Disturbance Alters the Phylogenetic Composition and
Structure of Plant Communities in an Old Field System
Department of Ecology and Evolutionary Biology, University of Toronto, Toronto, Ontario, Canada
The changes in phylogenetic composition and structure of communities during succession following disturbance can give
us insights into the forces that are shaping communities over time. In abandoned agricultural fields, community
composition changes rapidly when a field is plowed, and is thought to reflect a relaxation of competition due to the
elimination of dominant species which take time to re-establish. Competition can drive phylogenetic overdispersion, due to
phylogenetic conservation of ‘niche’ traits that allow species to partition resources. Therefore, undisturbed old field
communities should exhibit higher phylogenetic dispersion than recently disturbed systems, which should be relatively
‘clustered’ with respect to phylogenetic relationships. Several measures of phylogenetic structure between plant
communities were measured in recently plowed areas and nearby ‘undisturbed’ sites. There was no difference in the
absolute values of these measures between disturbed and ‘undisturbed’ sites. However, there was a difference in the
‘expected’ phylogenetic structure between habitats, leading to significantly lower than expected phylogenetic diversity in
disturbed plots, and no difference from random expectation in ‘undisturbed’ plots. This suggests that plant species
characteristic of each habitat are fairly evenly distributed on the shared species pool phylogeny, but that once the initial
sorting of species into the two habitat types has occurred, the processes operating on them affect each habitat differently.
These results were consistent with an analysis of correlation between phylogenetic distance and co-occurrence indices of
species pairs in the two habitat types. This study supports the notion that disturbed plots are more clustered than expected,
rather than ‘undisturbed’ plots being more overdispersed, suggesting that disturbed plant communities are being more
strongly influenced by environmental filtering of conserved niche traits.
Citation: Dinnage R (2009) Disturbance Alters the Phylogenetic Composition and Structure of Plant Communities in an Old Field System. PLoS ONE 4(9): e7071.
Editor: Jerome Chave, Centre National de la Recherche Scientifique, France
Received July 21, 2009; Accepted August 21, 2009; Published September 18, 2009
Copyright: ? 2009 Russell Dinnage. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits
unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Funding: This work was supported by an NSERC Discovery Grant to Peter Abrams (my academic supervisor). (http://www.nserc-crsng.gc.ca/) The funders had no
role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
Competing Interests: The author has declared that no competing interests exist.
* E-mail: firstname.lastname@example.org
are reset. From bare ground new communities sprout up and
change over time as the forces of seed bank dynamics, colonization,
environment and interspecific interactions act upon them. Studying
successional dynamics often yields insight into these processes,
which is why the process of succession in plant communities has
remained an important focus of research in community ecology
[1,2]. A relatively new method of analyzing community data
examines how the evolutionary history (phylogeny) of species
influences community structure. I hope to show that the techniques
of community phylogenetics have potential for expanding our
understanding of succession.
Disturbance can change the balance of forces acting on the
local community. By eliminating species and thus freeing space
and resources, disturbance usually will temporarily reduce the
impact of interspecific competition [3,4,1]. As succession occurs,
the original strength of competition is gradually restored.
Change in the strength of competition is thought to be one of
several important drivers of changes in community composition
during early succession . In general, this process of recurring
disturbance and successional change should promote coexis-
tence of competing plants if there is a trade-off between
competitive ability and colonization efficiency or resistance to
Any change in competition can also affect the phylogenetic
structure of communities [6–9]. Competition and ‘environmental
filtering’ affect the degree of similarity in the ecological roles
(‘niches’) of species in communities, and phylogenetic distance can
be treated as a proxy for this similarity – more closely related
species being assumed to be more alike. The concept of limiting
similarity [10,11] proposes that similarity in the resource
requirements and usage by consumer species limits their ability
to coexist. On the other hand similar species will also share
environmental tolerances, meaning that more similar species will
be more likely to coexist in any given area . Thus the processes
of competition and environmental filtering act in opposite
directions. By using phylogeny to explore such patterns of
similarity it may be possible to distinguish which process played
a stronger role in that community. The balance of competition
and environmental filtering is expected to change during the
process of succession, and should therefore produce predictable
changes in phylogenetic structure.
The strength of competition should be weaker in communities
where a recent disturbance has eliminated or reduced the
abundance of competitive dominants. It is known that succession
occurs in abandoned agricultural fields, changing communities
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from a bare plowed field through to the grassland, herbaceous
mixed community we usually refer to as ‘old field’, and eventually
to woodlands [13,14]. Succession from bare ground to a semi-
stable old-field community occurs quickly – on the order of a few
years – making it an ideal system to study succession. In eastern
North American old fields, the difference between communities of
plants before and after a disturbance is thought to result partially
from the elimination of competitive dominant species which
include several common grass species (Poa spp., Bromus spp., etc.)
and a few large herbaceous dicots such as Solidago spp., and Aster
spp., [15,16]. In this study I evaluate whether the phylogenetic
structure of an old field herbaceous plant community changes in a
predictable manner following elimination of these dominant
species. I predict that sites that have been recently disturbed will
be more phylogenetically ‘clustered’ than those that have not,
because reduced competition following disturbance will relax
limiting similarity. In addition, disturbance might select for
disturbance tolerance traits which could be phylogenetically
conserved. The purpose of this study is to test this prediction of
Several other studies have attempted to quantify the effect of a
disturbance on patterns of relatedness among species. Most,
however, have used taxonomic measures of relatedness and have
found mixed results, with some finding that disturbance increases
average relatedness [17–19], but others finding no difference .
One study found that plant communities tended to have lower
phylogenetic diversity in urban areas , but this study
encompassed the entirety of Germany, and so was conducted on
a very large scale. The study described here is concerned with
what happens at the patch scale within a single habitat type. This
allows control of differences in habitat that might be confounded
with disturbance when compared across large scales. This is
important because certain types of habitat may be selected for by
humans when creating anthropogenic disturbance.
I distinguish two approaches to incorporating phylogenetic
information: analyzing the phylogenetic composition and the
phylogenetic structure of communities. Phylogenetic composition
simply incorporates phylogenetic relatedness information into
traditional methods of studying communities – for example:
ordination approaches – which normally treat all species as
independent. Phylogenetic structure, on the other hand, is a
summary of the phylogenetic information contained in each
community, analogous to measures of diversity in traditional
analyses . Phylogenetic structure is analyzed with phylogenetic
diversity indices (several are reviewed in ). Phylogenetic
structure can be divided into phylogenetic alpha diversity (within
site) and phylogenetic beta diversity (between site) . I only look
at phylogenetic alpha diversity in this study, however, the concept
of comparing phylogenetic composition is related to phylogenetic
beta diversity, because site differences can be compared, however,
the method of calculating distances between sites is different.
The questions addressed here are: 1) Are recently disturbed old
field communities different than undisturbed communities both in
species composition and phylogenetic composition?; 2) Is the
phylogenetic structure of recently disturbed communities system-
atically different than that of undisturbed communities? If so, is
there evidence that reduced competition after disturbance allows
communities to be more phylogenetically ‘clustered’?
I was granted permission to conduct the study on the Koffler
Scientific Reserve (KSR) at Joker’s Hill (King City, Ontario;
http://www.ksr.utoronto.ca/jh.html), a 350 hectare property
containing a mix of primary forest, secondary forest and open
habitats, including a large area of old field sites. Many areas of the
reserve are plowed for experiments and agriculture. I chose fields
that had been plowed within the last 2 seasons as examples of
recently disturbed systems (R. Dinnage, personal observation). I
located 19 of these recently disturbed fields that were separated
from each other by at least 50 meters. Most were separated by
100 meters or more, and were spread throughout the old field
habitat on the reserve. In each of these fields a 10610 meter plot
was placed haphazardly within 10 meters of the edge of the
plowed area. Each of these ‘disturbed’ plots was then paired with
an ‘undisturbed’ plot of the same size from just outside the plowed
The community composition of herbaceous forbs was measured
by surveying the presence or absence of species within four
161 meter quadrats placed within the four quadrants of each plot.
The data from the four quadrats were later combined to the plot
level, with the number of quadrats in which each species was
found acting as a coarse measure of frequency (0–4). The survey
was conducted between August 24–31, 2007. All analyses were
based on this survey data combined with a phylogeny for all
species found in the samples. The raw sample data (data S1) and
the phylogeny (data S2) are included as supplementary informa-
I created a phylogeny for all the herbaceous old field plants I
surveyed by combining a backbone tree based on the APG
generated by Phylomatic (http://www.phylodiversity.net/phylomatic/
phylomatic.html)with subtrees created using downloaded sequences.
I made three such trees for three families that lacked resolution on
the backbone tree (Asteraceae, Lamiaceae, and Brassicaceae), using
allspeciesfrom thesefamiliesfound inthesamplesplus several other
species which had divergence estimates between them .
The internal transcribed regions (ITS1 and ITS2; but not 5.8S)
for each species in these sub-trees plus an outgroup species (from
the hypothesized sister family) were downloaded from GENBANK
. After downloading I aligned them using MAFFT alignment
 with default settings, concatenated them, then analyzed them
with maximum parsimony using the PHYLIP 3.47  software
package (dnapars program) with default settings.
Branch lengths for the backbone tree were calculated with the
BLADJ program included with Phylocom 3.41 . This program
assignsages to nodes that wereestimatedin reference, and then
estimates the ages of remaining nodes so that they spread evenly
between the dated nodes. This method loses some phylogenetic
information, but is better than simply using number of nodes
separating taxa as an estimate of phylogenetic distance, especially
for community phylogenies which are highly incomplete.
Branch lengths on the three subtrees were calculated from the
maximum parsimony analysis and then converted into age
estimates using rate smoothing in the software package r8s .
The estimated age of divergence of the family was assigned
according to reference . Several taxa that were included either
in reference  or  – which estimated divergence times for
groups within the Asteraceae – were included in the subtrees so
that an estimated age could be assigned to the common node
between them and improve the accuracy of the r8s estimate of
intervening nodes. Species not occurring in the samples were then
trimmed off, before I grafted these subtrees onto the backbone
tree. This final tree is a nearly fully resolved (to the genus level)
ultrametric tree with branch lengths in units of time (millions of
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year) – i.e., a community chronogram (figure 1). Measures of
community phylogenetic structure were based on this phylogeny.
Thuja occidentalis was an unusual occurrence in one plot and was
removed from subsequence analysis as a extreme outlier (very
large branch length and very rare). Inclusion of Thuja did not
change the results of the analysis.
Comparison of disturbed and undisturbed plots
I compared disturbed and undisturbed plots using several
measures of community structure, both traditional and phyloge-
netic. All analyses were performed using R Statistical Language
I looked for a difference in species composition between
disturbed and undisturbed sites using non-metric multidimensional
scaling (NMDS) using the metaMDS function in the vegan
package . NMDS is an ordination technique which graphically
arranges communities according to their similarity in species
composition. I used Bray-Curtis distance because it has been
found to perform well in simulations for ecological data . Plots
which occur close together on the NMDS generated axes are
similar in composition. For analysis I used three axes, which fit the
data well and resulted in a stress of 15.1%. To test the difference
between disturbed and undisturbed plots I used the envfit function
from vegan, with plot type as a categorical factor variable. Envfit
will calculate centroids for each factor level and calculate the
difference between centroids. Significance of this difference is
calculated using 1000 random permutations of the factor levels. If
the observed difference in centroids is greater than more than 95%
of the randomly permuted datasets, we can reject the null
hypothesis of no difference at an alpha of 0.05.
To test for differences in phylogenetic composition between
disturbed and undisturbed plots I again used NMDS, but instead
Figure 1. Community chronogram of old field species with their frequency in two habitat types. On the left is a community chronogram
with branch lengths in millions of years. On the right is a barchart showing the relative frequencies of the species in the two different plot types.
Branch colors represent the relative frequency within the plot types of the clade it connects to the tree. Darker grey is more in undisturbed plots, light
grey is more in disturbed plots. Node labels: (1) Root. (2) Asterids. (3) Asterid 1. (4) Lamiales + Solanales. (5) Lamiales. (6) Solanaceae. (7) Asterid 2.
(8) Asteraceae. (9) Asteroideae. (10) Astereae. (11) Erigeron. (12) Aster. (13) Goldenrods. (14) Solidago. (15) Anthemideae. (16) Heliantheae. (17) Cirsium.
(18) Rosids + Vitaceae. (19) Rosids. (20) Rosid 1. (21) Fabaceae. (22) Rosid 2. (23) Brassicaceae. (24) Caryophyllales. (25) Amaranthaceae. Node names
are based on the APG system of classification (http://www.mobot.org/MOBOT/research/APweb/) Note: Solidago altissima and S. canadensis have been
combined into S. canadensis for brevity.
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of species composition as the input I used a representation of the
phylogenetic nodal structure of each community. To do this I used
the node-as-factor function in Phylocom . This function
generates a matrix with a different column for every node in the
input phylogeny – then for each plot sample it fills in what nodes
are present in that community, weighted by their frequency. In
order for a node to be considered present in a community, at least
one species from the clade subtending that node must be present.
The result is similar to a standard community matrix, but with
columns representing phylogeny nodes instead of species. This
allows the incorporation of phylogenetic information into
ordination, by allowing communities that share nodes to be
considered similar. In an ordinary ordination species are treated
independently. For example, if two closely related species have
disjunct distributions, they could cause communities to be very
different on a traditional ordination. However, using a node-as-
factor approach, their close relationship will cause these
communities to be more closely clustered. I used three axes
resulting in a stress of 11.7%. Again, envfit was used to test the
difference between disturbed and undisturbed plots using 1000
I used two methods to compare phylogenetic structure amongst
habitats, and take concordance between the results to be a sign of
First, I calculated a phylogenetic diversity index
for all the plots that could be compared amongst them. I chose two
related phylogenetic diversity indices: phylogenetic species variability
(PSV) and phylogenetic species evenness (PSE) . PSV is calculated as
the expected variation within a community for a trait that is
evolving neutrally at a fixed rate (i.e. under brownian motion sensu
Felsenstein ). This method was useful for comparing between
habitats because it is unbiased with respect to species richness
[36,38]. This is desirable because disturbed and undisturbed
habitat are likely to differ in species richness. PSE allows for the
incorporation of abundance data into PSV. I used species
frequency as a measure of abundance.
PSV and PSE, like all phylogenetic diversity indices, are
dependent on the shape of the input phylogeny, which is a
function of the species pool considered. In other words, every
species pool will have a unique ‘expected’ phylogenetic diversity
for plots of differing species richness. Therefore, phylogenetic
diversity indices must be interpreted in terms of deviation from the
expected in order to make inferences about forces acting on the
plot scale (i.e. independent of the forces which created the species
pool). I therefore compare phylogenetic diversity in two ways. First
I compare the raw diversity values, which can tell us about the
overall pattern of phylogenetic diversity amongst habitat types. I
do this with a simple paired t-test for PSV and PSE. However,
since raw PSV and PSE incorporate information both about the
structure of the overall species pool of the habitat, in addition to
structure at the plot scale, this comparison cannot distinguish the
forces that are at work within each different habitat, unless we take
the species pool for each habitat to be the same. Therefore, I
compare how plots in each habitat deviate from their expected
phylogenetic diversity based upon the species pool for that habitat
by generating null distribution based upon a simple null model of
Null distributions were generated for PSV and PSE using the
phylostruct function in the R package ‘Picante’ . This function
generates null communities by randomly assembling them from
the observed species pool. The null model I used randomly placed
species into communities so that each species maintained its
original frequency among plots. Results using other possible null
models were similar. Null distributions of mean PSV and PSE
were generated for 1) all plots 2) just disturbed plots, and 3) just
‘undisturbed’ plots, to which the observed mean PSV and PSE
I compared the degree to which phylogenetic
distance amongst species pairs was correlated with their degree of
co-occurrence (as in ). I used the comm.phylo.cor function in the R
phylogenetic distances among species using an input phylogeny
and then compares this to an index of species co-occurrence using
correlation. I used Schoener’s index of co-occurrence (‘cij’ ),
following reference . For visualizing the results I placed species
pairs into ‘bins’ based on their phylogenetic distance from one
another. Each bin spanned approximately 10–15 million years. I
calculated the mean and standard error of the co-occurrence
indices within each phylogenetic distance bin and plotted this. The
raw data was used to calculate statistics for hypothesis testing.
The test was repeated for: 1) all plots, 2) just disturbed plots, and
3) just ‘undisturbed’ plot. Traditional Pearson correlation statistics
were produced for each, however, the assumption of this statistic
are violated. Because the comparison was conducted on pairwise
measures, and each species is compared to every other species,
datapoints are not independent. To control for this violation, I
performed a randomization test . Because I was interested in
the effects of phylogeny, species were randomly shuffled amongst
the tips of the phylogeny 1000 times and the Pearson correlation
recalculated each time. This produced a null distribution of
correlation coefficients to which the observed values could be
compared. This procedure is essentially similar to a ‘Mantel’ test. I
could also test if the Pearson correlation value differed significantly
between habitats by calculating the difference between generated
correlations for the disturbed habitat and those for the
‘undisturbed’ habitat for each 1000 iterations. This creates a null
distribution for the difference between habitats in their correlation
between phylogenetic distance and co-occurrence. If the actual
difference is greater than 95% of the generated values, then I can
conclude that it is significant at the a=0.05 level. Since I expected
disturbed plots to be more phylogenetically clustered, and thus
have a more negative correlation between phylogenetic distance
and co-occurrence I performed a one-tailed test of this hypothesis.
Disturbed plots had nearly 70% more species than undisturbed
plots (p,0.001). Nonmetric multidimensional scaling plots showed
strong segregation between disturbed and undisturbed plots. The
two environments separated mostly on axis 1 and axis 3 – only
these axes are shown in the plot (figure 2a). The difference in
centroids was significant (p,0.001).
NMDS using the phylogenetic node structure of the plots
showed even stronger separation between disturbed and undis-
turbed plots, with no overlap of the standard deviation ellipses
(figure 2b). This time most of the separation occurred in the first
two axes, which were plotted (figure 2b). The centroids were
significantly different (p,0.001).
Most of the major clades have a relatively even representation in
both habitat types. This can be seen in figure 3, as the major
division in the tree used here (rosids, asterids, Asteraceae) fall along
the dividing line between disturbed and undisturbed habitat.
Within these major groups, each smaller clade seems to dominate
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in one habitat or the other. On the other hand, it is very rare that
two species which are each others’ closest relative on the tree are
found in different habitats. Therefore, habitat preference seems to
be phylogenetically conserved at an intermediate phylogenetic
There was no significant difference in PSV (t=20.67, df=18,
p=0.51) or PSE (t=20.49, df=18, p=0.63) between habitats,
though they were both slightly lower in the ‘undisturbed’ habitat
(figure 4). However, habitats differed in how they deviated from
expected PSV and PSE. When looking at plots across both
habitats, on average both PSV and PSE were significantly lower
than expected by chance under a null model of community
assembly (PSV: p,0.001; PSE: p,0.001; figure 4). When
considered separately, however, disturbed plot were on average
significantly phylogenetically clustered – PSV and PSE were lower
than expected (PSV: p=0.008; PSE: p,0.001; figure 4). On the
other hand, ‘undisturbed’ plots had a random phylogenetic
structure, with no difference between observed PSV/PSE and
expected based on the null mode (PSV: p=0.59; PSE: p=0.68;
figure 4). This result was corroborated by a significant negative
correlation between co-occurrence and phylogenetic distance
between species in the disturbed plots (corr=20.21, p=0.003;
figure 5), but no significant correlation in the ‘undisturbed’ plots
(corr=20.03, p=0.32; figure 5). The difference in this correlation
between habitats was also significant (p=0.017).
Community composition differed between disturbed and
undisturbed plots. Disturbed plots had higher species richness,
consistent with previous results in old field systems [e.g 15,16].
Nonmetric multidimensional scaling confirmed that the two
habitat types differed in their species composition. This difference
was exaggerated in the analysis incorporating the phylogenetic
node structure of the plots. This means that disturbed plots are
quite phylogenetically distinct from undisturbed plots, with each
type of plot represented by different terminal clades. This can be
seen visually in figure 1 and 3.
Recently disturbed plots displayed larger variation in phyloge-
netic ordination scores than undisturbed plots. This is likely
because most species and clades that are dominant in undisturbed
habitats are also found to a lesser degree in disturbed plots. Several
factors are likely responsible for this, including the fact that many
are perennial plants which can resprout from rhizomes after the
plots were plowed. In addition there is probably a large propagule
pressure from old field dominants entering into the disturbed plots.
On the other hand, very few species or clades characteristic of
disturbed habitats were also found in undisturbed habitats. This
may be because most are annual weeds which cannot easily
establish under the conditions of high density and shading in the
undisturbed plots, because they are adapted to open habitats.
Overall, I found that when all plots were considered together,
they were on average significantly clustered phylogenetically,
when compared to a null model. This was true both for PSV, and
PSE when compared to a null model of species assembly. It was
also true when pairwise co-occurrence values were correlated with
phylogenetic distance. This is consistent with many other studies of
phylogenetic structure in plant communities, most of which have
found phylogenetic clustering when structure was found [reviewed
by 41,42]. However, simulation studies have found that these tests
can be liberal under several circumstances , including cases of
spatial autocorrelation due to limited dispersal, and phylogenetic
structure in the experiment-wide abundances. Abundance Phylo-
genetic Deviation index (APD ) measures the clustering of
species abundance on the phylogeny by comparing the mean
phylogenetic distance of species in the experiment, with the
abundance-weighted mean phylogenetic distance. Positive values
suggest clustering of abundances, whereas negative values suggest
overdispersion of abundances. In this study the APD value for
undisturbed plots was 0.08 and for disturbed plots it was 0.10 –
slight clustering. This could have made the overall test liberal,
however, it is the comparison among habitat types which is the
important result. Since the APD values are close, there is little
reason to suspect that the test for the disturbed sites is more liberal
than that for the undisturbed sites, and so there should not be a
higher probability of finding significant results in the disturbed
Figure 2. Non-metric multidimensional scaling scores for
disturbed and undisturbed plots. Plot of the nonmetric multidi-
mensional scaling scores for the two most important axes for all plots
using the a) species composition data, or b) phylogenetic nodal
structure data. The centroids for disturbed and undisturbed plots are
labelled and linked to all points with radiating lines. Ellipses represent 1
standard deviation. Size of the points represents the relative number of
species found in the plots.
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Despite no difference between disturbed and undisturbed
habitat types in phylogenetic diversity indices, there was a
difference in how they deviated from their expected phylogenetic
diversity, based on null models of community assembly (figure 4).
Disturbed plots were significantly more ‘clustered’ than expected
under a null model of community assembly, whereas undisturbed
plots did not deviate from random expectation. This could only
have come about if the ‘expected’ phylogenetic structure of each
In this study, I found that the available species pool for
disturbed and undisturbed habitat differed, and that the
phylogenetic diversity of each pool also differs. The average
phylogenetic diversity expected under a null model of community
assembly is reflective of the underlying phylogenetic structure of
the species pool. Disturbed plots had a higher expected
phylogenetic diversity, suggesting that at a regional scale disturbed
areas contain lineages that are less related than in undisturbed
areas. This is contrary to my expectation, as it is usually thought
that disturbance should select closely related species. One possible
explanation is that the undisturbed communities actually consti-
tute a harsher environment for species due to their high level of
competition, and that there may be a suite of traits that make
species suited to this environment which are phylogenetically
conserved. On the other hand, since I essentially only have a single
sample for each habitat’s pool of species, this difference may be
due to chance alone. It is impossible to assess the generality of this
pattern because most studies which have found higher clustering in
disturbed habitats have failed to distinguish between regional
species pool differences and more local plot level differences
The results at the plot-level within each habitat type were
different. Disturbed plots were more phylogenetically clustered
than expected by chance, so that individual plots had, on average,
lower phylogenetic diversity than their regional habitat pool. In
undisturbed habitat, phylogenetic diversity in individual plots did
not differ significantly from the regional habitat pool. A weaker
competitive environment in recently disturbed plots could lead to
more phylogenetic clustering than expected in several ways. If the
environmental tolerances of species are phylogenetically con-
served, then differences in the environment could act as a filter,
and closely related species will be more likely to coexist. A heavy
disturbance such as plowing could create a harsh or unique
environment that selects for species that can tolerate these
Stripping away dominant vegetation could lay bare environ-
mental variation which was masked before. This could happen if
the competitive stresses of the environment are strong enough that
they become more important than anything else, and so in a sense,
homogenize the environment. If so, such a competitive environ-
ment will act as an initial filter, reducing the species pool, but
thereafter species are distributed randomly with respect to
phylogeny. This could also happen if traits relating to competition
are less phylogenetically conserved than those involved with
dealing with abiotic stresses which may be more prevalent in
recently disturbed environments.
Another possible explanation is that both environments are
experiencing forces that promote phylogenetic clustering, but in the
undisturbed environment there are also strong counteracting forces
promoting phylogenetic overdispersion. This would happen if
ecological traits related to niche partitioning were phylogenetically
Figure 3. Non-metric multidimensional scaling scores for all phylogenetic nodes with reference to habitat occurrence tendency.
Ordination plot for the phylogenetic ordination shown in figure 2b but with plot points removed and phylogenetic node vectors displayed. For
clarity, only important or non-redundant nodes are displayed. Filled bubbles are a rough representation of the branching structure of the nodes from
one another. Dark filling represents more association with undisturbed plots whereas lighter filling represents more association with disturbed plots.
Dotted ellipses represent the centroids and 1 SD area as a reference for where disturbed and undisturbed plots fall on the diagram. Nodes which are
referred to can be seen on figure 1.
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conserved, and that the stronger competition in undisturbed plots
led to stronger niche differentiation. Opposing processes that
counteract each other’s effect on phylogenetic structure has been
demonstrated before. One study found that when environmental
factors were statistically removed from sunfish communities,
phylogenetic overdispersion was revealed . An argument
against this possibility is that phylogenetic conservation of niches
has been difficult to demonstrate in plants. For example a study of
meadow communities showed that phylogenetic distance was not
correlated withniche seperation along several axes of soil conditions
. Another study came to the conclusion that the intensity of
competition between plant species pairs was only weakly correlated
with phylogenetic distance in a meta-analysis of pot experiments,
and only for certain taxa .
Though competition and environmental filtering are often
thought of as dominant forces in the structuring of communities,
there are other factors that could come into play in this system and
others. Predation, or herbivory in this case, could be involved in
the structuring of communities. Herbivory could promote
phylogenetic overdispersion if herbivores fed on more than one
species, and those species tended to be closely related, through the
action of ‘apparent competition’ , in a manner analogous to
resource competition. Theory has shown that apparent competi-
tion can act very similarly to resource competition , and so
limiting similarity may act here as well, only in this case the
similarity is in shared predators rather than shared resources. This
effect can also be thought of as a phylogenetic extension of the
Janzen-Connell hypothesis [49,50] as described in a recent review
of community phylogenetics . Such ‘‘Janzen-Connell’’ effects
could be stronger in the undisturbed plots. Though it is unlikely
that herbivore pressure differs greatly between the habitats (given
their close spatial proximity), herbivore effects would likely be
gradual and only result in significant difference in community
Figure 4. Phylogenetic structure values for disturbed and
undisturbed plots, and overall. Plot showing the mean deviation
in the phylogenetic structure measures for each of the plot types and
overall. Diamonds represent the observed mean. Solid lines represent
the line are the 95% confidence interval from the null model.
Figure 5. Relationship between co-occurrence and phylogenetic
relatedness for disturbed and undisturbed plots. Plots showing
the relationship between phylogenetic distance of species and their
degree of co-occurrence for disturbed and undisturbed plots. Co-
occurrence index is Schoener’s index . Line of best fit is included for
illustrative purposes, and is based on least-squares.
Disturbance and Phylo. Struct.
PLoS ONE | www.plosone.org7 September 2009 | Volume 4 | Issue 9 | e7071
structure over many years – years which the undisturbed plots
have experienced and which recently disturbed plots have not.
Predation could also act as a filter. Though smaller specialized
herbivores such as insects may not vary between the habitats, deer
herbivory may. Deer are common on the property on which I
conducted my surveys and they may impose pressure on old field
plant communities. The increased exposure of disturbed fields
makes plants more apparent, and so deer could be a stronger force
in recently disturbed plots. If traits that lead to deer-resistance are
phylogenetically conserved, deer could act as a filter leading to
phylogenetic clustering in areas where deer are more common.
Many of the effects discussed above vary in the timescale over
which they act. Most of the filters promoting clustering will act
immediately, whereas those thought to promote overdispersion
will act gradually. It may be useful to define filters as density-
independent effects on fitness, whereas competitive effects
(including both resource and ‘apparent’) are density-dependant,
in that they become stronger in high densities. It may be then that
disturbance exposes plant communities to environmental filters
which leads to greater than expected phylogenetic clustering at low
densities, after which communities gradually return to their
‘expected’ level of phylogenetic structure, through the action of
weak dispersion promoting forces, such as limiting similarity and
Janzen-Connell effects, which become important as densities
increase. It is particularly interesting to note however, that in this
system this process leads to no difference in the absolute
phylogenetic diversity of the different habitats, due to differences
in their species pool and therefore differences in the expected
phylogenetic structure of each habitat.
This could have implications for conservation. It is becoming
clear that phylogenetic diversity has consequences for ecosystem
functioning [51,52]. If so, reductions in phylogenetic diversity
could have negative effects that may be independent of the effects
of species richness. Indeed, one study found that urban areas
(assumed to be more disturbed) actually had higher species
diversity of plants but that phylogenetic diversity was lower .
This likely reduces the positive aspects of increased species
richness. Consistent with many other studies [17–19,21], I
demonstrated the ability of disturbance to decrease the phyloge-
netic diversity of an area, however, I also show that whether this
leads to an absolute difference in phylogenetic diversity between
disturbed and undisturbed habitats is dependant on the pool of
available species in each habitat. In this case, disturbed areas had
the potential for higher phylogenetic diversity than undisturbed
areas, but clustering at the plot level led to statistically
indistinguishable values for phylogenetic diversity in each habitat.
Factors that influence ecological succession may act in a biased
manner with respect to phylogeny, because of a correspondence
between phylogeny and ecological similarity. Therefore, phyloge-
netic information should be useful in understanding these forces.
In this study I found phylogenetic information could be used to get
a fuller picture of compositional changes in plant communities. In
particular, disturbed plant communities were more phylogeneti-
cally clustered than expected by chance, suggesting the action of
environmental filters on phylogenetically conserved traits. Impor-
tantly, this led to no difference in phylogenetic diversity between
disturbed and undisturbed plots, because the underlying species
pool for disturbed plots had a higher phylogenetic diversity. This
suggests that processes that structure communities can have
different effects on phylogenetic diversity at different scales, from
the regional to the plot level. This necessitates the careful choice of
null models when comparing phylogenetic diversity indices
amongst habitats. Analyzing differences in phylogenetic structure
and composition at different scales can lead to useful insights into
habitat differences in community composition.
delimited text file). Columns are species denoted by their binomial
latin name. Rows are the plots sampled. Value in each cell is the
number of quadrants in the plot the species was found in (0–4).
Found at: doi:10.1371/journal.pone.0007071.s001 (0.01 MB
Raw Data. Raw data used in the study (comma
format). Note: Thuja occidentalis not included.
Found at: doi:10.1371/journal.pone.0007071.s002 (0.00 MB
Phylogeny. Phylogeny file used in this study (in Newick
I would like to thank Peter Abrams for supervisory support and Anna
Simonsen for field assistance. Ann Zimmerman provided assistance and
granted permission for the use of KSR. Andrew MacDonald, Steven Hill,
Matthew Helmus, and Marc Cadotte provided valuable feedback on
earlier versions of the manuscript.
Conceived and designed the experiments: RD. Performed the experiments:
RD. Analyzed the data: RD. Wrote the paper: RD.
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