the soil variation within a 400 m2 plot, facilitating
differentiation within the epiphytic domain at mid-elevations.
Second, epiphytes are more exposed to, and thus coupled to,
environmental stress (Hietz & Hietz-Seifert, 1995) than
terrestrial species, so that selecting forces may be more
pronounced. This interpretation is supported by the fact that
species richness of epiphytes varies more strongly along the
elevational gradient (from one to 48 species per plot) than that
of terrestrial species (three to 32), suggesting that epiphytic
fern assemblages are under relatively stronger limiting condi-
tions at the extremes of the gradient than terrestrials.
CONCLUSIONS
Our results show that both terrestrial and epiphytic fern
assemblages exhibit almost random phylogenetic structure
along the elevational gradient. Only epiphytic assemblages tend
towards trait overdispersion at mid-elevations and trait
clustering towards gradient extremes. This can be explained
by temperate and humid environmental conditions at mid-
elevations, which facilitate a wide trait range due to the lack of
strong environmental filters (frost, drought). Phylogenetic and
trait diversity do not show, at least for epiphytes, a strong
relationship. This may reflect selective pressure that results in
reduced trait and hence niche overlap between closely related
species (‘selective trait shifts’). This process inflates trait space,
while the phylogenetic relationships are maintained.
More generally, we found that comparison of empirical and
null assemblages enables the detection of assemblage structures
that deviate from random expectations. The direction of such
402
deviations, especially along spatial and environmental gradi-
ents, gives insights into the processes governing species
assembly. Our results were qualitatively congruent for both
null models and, as expected, the unconstrained null model
showed more pronounced trends due to more liberal condi-
tions in constructing random assemblages.
ACKNOWLEDGEMENTS
This study was supported financially by grants from the
Deutsche Forschungsgemeinschaft (DFG) and Deutscher
Akademischer Austauschdienst (DAAD). We thank Mirkka
Jones, Rafael Wüest and two anonymous referees for critical
comments and discussions on the manuscript. We thank
Sandrine Pavoine, Steven Kembel, Emmanuel Paradis, Karsten
Wesche, Henrik von Wehrden and Daniel Kissling for
statistical support and for advice concerning R packages.
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SUPPORTING INFORMATION
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online version of this article:
Journal of Biogeography 38, 394–405
ª 2010 Blackwell Publishing Ltd
Phylogenetic and trait diversity of ferns
Appendix S1 Standardized regression coefficients of ordin-
ary least squares and simultaneous autoregressive models of
fern richness distribution along an elevational gradient in
Costa Rica.
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BIOSKETCHES
Jürgen Kluge is a lecturer at the Faculty of Geography at the
University of Marburg, and research assistant at the Depart-
ment of Systematic Botany of the University of Zurich. He has
research interests in the field of diversity and biogeography
with a special focus on pteridophytes and bryophytes.
Michael Kessler is researcher at the Department of System-
atic Botany of the University of Zurich, and scientific curator
of the Botanical Garden of the university. His research focuses
on the systematics, diversity, biogeography and conservation
of tropical plants and birds, with a special focus on mountain
forests.
Editor: Ole Vetaas
405