Journal of Applied Ecology 2016, 53, 1871–1879 doi: 10.1111/1365-2664.

12702

Species distribution models predict rare species

occurrences despite significant effects of landscape
context
J. L. McCune*
Department of Integrative Biology, University of Guelph, Science Complex, Guelph, ON N1G 2W1, Canada

Summary
1. The true status of many endangered plants is uncertain because the locations of all extant
populations are not known. Species distribution models (SDMs) can direct searches for addi-
tional populations, but habitat fragmentation may influence the distribution of rare species
more than climatic or edaphic factors in human-dominated landscapes. In this study, I test
the ability of SDMs to predict rare plant occurrences in a fragmented landscape and the
importance of predicted habitat suitability versus landscape context.
2. I built SDMs for eight rare woodland plants and assessed them using an independent data
set including plant community surveys of 51 sites. I used community data to determine
whether SDMs predict the right habitat type even when the target rare species was absent. I
then modelled rare species presence based on predicted habitat suitability, distance to the
nearest known population and the amount of forest habitat within 500 m of the site.
3. SDMs were effective for seven of the eight species, with the degree of predicted habitat
suitability positively related to species’ occurrence. I found new populations of four of the
eight species. However, the amount of forest habitat available in the vicinity of a plot was
also a positive predictor of rare plant occurrences. Among sites predicted to be suitable, the
distance to the nearest known population was the strongest predictor of rare plant occur-
rence.
4. Synthesis and applications. Species distribution models (SDMs) can effectively target
searches for populations of rare species even in human-dominated landscapes. Surveying the
plant community at sites predicted to be suitable can help to improve the SDM. SDMs used
in conjunction with data on landscape context can maximize the efficiency of searches for rare
species and show which species are restricted by dispersal limitation and habitat
fragmentation in addition to edaphic and climatic factors.
Key-words: associated species, dispersal limitation, disturbance, forest, habitat fragmenta-
tion, human-dominated landscapes, MAXENT, rare plants, species distribution model,
woodland

populations are likely present on privately owned land

Introduction
An important question for maintaining biodiversity in
human-dominated landscapes is whether rare species can
cope with disturbance and fragmentation. But for many
rare species we lack the basic data on population size,
locations and changes over time that we need to answer
it. Canada’s rare plant species are a prime example of
this. Data on the current and historical status of many of
these species are sparse or absent. Undocumented
*Correspondence author. E-mail: jmccune@uoguelph.ca
that has not been surveyed (Lovett-Doust et al. 2003).
The greatest threats to Canada’s endangered plant species
are residential and commercial development and recre-
ational activities (McCune et al. 2013), and thus, undis-
covered populations of rare plants are in danger of
inadvertent destruction by humans.
One way to improve our knowledge of the status of
rare species is to use species distribution models (SDMs)
to prioritize areas for field surveys. SDMs predict a spe-
cies’ distribution across space based on georeferenced
occurrence records and environmental predictors (Guisan

© 2016 The Author. Journal of Applied Ecology © 2016 British Ecological Society
1872 J. L. McCune
& Zimmermann 2000). Hundreds of papers involving
SDMs are published every year (Franklin 2013), and the
distributions of thousands of individual species have been
modelled (e.g. Kharouba et al. 2013). SDMs are used for
a broad range of applications, including forecasting range
shifts with climate change and invasions by introduced
species (Franklin 2013). SDMs also have important
applications to conservation, including reserve selection
(Guisan et al. 2013).
Several studies have used SDMs to predict habitat for
rare plant species (e.g. Engler, Guisan & Rechsteiner
2004; Bourg, McShea & Gill 2005; Guisan et al. 2006;
Williams et al. 2009; Le Lay et al. 2010). However, rare
species may be absent from suitable sites because of dis-
persal limitation, competition and historical factors
(Boetsch, Van Manen & Clark 2003; Gogol-Prokurat
2011). In human-dominated landscapes where habitat is
fragmented, the history of land use within and surround-
ing a habitat patch and its isolation from other patches
may determine occurrences to an equal or greater degree
than edaphic and climatic conditions (Rogers et al. 2009).
Several authors have pointed out the need to incorporate
landscape connectivity and/or dispersal into SDMs (e.g.
Franklin 2010; Folt^ete et al. 2012). Yet there have been
no studies that test the importance of climatic and
edaphic factors versus habitat fragmentation and dispersal
limitation for the distribution of rare plants by building
and testing SDMs in conjunction with data on the state
of the landscape.
In this study, I used SDMs to predict suitable habitat
for rare woodland plant species in southern Ontario,
Canada. Southern Ontario represents <1% of Canada’s
land area, but supports 35% of the human population
(Government of Ontario 2000). I chose eight rare plant
species that vary in their distribution, habitat specificity
and prevalence. I had two objectives: (i) to assess the util-
ity of SDMs for predicting suitable habitat for rare plants
with different range and habitat characteristics by using
multiple measures, including plant community data, and
(ii) to test the importance of predicted habitat suitability
(based only on geology, soils, climate and topography)
and landscape context for the probability of detecting
each species. I hypothesized that range-edge species and
those with more specialist habitat requirements would be
more accurately modelled by SDMs. If landscape context
has a role in determining rare plant distributions, then I
predicted that the presence of a species would be more
accurately modelled if the amount of forest on the sur-
rounding landscape and/or the distance to the nearest
known population were taken into account.
Materials and methods
THE STUDY REGION AND SPECIES
Southern Ontario was once dominated by mixed deciduous and
coniferous forests (Crins et al. 2009; Fig. 1). Current forest cover
© 2016 The Author. Journal of Applied Ecology © 2016 British Ecological Society, Journal of Applied Ecology, 53, 1871–1879
Fig. 1. The location of the study area in southern Ontario (inset,
shaded), and a close-up of the study area (shaded) showing the
Precambrian shield (crosshatched), the Niagara escarpment (thick
black line), three major cities (black stars) and the locations of 51
surveyed 1-ha grid squares (white dots).
ranges from 7 to 40% of pre-settlement cover, depending on the
county (Larson et al. 1999). The main land use is agriculture,
except for where the Precambrian shield extends southward, and
very shallow soils over the bedrock prevent intensive agriculture
(Crins et al. 2009; Fig. 1). The total extent of the study area is
approximately 11 million hectares, with elevation ranging from
20 to 575 m above sea level. The topography is gentle, except for
the Niagara escarpment, a thin line of limestone cliffs (Crins
et al. 2009; Fig. 1).
There are over 700 plant species ranked S1 (extremely rare, 1–5
known populations), S2 (very rare, 6–20 known populations) or
S3 (rare to uncommon, 21–80 known populations) (Oldham &
Brinker 2009). I chose eight of these species with different range
types, habitat specificity and rarity levels (Table 1). Many of
southern Ontario’s rare plant species are at the northern edge of
their range here, with the bulk of their distribution extending
south into the United States. I selected two species which have
the majority of their range in Ontario (Table 1). Distributions of
species are often more accurately predicted by SDMs at the range
edge, presumably because the species relies on particular environ-
mental conditions that are patchy near the edge of the range
(MacDougall & Loo 2002; Luoto et al. 2005).
The eight species also differ in their habitat specificity. For
example, the fern Asplenium scolopendrium grows only on the
rocky limestone substrates of the Niagara escarpment (Oldham &
Brinker 2009), whereas the orchid Cypripedium arietinum grows
in a wider range of habitats (Brzeskiewicz 2000; Blaney & Maze-
rolle 2007; Table 1). Habitat specialists are often more accurately
modelled than generalists because of their reliance on spatially
restricted environmental conditions (Hernandez et al. 2006; Le
Lay et al. 2010). All eight species are easy to recognize in the
field, and primarily associated with woodland habitats. I com-
piled a list of common associated species of each of the eight spe-
cies from the literature (Appendix S1 in Supporting Information).
BUILDING MODELS
I built SDMs for each species using MAXENT (Phillips, Anderson
& Schapire 2006; Elith et al. 2011), which performs as well or
better than other modelling methods (Hernandez et al. 2006; Wil-
liams et al. 2009). I gathered data on soils, topography, surficial
 Predicting rare species occurrences 1873

Table 1. Range characteristics and habitat preferences of the eight plant species. Status designations are special concern (SC), threatened
(THR) and endangered (END). Species without a status category have not yet been assessed. See text for S rank definitions. The final
column indicates the beta diversity of surveyed plots predicted to be suitable for each species, as estimated by the average Bray–Curtis
distance to the centroid of that group of plots. The beta diversity of all 51 plots was 46
15

Beta diversity of plots

% of range in predicted to be
Scientific name Status S rank Ontario Breadth of habitat suitable

Arisaema dracontium SC S3 <5 Medium (floodplain forests) 42
63

Asplenium scolopendrium SC S3 >50 Narrow (limestone, Niagara escarpment) 33
96
Chimaphila maculata END S1 <5 Narrow (dry sandy soil near Great Lakes) 37
08
Corallorhiza odontorhiza S2 <5 Narrow (dry sandy soil near Great Lakes) 31
88
Cornus florida END S2? <5 Wide (deciduous forest edges/understorey) 43
95
Cypripedium arietinum S3 >50 Wide (swamps or shallow soil over limestone) 45
27
Phegopteris hexagonoptera SC S3 <5 Medium (rich, moist, mature maple/beech forests) 43
06
Vaccinium stamineum THR S1 <5 Narrow (recently burned areas near Great Lakes) 33
11

geology and climatic factors (see Appendix S2), and converted
each variable to a 100 9 100 m grain size. I chose a set of 14
predictors that were minimally intercorrelated. I obtained georef-
erenced observation records for all eight target species from the
Ontario Ministry of Natural Resources and Forestry (OMNRF)
Natural Heritage Information Centre (NHIC). The records include
herbarium records, opportunistic sightings and purposeful
searches by biologists, and are represented by polygons which indi-
cate the spatial certainty of the observation. I eliminated all
records with an area of >100 m radius; 91% of the records were
from 1980 or later, with only one record from prior to 1958. High
spatial accuracy of records was the most important criterion for
of 2014, I surveyed 51 grid squares (Fig. 1), with the goal of
maximizing the variation in the range of habitat suitability pre-
dicted by the model, and distance from the nearest record of the
species. At each site, we used a global positioning system to
locate the centre of the grid square. We thoroughly searched each
square, with search times ranging from 3 to 6 person hours
depending on the vegetation and terrain. We recorded all vascu-
lar plant species present, and estimated the abundance of each
using a coarse 5-category scale.
STATISTICAL ANALYSES

inclusion, and given the relatively low number of records available,

I did not remove spatially accurate pre-1980 records, considering Standard model assessments
them to be good indicators of the topographic, geological, edaphic
MAXENT provides the AUC (area under a receiver operating char-
and climatic conditions in which the species could survive.
acteristic curve; see Fielding & Bell 1997) for training and test
I used MAXENT version 3.3.3 to model the distribution of each
data. I also calculated AUC, sensitivity (the proportion of pres-
species (https://www.cs.princeton.edu/  schapire/maxent/; Phil-
ences predicted correctly by the model) and specificity (the pro-
lips, Anderson & Schapire 2006). I excluded duplicate observa-
portion of absences predicted correctly by the model) using an
tion records from the same 100 9 100 m grid square, which
independent data set that was not used to build the SDMs. This
resulted in a total number of observations ranging from 5 to 295,
data set was a combination of records from the 51 forest surveys
depending on the species (Table 2). Although SDM accuracy can
plus records held by the NHIC that had not yet been incorpo-
decline when based on fewer than 30 records (Wisz et al. 2008),
rated into the official data base. I used only records with ≤100 m
MAXENT has been shown to perform well even with sample sizes
positional accuracy, and eliminated any records in the same grid
as low as 5 (Hernandez et al. 2006; Pearson et al. 2007). For each
square as a record used to build the SDM. This data set also
species, I built seven models with slightly different MAXENT set-
included a few absence records resulting from unsuccessful tar-
tings, each time randomly excluding 25% of the observation
geted searches by NHIC staff for a particular species. These
records to use as test data, repeating this subsampling 10 times
absences are biased, because targeted searches are performed only
and taking the average of all 10 replicates (Appendix S2). I
in areas that seem to have suitable habitat according to expert
selected the best model based on minimal predicted area (MPA;
botanists. However, the bulk of the absences for each species
Engler, Guisan & Rechsteiner 2004). I used the cumulative model
resulted from my field surveys, which include sites with both suit-
output, which avoids assumptions about species prevalence (Phil-
able and unsuitable habitats; therefore, I consider the absences in
lips, Anderson & Schapire 2006; Merow, Smith & Silander 2013).
combination to be a relatively unbiased sample of the region. I
The cumulative value at each grid square ranges from 0 to 100%,
eliminated any absences that were in the same grid square as a
with 100% being the most suitable. I set the threshold for pre-
presence, which represent re-surveys of areas formerly known to
dicting suitable habitat to the minimum value resulting in the
support a population of the species. I consider these to be false
correct prediction of 90% of all records used to build the model
absences. I calculated AUC, sensitivity and specificity for the
(i.e. a 10% omission rate) and selected the model that predicted
independent data set using the ‘dismo’ package in R (R Founda-
the lowest percentage of the study area to be suitable.
tion for Statistical Computing, Vienna, Austria).

FIELD SAMPLING
I randomly selected 100 forested grid squares predicted to be suit-
able for each species, stratified by the distance to the nearest
observation used to build the model. In the spring and summer
Plant community and landscape analyses
To characterize the plant community composition of the sur-
veyed grid squares, I converted the coarse abundance scale used

© 2016 The Author. Journal of Applied Ecology © 2016 British Ecological Society, Journal of Applied Ecology, 53, 1871–1879
1874 J. L. McCune

in the field surveys to an ordinal scale from 1 (very rare) to 5

Specificity
model. Model threshold is the threshold of habitat suitability (MAXENT’s cumulative output) above which a grid square is predicted to be suitable. See text for explanations of AUC, sensitivity
Table 2. Summary of species distribution model (SDM) characteristics and evaluation measures. MPA (minimal predicted area) is the percentage of the study area predicted suitable by the best
(dominant) and ordinated all squares using non-metric multidi-

(%)
mensional scaling (NMDS) based on Bray–Curtis similarity

62
86
82
92
62
76
49
94
(McCune & Grace 2002), excluding the target species. If the
SDMs were useful, I expected that species with narrow habitat
preferences would have lower beta diversity among plots pre-
Sensitivity dicted suitable compared to species with wide habitat tolerances.
(%) To test this, I calculated the multivariate dispersion (average

NA
74
60
78
14
68
91
22
community similarity) for the 51 sites as a whole, for the group
of sites predicted to be suitable for each target species where the
species was absent, and for the group of sites predicted to be
0
7594
0
8908
0
8707
0
8739
0
7700
0
8908
0
4172
NA
suitable for each target species in which the species was found
AUC

(Anderson, Ellingsen & McArdle 2006). I tested for significant

differences in community dispersion using a distance-based test
for homogeneity of multivariate dispersions (PERMDISP;
Anderson, Ellingsen & McArdle 2006) in the program PRIMER
absences)
absences)
absences)
absences)
absences)
absences)
absences)
absences)
No. independent

(Clarke & Gorley 2015). I also compared the beta diversity

among suitable sites with and without the target species present
using the same method.
(55
(49
(49
(51
(53
(41
(53
(51
records

I compared the relative abundance of associated species in

69
58
58

64
62
51
142

131

squares that were predicted suitable versus unsuitable using Wil-

coxon rank-sum tests. Then, I used generalized linear models
Independent data

(glm) with a binomial link to model suitable versus unsuitable

field searches

sites based on relative abundance of associates (see

ratio from

Appendix S3).
Success

I also calculated the relative abundance of disturbance-asso-

0/3

0/3
2/17
3/10
2/11

5/20
0/10
0/24

ciated species in each surveyed square. I designated a species as

disturbance-associated if its habitat description in the Michigan
Flora (Reznicek, Voss & Walters 2011) included one or more of
the terms ‘disturbed places’, ‘roadsides’, ‘railroads’, ‘openings and
threshold

trails’, ‘fencerows’, ‘powerline clearings’, ‘ditches and swales’ or

Model

29
88
26
09
59
95

27
95
27
78
63
83
70
5
21
2

‘meadows and pastures’. Disturbance-associated species tend to

colonize sites with less natural vegetation on the surrounding
landscape (e.g. Vallet et al. 2010; McCune & Vellend 2015). I
used ArcGIS to calculate the total area forested within 500 m of
MPA

0
81
0
47
0
08
0
27
1
22
3
60
2
12
0
05

each surveyed plot, and then used a Spearman rank correlation

(%)

test to determine whether there was a significant correlation

between forested area and the relative abundance of disturbance-
associated species.
0
9743
0
9861
0
9453
0
6737
0
9726
0
9454
0
9276
0
9742
AUC
(test)

Assessing the relative importance of distance and

landscape disturbance
0
9904
0
9926
0
9958
0
9924
0
9841
0
9662
0
9862
0
9988
(train)
AUC

Using the independent data set for each species, I built a glm of
species presence/absence based on the habitat suitability predicted
by the MAXENT model and the total area of forest within 500 m
Model building

of the square. I did not include distance to the nearest known

No. records

population in these models because this variable is highly corre-

lated with predicted habitat suitability. I used spline correlograms
144

295
73

15

77
38
5

to check for spatial autocorrelation in the model residuals. If I

detected spatial autocorrelation, I incorporated a spatial autoco-
variate in a revised model (Dormann 2007; Bardos, Guillera-
Arroita & Wintle 2015). For each species, I compared a model
Phegopteris hexagonoptera
Asplenium scolopendrium

Corallorhiza odontorhiza

with intercept only to models with habitat suitability only, forest

Cypripedium arietinum

Vaccinium stamineum
Arisaema dracontium

area only, both habitat suitability and forest area, and both pre-
Chimaphila maculata

dictors as well as an interaction term. I considered a variable to

be significantly related to species presence/absence when the dif-
and specificity

Cornus florida

ference in AIC between a model with intercept only and a model

including the factor was >5, which corresponds to strength of evi-
Species

dence at least 12 times stronger than the alternative model (Burn-

ham, Anderson & Huyvaert 2011).

© 2016 The Author. Journal of Applied Ecology © 2016 British Ecological Society, Journal of Applied Ecology, 53, 1871–1879
 Predicting rare species occurrences 1875

To examine the importance of distance from the nearest known

2
(a) Asplenium scolopendrium
population, I examined the independent data for grid squares
predicted to be suitable only. In this subset of the data, distance
and habitat suitability are not highly correlated (r ranges from

1
0
21 to 0
51). I built logistic models relating species presence/ab-
sence to combinations of habitat suitability, distance and forest
area, plus a spatial autocovariate when necessary.

NMDS2
Logistic models were built in R, using package ‘NCF’ for spline

0
correlograms and ‘SPDEP’ for preparing spatial autocovariates.

−1
Results

STANDARD MODEL TESTS

−2
AUC values >0
90 generally indicate a very useful model
(Swets 1988). All species except C. odontorhiza had high −2 −1 0 1 2
AUC values based on the subset of records withheld from NMDS1
the training data (Table 2). The proportion of the study
area predicted suitable for each species (MPA) ranged

2
(b) Cornus florida
from 0
05% to 3
6%, and generally corresponded to the
prevalence and distribution of the species. For example,
C. maculata (MPA = 0
08%) had only 15 presence
1

records mainly located in two very small regions within

the study area, whereas C. arietinum (MPA = 3
6%) has
NMDS2

77 presence records spread across a wide area.

0

Appendix S4 shows a map for each species.

Field surveys led to the discovery of new populations
of four species, with the highest success for A. scolopen-
−1

drium, which was present at three of the ten survey sites

predicted suitable (Table 2). I did not find any target spe- Not suitable, absent
cies in a square that was not predicted suitable. I was able Suitable, absent
to search only four and three squares, respectively, for Suitable, present
−2

C. odontorhiza and V. stamineum, and did not find these

species at any sites. The NHIC held no additional occur-
rence records for V. stamineum, and therefore, I was
unable to carry out an independent test of the model for
this species beyond the three grid squares I surveyed.
For all species, AUC based on the independent data set
was lower than AUC for the data used to build the SDM
(Table 2), which is a common finding (e.g. Elith & Burgman
2002). However, all species except for P. hexagonoptera had
independent AUC values above 0
7, which is the threshold
for a ‘useful’ model (Swets 1988). Sensitivity was good, with
a majority of presences being predicted suitable by the
model, except for C. odontorhiza (14%) and
P. hexagonoptera (22%) (Table 2). The majority of inde-
pendent absences were correctly predicted by the models for
all species except for P. hexagonoptera (Table 2).
PLANT COMMUNITY DATA
The relative abundance of associated species was signifi-
cantly higher in grid squares predicted to be suitable by
the SDM for five of the eight species, although there was
a lot of variation for both suitable and unsuitable sites
(Appendix S3). Logistic models accounting for spatial
autocorrelation showed the relative abundance of
−2 −1 0 1 2
NMDS1
Fig. 2. Non-metric multidimensional scaling (NMDS) ordination
of all 51 surveyed grid squares in plant species space based on
the Bray–Curtis dissimilarity measure. Stress in three dimensions
is 13. (a) Grid squares predicted suitable and unsuitable, with
and without the species present, for habitat specialist Asplenium
scolopendrium. (b) Grid squares predicted suitable and unsuitable,
with and without the species present, for habitat generalist
Cornus florida.
associates to be significantly related to the predicted habi-
tat suitability for only two species (Appendix S3).
The beta diversity of grid squares predicted to be suit-
able for each species generally matched habitat breadth,
whereby species with a narrow habitat range had lower
beta diversity among sites predicted to be suitable than did
habitat generalists (Table 1; Fig. 2). The sites where a tar-
get species was found tended to be clustered together in
plant community space, with a lower level of beta diversity
than all suitable plots as a whole (Fig. 2). This was true
regardless of the habitat breadth of the species. Compar-
isons between the beta diversity among suitable sites with
and without each target species were not always statisti-
cally significant, but in these cases there were few sites with

© 2016 The Author. Journal of Applied Ecology © 2016 British Ecological Society, Journal of Applied Ecology, 53, 1871–1879
1876 J. L. McCune
Arisaema dracontium
80 100
60
40
20
Habitat suitability (%)
0
abs pres
Cornus florida
80 100
60
40
20
0
abs pres
Fig. 3. Habitat suitability (based on MAXENT’s cumulative output) versus presence (pres) or absence (abs) of each species in the indepen-
dent data set. The data is indicated in grey, with open dots for sites with <40-ha total forest cover within 500 m and closed dots for sites
with >40-ha total forest cover within 500 m. Black dots indicate the mean habitat suitability for low forest (open dots, dashed lines) and
high forest (closed dots, solid lines). Grey bars indicate the overall mean for both forest categories.
the species present, providing insufficient power to detect a
significant difference by permutation tests (Appendix S5).
THE IMPORTANCE OF LANDSCAPE CONTEXT
The total area of forest within 500 m of a site was negatively
correlated with the relative abundance of disturbance-asso-
ciated species (Spearman’s r = 0
48, P = 0
00043). For the
independent occurrence data, predicted habitat suitability
was included in the best model of species presence/absence
for all species except A. scolopendrium. The other species
showed a positive relationship between predicted habitat
suitability and presence except for P. hexagonoptera, for
which habitat suitability was a negative predictor of pres-
ence (Fig. 3, Appendix S6). The area of forest within 500 m
was also an important predictor of presence for Chimaphila
maculata and Corallorhiza odontorhiza – in fact neither spe-
cies was ever present in sites with surrounding forest area
lower than 40 ha (Fig. 3). There was an interaction between
habitat suitability and forest area for three species: A. dra-
contium, C. florida and P. hexagonoptera. For the first two,
habitat suitability was a stronger predictor of species pres-
ence in sites with high forest area within 500 m, whereas for
P. hexagonoptera, the negative relationship between habitat
suitability and species presence became even stronger in
sites with low forest area (Fig. 3).
For sites above the threshold for habitat suitability, the
degree of habitat suitability was no longer a good predic-
tor of species presence for any species. The strongest pre-
dictor of species presence at suitable sites was the distance
from the nearest known occurrence of the species, with
sites closer to known records having a much higher prob-
ability of the species being present. This was true for all
© 2016 The Author. Journal of Applied Ecology © 2016 British Ecological Society, Journal of Applied Ecology, 53, 1871–1879
Asplenium scolopendrium Chimaphila maculata Corallorhiza odontorhiza
abs pres abs pres abs pres
Cypripedium arietinum Phegopteris hexagonoptera
<40-ha forest within 500 m
>40-ha forest within 500 m
abs pres abs pres
species except for C. odontorhiza and C. arietinum (Fig. 4;
Appendix S6). There was a strong positive influence of
total forest area within 500 m on the probability of
presence for three species: A. dracontium, C. maculata and
P. hexagonoptera (Appendix S6).
Discussion
SDMs based on presence-only records and data on soils,
geology, topography and climate effectively predicted the
distributions of seven of these eight rare woodland plants.
While independent test data yielded a low sensitivity
(14%) for C. odontorhiza, the AUC value was quite high
(Table 2), suggesting that the choice of threshold for suit-
ability was ineffective. Pearson et al. (2007) suggest lower-
ing the habitat suitability threshold to 0% omission when
the number of records is very low, as in this case. When I
did this, the sensitivity based on the independent data set
improved to 86%, while the specificity was still good at
76%. I used this new threshold for the subsequent model
tests for this species.
Forest surveys based on these SDMs resulted in the dis-
covery of new populations of four of the eight species,
even though only 51 sites were searched. Although the
success rate was relatively low – ranging from 12% to
30% of sites predicted to be suitable – this is a common
finding for rare species (MacDougall & Loo 2002; Wil-
liams et al. 2009), and is an improvement over the 0%
discovery rate at sites where the habitat was not predicted
suitable. Sites predicted to be suitable tended to have a
higher relative abundance of common associates of the
target rare plant. However, there was a large amount of
variation between sites. This is to be expected, especially
 Predicting rare species occurrences 1877

Arisaema dracontium Asplenium scolopendrium Chimaphila maculata Corallorhiza odontorhiza

60 65 70 75 80 85
90

80
70
70

70
50
50
Habitat suitability (%)

60
30
30

0 5 10 15 20 25 30 0 5 10 15 20 25 30 0 5 10 15 0 5 10 15 20 25 30

Cornus florida Cypripedium arietinum Phegopteris hexagonoptera

100

Species absent
90

90
Species present
80

70

70
60

50

50
40

30
20

30
0 5 10 15 0 10 20 30 40 0 5 10 15 20 25 30
Distance to nearest record (km)

Fig. 4. Habitat suitability (based on MAXENT’s cumulative output) versus distance to the nearest record used to build the SDM for the
independent data set, showing sites with habitat suitability above the suitability threshold only. Distance is negatively related to species
presence for all species except C. odontorhiza and C. arietinum. Note that the scale of axes may differ by species.

for species with a wide habitat breadth like C. florida,
which has a wide range of common species associated
with it in different contexts. However, this variation in
the relative abundance of associates may also reflect habi-
tat characteristics that are not well represented by the pre-
dictors used in the SDMs. Factors like historical grazing,
successional stage and canopy type that are not accounted
for in the models are likely reflected in this high variabil-
ity of associate abundance.
Plant community diversity was a good representative of
habitat breadth, with the beta diversity of suitable sites gen-
erally corresponding to the habitat breadth of each species.
Habitat specialists did not have qualitatively more useful
SDMs than species with wider habitat breadth. Similarly,
range-edge species were not more effectively modelled than
species with most of their range in southern Ontario. Elith
& Burgman (2002) found similar results for eight rare plants
in Australia, for which SDM utility was not associated with
the species’ level of rarity or range within the study region.
The higher community similarity of sites where a species
was found compared to all suitable sites suggests that there
was an important environmental factor or factors not
accounted for by the variables included in the SDM. These
are probably factors related to canopy cover, successional
state or disturbance history. An indicator species analysis
of suitable sites with and without the target species sup-
ports this theory for two of the target species
(Appendix S1). Suitable sites for A. scolopendrium that
lacked the species tended to include the conifer Thuja occi-
dentalis. Asplenium scolopendrium is reportedly never found
beneath conifers (Cinquemani Kuehn & Leopold 1992).
Other studies have found vegetation type to be an impor-
tant predictor of habitat suitability for some rare plants
(e.g. Bourg, McShea & Gill 2005; Williams et al. 2009;
Gogol-Prokurat 2011). Incorporating canopy type into the
model would likely improve predictive power for
A. scolopendrium and perhaps for other species as well. In
the case of C. maculata, unoccupied suitable sites tended to
have higher frequency and abundance of the shrubs Lin-
dera benzoin and Sambucus racemosa. Both flourish in gaps
caused by canopy disturbance (Cipollini, Wallace-Senft &
Whigham 1994; Reznicek, Voss & Walters 2011). Data on
disturbance history could therefore improve SDMs for
C. maculata, as it has for rare plants in other regions
(Bourg, McShea & Gill 2005; Gogol-Prokurat 2011). How-
ever, information on the frequency or intensity of canopy
disturbance is often not readily available as broadscale
geospatial data, and is probably best incorporated as a fil-
ter after SDM building, during site selection in the field.
It is critical to assess whether predicted habitat suitability
is actually proportional to the probability of a species’ pres-
ence when using SDMs in conservation-related applications
(Gogol-Prokurat 2011; Merow, Smith & Silander 2013). In
this study, habitat suitability as predicted by MAXENT’s
cumulative output was positively related to the probability
of species presence for all species except A. scolopendrium
and P. hexagonoptera. For A. scolopendrium, this may be
an artefact of correcting for spatial autocorrelation.
Because this fern specializes on the spatially limited lime-
stone substrate of the Niagara escarpment, both habitat
suitability and occurrence records tend to be strongly spa-
tially correlated. By ‘correcting’ for this, the relationship
between the two may have been obscured (e.g. Dormann
2007). Indeed, when I built a glm without the spatial auto-
covariate, habitat suitability was an important predictor of
the species’ presence (results not shown).
For P. hexagonoptera, predicted habitat suitability was a
negative predictor of the species’ presence (Fig. 3). While
the AUC in the model building stage was very high, the
model performed very poorly for the independent data set

© 2016 The Author. Journal of Applied Ecology © 2016 British Ecological Society, Journal of Applied Ecology, 53, 1871–1879
1878 J. L. McCune
(Table 2). There are a number of possible explanations.
First, perhaps the model failed to accurately characterize
the species’ habitat requirements because important envi-
ronmental factors were missing. Second, the species may
have been missed during site surveys. However, this fern is
a perennial with distinctive fronds which emerge in late
May and persist until autumn, and is unlikely to be missed
in careful surveys, and there were also many errors of the
opposite kind, where the species was present in areas pre-
dicted to be unsuitable. Finally, it could be that
P. hexagonoptera is not currently in equilibrium with the
environment because of population fluctuations resulting
from high levels of human disturbance and/or stochastic
extirpations of small populations and temporary survival
of ‘sink’ populations in unsuitable areas (MacDougall &
Loo 2002; Le Lay et al. 2010). This is the most likely expla-
nation for the poor model performance. Of 71 total occur-
rences of this species in Ontario, only 21 have been
confirmed in the last 20 years, and searches of known loca-
tions have frequently been negative (van Overbeeke, Jalava
& Donley 2013). The inability of the SDM to predict pres-
ence and absence of this species may be a further indication
that it is on its way to extirpation in southern Ontario.
In addition to habitat suitability based on environmen-
tal predictors, the amount of forest cover within 500 m of
a site is an important determinant of rare woodland plant
species presence in this landscape. The area of forest
within 500 m was negatively correlated with the relative
abundance of disturbance-associated species in the 51 sur-
veyed sites, suggesting that rare plants are more likely to
occur in areas of lower disturbance. However, the amount
of forest in the vicinity of a site also indicates degree of
isolation from other potentially suitable patches, and it is
difficult to tease apart the relative influence of disturbance
and fragmentation, per se. Nevertheless, there is a higher
likelihood of finding these rare plants in areas with more
intact forest, and these areas should be prioritized for
field surveys. Boetsch, Van Manen & Clark (2003) found
a very similar pattern for Cardamine clematitis, which was
absent in suitable patches <40 ha in size.
For sites predicted to have suitable habitat, the degree
of habitat suitability was not an important predictor of
presence for any species. Once over the threshold, a site
with cumulative output of 50% is just as likely to contain
the species as one with 100%. For this subset of sites, the
most important predictor of species presence was the dis-
tance to the nearest known population, independent of
relative habitat suitability and spatial autocorrelation.
Interestingly, this was true for all species except C. ariet-
inum and C. odontorhiza, both of which are orchids with
tiny, windblown seeds. However, C. maculata and the two
fern species also have extremely light and small propag-
ules, so the importance of isolation from other popula-
tions is not entirely predictable based on propagule size.
Nevertheless, this evidence supports the hypothesis that
dispersal limitation plays a strong role in determining the
distributions of some rare plants on this landscape.
© 2016 The Author. Journal of Applied Ecology © 2016 British Ecological Society, Journal of Applied Ecology, 53, 1871–1879
Conclusions
The conservation of rare species relies first on accurate
knowledge of their current distribution and status. This
study has shown that even in fragmented, human-domi-
nated landscapes, SDMs based on climatic and edaphic
factors can be effective tools to prioritize areas for field
surveys. In addition, by ground-testing SDM predictions
in conjunction with plant community and landscape con-
text data, conservation biologists can determine which
environmental variables could improve SDM accuracy,
and which rare species may be most affected by landscape
context and/or dispersal limitation.
Acknowledgements
K. Tisshaw and M. Strub were excellent field assistants. M. Oldham
advised me on the selection of plant species and assisted with plant identi-
fication. C. Lacroix also helped with species identifications. The OMNRF
NHIC provided location data for rare plant populations. The Canadian
Forest Service provided climate data. The Bruce Trail Association, the
Grand River Conservation Authority, the Hamilton Naturalists Club, the
Long Point Basin Land Trust and 36 private landowners gave permission
to access land. A. MacDougall and two anonymous reviewers provided
helpful comments on the manuscript. This research was funded by the
Liber Ero fellowship Programme.
Data accessibility
Species occurrence records: available from the Natural Heritage
Information Centre of Ontario (nhicrequests@ontario.ca). Envi-
ronmental data (topography, geology, soils, climate): see
Appendix S2. Plant community and landscape data for the 51
surveyed sites: see Appendices S7 and S8. Independent occurrence
records with associated landscape data: see Appendices S9 and
S10.
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Received 14 February 2016; accepted 16 May 2016
Handling Editor: Christopher Baraloto
Supporting Information
Additional Supporting Information may be found in the online version
of this article.
Appendix S1. Species descriptions, associated species, and indica-
tor species analysis results.
Appendix S2. Details of MAXENT modelling, including environ-
mental data sources.
Appendix S3. Associated species model methods and results.
Appendix S4. Maps for each species showing the results of the
MAXENT model.
Appendix S5. PERMDISP results.
Appendix S6. glm results.
Appendix S7. Plant community and landscape data for the 51
surveyed sites.
Appendix S8. Metadata for Appendix S7.
Appendix S9. All independent occurrence records with associated
landscape data.
Appendix S10. Metadata for Appendix S9.