Ecography 35: 879–888, 2012

doi: 10.1111/j.1600-0587.2011.07138.x
© 2012 The Authors. Ecography © 2012 Nordic Society Oikos
Subject Editor: Alexandre Diniz-Filho. Accepted 19 December 2011

A new method for dealing with residual spatial autocorrelation in

species distribution models

Beth Crase, Adam C. Liedloff and Brendan A. Wintle

B. Crase (beth.crase@nt.gov.au) and B. A. Wintle, School of Botany, The Univ. of Melbourne, Parkville, VIC 3010, Australia. – A. C. Liedloff,
CSIRO Ecosystem Sciences, Berrimah, NT 0828, Australia.

Species distribution modelling (SDM) is a widely used tool and has many applications in ecology and conservation biology.
Spatial autocorrelation (SAC), a pattern in which observations are related to one another by their geographic distance, is
common in georeferenced ecological data. SAC in the residuals of SDMs violates the ‘independent errors’ assumption
required to justify the use of statistical models in modelling species’ distributions. The autologistic modelling approach
accounts for SAC by including an additional term (the autocovariate) representing the similarity between the value of the
response variable at a location and neighbouring locations. However, autologistic models have been found to introduce
bias in the estimation of parameters describing the influence of explanatory variables on habitat occupancy. To address
this problem we developed an extension to the autologistic approach by calculating the autocovariate on SAC in residuals
(the RAC approach). Performance of the new approach was tested on simulated data with a known spatial structure and
on strongly autocorrelated mangrove species’ distribution data collected in northern Australia. The RAC approach was
implemented as generalized linear models (GLMs) and boosted regression tree (BRT) models. We found that the BRT
models with only environmental explanatory variables can account for some SAC, but applying the standard autologistic or
RAC approaches further reduced SAC in model residuals and substantially improved model predictive performance. The
RAC approach showed stronger inferential performance than the standard autologistic approach, as parameter estimates
were more accurate and statistically significant variables were accurately identified. The new RAC approach presented here
has the potential to account for spatial autocorrelation while maintaining strong predictive and inferential performance,
and can be implemented across a range of modelling approaches.

Species distribution models (SDMs) relate species distribu-
tion data as such abundance, occurrence (presence only)
or presence/absence to environmental characteristics (Elith
and Leathwick 2009). They have been applied extensively
in conservation planning and management, for predicting
range shifts in response to climate change (Bakkenes et al.
2002, Peterson et al. 2002, Midgley et al. 2003, Thomas
et al. 2004), and in invasive species management, disease
mapping and evolutionary biology (Austin 2002, Miller
et al. 2004, Araújo and New 2007). Such models have two
broad applications, firstly to facilitate an understanding of
the variables influencing species distribution (inference);
and secondly, for predicting a species’ spatial distribution.
Accurate predictive ability of models depends on the use of
sound ecological rationale and robust variable selection dur-
ing model building. The modelling framework applied to
the development of SDMs should ideally produce models
that perform well for both explanation and prediction.
SDMs use spatially referenced observations of species
occurrence as the dependent variable in the modelling pro-
cess. Most species observation data exhibit spatial autocor-
relation (Lennon 2000). Spatial autocorrelation (SAC) is a
pattern in which observations are related to one another by
the geographic distance between the observation (Legendre
and Fortin 1989, Fortin and Dale 2005). When SAC is posi-
tive, locations close to each other exhibit more similar val-
ues than those further apart. The presence of SAC in model
residuals violates the assumption of independent and identi-
cally distributed errors and can inflate type I errors (Legendre
1993, Kühn 2007). This can lead to the selection of unim-
portant explanatory variables and poorly estimated parameters
(regression coefficients) in SDMs (Lennon 2000, Dormann
2007a). This is an important issue in ecology as autocorre-
lation is a general property of ecological variables measured
over geographic space (Legendre and Legendre 1998).
Several methods have been developed to account for the
effects of SAC and can be used to model species distributions
(reviewed by Keitt et al. 2002, Dormann et al. 2007). The
autologistic approach is widely applied (Dormann 2007b)
and accounts for SAC by including an additional term in
the model (the autocovariate) to represent the influence
of neighbouring observations (Besag 1972, Augustin et al.
1996). This autocovariate specifies the relationship between
the value of the observation at a location and those at neigh-
bouring locations. Autologistic models have good predictive
performance in comparison to models that do not account

879
for SAC (Hoeting et al. 2000, Wintle and Bardos 2006,
Betts 2009), however, parameter estimates can be biased
(Dormann 2007b, Dormann et al. 2007), potentially dis-
torting inference.
Simultaneous autoregressive (SAR) models and general-
ized estimating equations (GEE) are alternative approaches
for dealing with SAC and use an autocovariate to represent
only the portion of spatial structure in the response vari-
able that is not explained by the environmental explanatory
variables (Carl and Kühn 2007, Dormann et al. 2007). That
is, the autocovariate specifies the relationship between the
value of the residuals at each location and those at neigh-
bouring locations. When analysing simulated data these
approaches produced less biased parameter estimates than
the autologistic approach (Dormann et al. 2007). The way
the autocovariate is calculated for the SAR and GEE
approaches is more congruent with theory because it is the
SAC remaining in model residuals that violates assumptions
of statistical model, not SAC in the response variable per se
(Legendre 1993).
However, SAR and GEE models are more complex
to apply than the autologistic approach. The autologis-
tic approach is usually applied within a GLM framework
(Augustin et al. 1996, Luoto et al. 2001, Betts et al. 2006,
Wintle and Bardos 2006). In contrast to SAR and GEE
models, GLMs are widely applied in ecology and other dis-
ciplines, their use is supported by numerous textbooks and
software packages and they are easy to implement and inter-
pret. In addition, the autologistic approach has the potential
to be implemented across a range of modelling techniques,
such as tree-based machine learning methods including
boosted regression trees (BRT) and Random Forests. These
methods have been shown to model complex relationships
and interactions between variables, leading to strong predic-
tive performance (Breiman 2001, Elith et al. 2006, De’ath
2007). Tree-based learning methods could be a useful tool
for modelling spatially autocorrelated data (Hothorn et al.
2011), as they may capture complex structures within the
data that simpler modelling approaches may miss (Elith and
Graham 2009).
Given that virtually all spatially explicit ecological data-
sets contain SAC (Lennon 2000), it is important that species
distribution modelling methods can account for the spatial
autocorrelation that cannot be attributed to the spatial struc-
turing of predictor variables included in the SDMs. SDMs
accounting for SAC should have strong predictive and infer-
ential performance, be straight forward to apply and able to
be implemented across a range of modelling approaches. In
this paper we extend the autologistic approach by fitting an
autocovariate derived from model residuals instead of directly
from the response variable. This combines the strengths of
SAR and GEE approaches with the accessibility of the autol-
ogistic approach. We compare predictive and inferential per-
formance of three models implemented within GLM and
BRT frameworks. In the first model (environment only),
explanatory variables are used to model the occurrence of the
focal species; in the second model (standard autologistic),
autocovariates derived directly from the response variable are
included as well as the environmental variables; and for the
third model (residuals autocovariate, RAC), autocovariates
derived from the residuals of an environment only model
880
plus the environmental explanatory variables are included.
For both BRT and GLM, the three modelling strategies are
compared on the basis of their predictive power, their infer-
ential performance and their ability to reduce residual SAC.
Methods
Datasets
Two datasets with Bernoulli distributed observation data
(presence/absence), one simulated and the other derived
from field mapping of mangrove tree species were used to
illustrate and evaluate alternative approaches to modelling
autocorrelated species distribution data. The first dataset
was simulated by Dormann et al. (2007) and used to com-
pare the performance of several spatial regression modelling
methods including spatial eigenvector mapping, autoregres-
sive models (e.g. SAR), generalized linear mixed models
and generalized estimating equations. The distribution of
the virtual species (called ‘Snouter’) was simulated ten times
across a grid of 1108 cells based on a known linear response
to an environmental variable (rain) and a spatially correlated
error structure. Two explanatory variables, one informative
(rain) and the other not (djungle) were used to model the
distribution of the virtual species. The uninformative djun-
gle variable was used to test the frequency with which the
various modelling methods made type I inferential errors.
For detailed methodology refer to (Dormann et al. 2007).
The second dataset provided the mapped distribution of
three mangrove species (Sonneratia alba, Ceriops tagal and
Rhizophora stylosa) along the Elizabeth River in Darwin
Harbour, northern Australia (Brocklehurst and Edmeades
1996). The presence or absence of each species (the response
variable) was represented as a binary map of 25 by 25 m grid
cells over an area of 8  8 km (a total of 102 400 cells). Three
explanatory variables (elevation, distance to water and dis-
tance to harbour) were used as independent variables in our
regression models of mangrove species distribution. These
variables are correlated with soil physicochemical gradients
including salinity, nitrogen, phosphorous and sulphide, and
are used as proxies for these gradients (Bunt et al. 1982,
Boto and Wellington 1983, Ball 1998, McKee et al. 2002).
Elevation was used as a proxy for inundation frequency, soil
nitrogen, phosphorous and sulphide (Boto and Wellington
1983, Ball 1998, Matthijs et al. 1999) and was derived from
a digital elevation model (DEM derived from 1:25 000
contours captured at vertical intervals of 5 m). Distance to
nearest water represents gradients in salinity, nitrogen, phos-
phorous, sulphide and inundation frequency and duration
(Boto and Wellington 1983, Matthijs et al. 1999, McKee
et al. 2002). Distance to the outer harbour provided a
proxy for the salinity of inundating water (Bunt et al. 1982,
Williams et al. 2006). Distance to water and distance to the
outer harbour were generated from a coastal map of Darwin
harbour (scale 1: 25 000; resolution 12.5 m).
Modelling approach
Three classes of models were considered. First, an envi-
ronment only model that does not explicitly account for
SAC; second, the standard autologistic model, an approach
commonly applied in ecological studies (Dormann 2007a)
that includes an additional autocovariate representing SAC
in the response variable; and finally, a new approach that
utilizes an autocovariate derived from the residuals of an
environment only model, termed a residuals autocovari-
ate (RAC) model. The only difference between these three
classes of models is whether or not an autocovariate term is
included and the way the term is derived. The environmental
explanatory variables are identical in all models. The models
in each class (environment only, standard autologistic, and
RAC) were implemented with a GLM and BRT approach.
Generalized linear modelling is an approach where the
response variable is related to explanatory variables via a link
function (McCullagh and Nelder 1983). A linear model
combining the explanatory variables is fitted to the observed
values of the response variable. In this study we have a value
for the response variable for each cell (location) and test
how accurate the models are by comparing the modelled
and observed values. The linear predictor, Xb, consists of a
matrix of the explanatory variables X, and a vector of associ-
ated parameters b. The linear predictor is related to the esti-
mated (modelled) value E(Y) via a link function g as
E(Y)  m  g21(Xb) (1)
where m is the mean of the distribution of the predicted value
of the response variable.
The link function relates the mean of the response vari-
able to the linear predictor, and as the datasets used in this
study are binary with a Bernoulli distribution, a logit link
function was used (McCullagh and Nelder 1983), such that
Xb  ln(m/(12m)) (2)
The GLMs were implemented considering only linear
relationships between the environmental explanatory vari-
ables and the response variable. The analyses were per-
formed using the statistical package R (ver. 2.11.1; R Core
Development Team).
Boosted regression tree (BRT) models were also used to
relate the occurrence of the target species to the explana-
tory variables (Breiman et al. 1984, Friedman et al. 2000).
BRT models function by combining two algorithms, the
first generates trees by recursive binary splits, with explana-
tory variables and split points (nodes) selected to minimize
prediction errors. The second algorithm, called boost-
ing, combines many trees in a forward stagewise process,
by selecting, at each step, the tree that maximises reduction
in deviance (De’ath 2007). BRT models were implemented
with a tree complexity of three (i.e. each tree has three
nodes) enabling simple interactions between variables to be
captured. A 10-fold cross validation procedure was used to
determine the optimum number of trees to be fitted to the
BRT model and the learning rate was set to ensure that at
least 1000 trees were produced during the fitting process,
as recommended by Elith et al. (2008). For more a detailed
explanation of these terms and more information on the
BRT fitting procedure refer to Elith et al. (2008). BRT mod-
els were developed using the R-package ‘gbm’ (Ridgeway
2010), and the custom functions of Elith et al. (2008).
Environment only model
The environment only model was fitted with the environ-
mental explanatory variables and spatial autocorrelation
was not considered. Therefore, variation in the probability
of occurrence of the target species is related only to varia-
tion in the environmental variables. For the simulated data
two explanatory variables, ‘rain’ and ‘djungle’, were included
in the model. For the mangrove species data three explana-
tory variables, ‘elevation’, ‘distance to water’ and ‘distance to
harbour’ were included. For the GLMs, the linear predictor,
at location i is related to the explanatory variables as
a
Xbi  a  ∑d g k ki (3)
k1
where a is the intercept, dk is the parameter to be estimated
for each explanatory variable k, where k ranges from 1 to a,
the maximum number of variables, and gki is the value of
the explanatory variable k at location i. In fitting the BRT
models the same variables were used although the fitting
procedure differs from the GLM as described in the previous
section.
Autologistic model
The autologistic model included the explanatory variables
as in the environment only model, plus an additional vari-
able, the autocovariate, representing SAC in the response
variable. SAC is accounted for in the model by estimating
how much the response variable at a location is correlated
with the values of the response variable at neighbouring
locations (Dormann et al. 2007). Fitting the autologistic
model, where the autocovariate is derived from the response
variable, is a two step process. First the autocovariate is cal-
culated based on the observation data, then the explanatory
variables and the autocovariate are fitted within a GLM or
a BRT approach. To calculate the autocovariate, the obser-
vations (the values of the response variable) are arranged in
a grid and a neighbourhood size defined. There are several
ways to calculate the autocovariate and they fall into two
general classes: direct estimates and focal calculations. For
direct estimates, the autocovariate is calculated as the aver-
age of the number of occupied cells in a set of neighbour-
ing cells, divided by the distance to the neighbouring cells
(inverse distance weighting) (Augustin et al. 1996). Focal
calculations of the autocovariate are a special instance of
inverse distance weighting where cells within a selected
neighbourhood have a weight of 1, and all other cells 0.
The autocovariate is then calculated as the average or maxi-
mum value within the defined neighbourhood (Leathwick
and Austin 2001, Luoto et al. 2001). A first-order neigh-
bourhood is defined as the eight cells adjacent to the cen-
tral cell and a second-order neighbourhood includes the
16 cells adjacent to the first-order neighbours (O’Sullivan
and Unwin 2003). Here a first-order neighbourhood with
a focal mean autocovariate is presented as this produced the
strongest model performance (in terms of cross-validated
AUC scores, deviance explained and reduction in SAC
in model residuals) in comparison to two other methods
881
(inverse distance weighting and maximum focal autoco-
variate, both calculated for first- and second-order neigh-
bourhoods, results not shown here). The focal means were
calculated in R using the package ‘raster’ (Hijmans 2011).
For the autologistic model, SAC is accounted for by
estimating how much the response variable at site i is cor-
related with the values of the response variable at neigh-
bouring sites j (Dormann et al. 2007). For the GLMs, when
the autocovariate is calculated as a focal mean, the relation-
ship between the presence of the target species and the linear
predictor, at location i, can be represented as
a
∑d g ∑y
1
Xbi  a  k ki  da1 j
N (i )
k1 j ∈N ( i )
where a, d, g, k, i and a are as defined for Eq. 3, and the
final term is the autocovariate where yj is the value of the
response variable at location j, where j is a cell within the set
of cells forming neighbourhood N(i). For each location i, a
neighbourhood is defined, so the summation is across the set
of cells in the neighbourhood and divided by the number of
cells in the neighbourhood. A parameter, da1, is estimated
for the autocovariate simultaneously with estimates of the
parameters associated with the environmental explanatory
variables (dk). Here the same autocovariate and environmen-
tal explanatory variables were fitted to the GLM and BRT
models.
Residuals autocovariate model
The residuals autocovariate (RAC) model includes the
environment only explanatory variables plus an autocovari-
ate that represents spatial autocorrelation in the residuals
of the environment only model. In a RAC model, SAC is
accounted for by estimating the strength of the relationship
between the environment only model residuals at a loca-
tion and the values of those residuals at neighbouring loca-
tions. Fitting models when the autocovariate is based on the
residuals is a three step process. First, a model describing the
influence of environmental variables on species occupancy
is fitted as either a GLM or a BRT model. Second, the resid-
uals from that model are calculated for each grid cell and
the autocovariate calculated based on these residuals using
a mean focal operation for a first order neighbourhood, in a
procedure identical to the autologistic model. This produces
an autocovariate calculated from the model residuals rather
than directly from the response variable as is the case in
the standard autologistic approach. The residuals are in the
scale of the link function (logit), and are approximately nor-
mally distributed, potentially ranging from negative infinity
to infinity. In the third step the environmental explanatory
variables and the residuals autocovariate are fitted to a GLM
or BRT model, and the parameter values describing the
influence of explanatory variables and the autocovariate on
the observed occupancy data simultaneously estimated.
The RAC model linear predictor, at location i, has the
following form, when fitted as a GLM
a and 21 (indicating strong negative SAC e.g. dispersion)
∑d g ∑ ( y 2q )
1
Xbi  a  k ki  da1 j j
k1
N (i ) j ∈N ( i )
882
where qj is the estimated probability of occurrence at site
j derived from an environment only model (Eq. 3). The
remaining terms are as defined for Eq. 3 and 4. The same
RAC autocovariate and environmental explanatory variables
were fitted to the GLM and BRT models. The RAC mod-
els were fitted using the statistical package R (ver. 2.11.1;
R Core Development Team) and code is provided in the
Supplementary material Appendix 1.
Assessment of model performance
The predictive and inferential performance of the three
(4) classes of models were assessed against the following cri-
teria: predictive ability, reduction in SAC and inferential
performance.
Predictive ability of the models
Predictive accuracy is measured according to the match
between the predictive map of the probability of species
occurrence produced by the model and the observed spatial
distribution of the species. Prediction accuracy was assessed
quantitatively in two ways. In the first, we calculated the
area under the receiver operating curve (AUC), a metric
that combines the trade off between sensitivity (the true
positive proportion) against the false positive proportion,
across all possible thresholds (Swets 1988). A model with
a high AUC score has a greater ability to correctly rank
sites that are actually occupied by the target organism
above unoccupied sites. For pairs of randomly selected sites
ranked in order of predicted probability of occupancy, a
model with an AUC score of 1 will correctly rank the sites
100% of the time, while an AUC score of 0.5 indicates
that the model will rank sites correctly only 50% of the
time (Pearce and Ferrier 2000). The AUC was calculated
on the held-out folds of a 10-fold cross validation (Stone
1974), therefore, the model was not tested against the data
on which it was fitted.
The second performance metric, deviance explained
by the model, indicates the goodness of fit between the
modelled values and the observed values (Crawley 2007).
The percent of deviance explained was calculated as the
null deviance less the residual deviance as a proportion of
the null deviance. Deviance explained incorporates mea-
sures of the match between the actual and predicted fre-
quency of occurrence, and strong explanatory power is
indicated by a high percent of deviance explained (Ferrier
and Watson 1997).
Ability of the model to account for spatial autocorrelation
The ability of the models to account for SAC is indicated by
the reduction of SAC in model residuals. SAC was measured
by calculating Moran’s index and plotting these values as
correlograms. Moran’s index indicates the strength of the
correlation between observations as a function of the dis-
tance separating them, with the distance between obser-
vations grouped into intervals. Values of Moran’s I range
between 1 (indicating strong positive SAC e.g. clustering)
(5) with zero indicating a random pattern with no spatial auto-
correlation (Cliff and Ord 1981). Moran’s I was calculated
Table 1. The predictive performance and ability to control residual was similar, however for the mangrove species occurrence
SAC for three models (environment only, autologistic and RAC, data the BRT models outperformed the GLM’s in deviance
implemented as GLMs and BRTs) for simulated data, as indicated by
the mean ( SE) of cross-validated percent of deviance explained, reduction.
AUC scores and Moran’s I.
% deviance
Model explained AUC Moran's I Synthetic data
GLM environment 7.29  0.17 0.66  0.02 0.343  0.016 Predictive ability (GLM and BRT)
GLM autologistic 58.95  0.20 0.96  0.01 20.039  0.003
Model predictive performance was evaluated using cross-
GLM RAC 58.95  0.38 0.95  0.01 20.040  0.003
BRT environment 8.03  0.01 0.67  0.02 0.336  0.017
validated AUC scores and the deviance explained by each
BRT autologistic 56.29  0.03 0.95  0.01 20.006  0.006 model (Table 1). The GLM and BRT environment only
BRT RAC 55.80  0.03 0.95  0.01 20.008  0.009 models had AUC scores of  0.70 and the percent of devi-
ance explained was very low, with both the GLM and BRT
approaches accounting for  9%. The addition of either
and correlograms plotted using R, with the ‘spdep’ package the autocovariate derived from the response variable or the
(Bivand 2010) and ‘ncf ’ package (Bjørnstad 2009). autocovariate derived from residuals improved AUCs by
0.28–0.30 over the environment only models, with similar
Quality of the model for inference improvements for both the autologistic model and the RAC
The reliability of model inference was measured for GLMs (Table 1). Notably, there was little difference in these scores
as: a) the unbiased estimation of model parameters; b) the between the GLM and BRT approaches.
accurate selection of explanatory variables as statistically sig-
nificant, and c) correct identification of the sign of regression Spatial pattern in residuals (GLM and BRT)
slopes indicating positive or negative relationships between The spatial autocorrelation remaining in model residuals
the response and explanatory variables. As BRT models are was measured by calculating Moran’s I (Table 1). Moran’s I
not used for parameter estimation, fitted functions repre- was very similar for the GLM and BRT models without the
senting the relationship between the response variable and autocovariates, and was reduced to approximately zero for
each explanatory variable are plotted and compared qualita- all models containing an autocovariate term. The autologis-
tively. The relative importance of variables is indicated by the tic and RAC GLM and BRT models had Moran’s I ranging
proportion of times a variable is selected as a node within the from 20.008 to 20.04 indicating that all spatial modelling
BRT algorithm (Elith et al. 2008). methods tested here effectively removed spatial structure
from model residuals.
Correlograms, a visual representation of SAC, were plot-
Results ted for the raw data and residuals of each model (Fig. 1). The
spatial structure of the raw data, and the GLM and BRT
The predictive performance of the autocovariate models environment only models were similar (Fig. 1a, b, g), and
describing variation in mangrove species’ occurrence was showed that locations within five cells of each other had the
stronger than for the environment only models, as indicated strongest spatial autocorrelation. The correlation structure
by substantial improvements in cross-validated AUC scores was very similar for all the autologistic and RAC models fit-
and the percent of deviance explained (Table 1, 2). Both the ted, irrespective of whether they were GLMs or BRTs, with
standard autologistic model and the RAC model reduced negligible spatial structure in residuals at any lag distance.
residual SAC to negligible levels (0.35 to 20.006 simulated This indicates that all methods successfully explained the
data; 0.6 to 20.04 for C. tagal ). For the simulated data the spatial structuring of the observation data.
RAC approach produced less biased parameter estimates
than the environment only model, and significant variables Parameter estimation bias (GLM)
were correctly identified as statistically significant by the The spatial modeling approaches were assessed for their
RAC model but not by the standard autologistic model. ability to correctly estimate the true parameter values used
For the simulated data GLM and BRT model performance to generate the artificial Snouter dataset, and to correctly

Table 2. The predictive performance of three models (environment only, autologistic and RAC, implemented as GLMs and BRTs) for three
mangrove species, as indicated by the mean ( SE) of cross-validated percent of deviance explained and AUC scores.
Mangrove species
Sonneratia alba Rhizophora stylosa Ceriops tagal
% deviance % deviance % deviance
Model explained AUC explained AUC explained AUC
GLM environment 44.55  0.09 0.95  0.002 13.13  0.03 0.75  0.002 2.87  0.02 0.65  0.003
GLM autologistic 90.36  0.06 1.00  0.0001 79.78  0.03 0.99  0.0003 75.25  0.02 0.98  0.0003
GLM RAC 78.02  0.08 0.99  0.001 68.32  0.05 0.97  0.001 63.89  0.04 0.96  0.001
BRT environment 72.64  0.002 0.99  0.001 32.47  0.005 0.87  0.002 22.49  0.004 0.80  0.002
BRT autologistic 92.10  0.001 1.00  0.0001 80.68  0.004 0.99  0.0003 75.96  0.004 0.98  0.0005
BRT RAC 86.93  0.002 1.00  0.0002 76.70  0.002 0.99  0.0003 72.63  0.003 0.98  0.0003

883

Figure 1. The ability of three models (environment only (a, b),
autologistic (c, d), and RAC (e, f )) to control SAC in model
residuals, as indicated by correlograms of Moran’s I plotted
against distance classes, for simulated data. Models were imple-
mented as GLMs (a, c, e) and BRTs (b, d, f ). Spatial autocorrela-
tion in the raw data is shown in panel (g).
identify significant explanatory variables (Table 3). All mod-
eling approaches correctly found djungle to be a non-signifi-
cant explanatory variable. However, the standard autologistic
approach also erroneously found the rain variable to be non-
significant (a type I error). The parameter estimate for rain
by the GLM RAC model consistently over-estimated the
influence of rain on the distribution of the virtual organism
(true value of rain 20.002, RAC estimate 20.005  0.001).
Fitted functions (BRT models)
Fitted functions graphically representing the relationship
between the response variable and each explanatory variable
were plotted and visually interpreted (Fig. 2). For the
environment only model, rain was the most important
variable and the likelihood of Snouter occurring declined
strongly as rain increased. For the standard BRT autologistic
884
Table 3. The inferential performance of three models (environment
only, autologistic and RAC, implemented as GLMs) for simulated
data, as indicated by the mean ( SE) of parameter estimates for the
explanatory variables. ns: non significant, *p  0.001.
Explanatory variables
Model
Actual value of Rain Djungle
parameter: (20.002) (0.0)
GLM environment 20.0022  0.0003* 0.0052  0.013 ns
GLM autologistic 20.0006  0.0004 ns 0.0029  0.0167 ns
GLM RAC 20.005  0.001* 0.0065  0.0072 ns
model however, the relationship between rain and Snouter
occurrence is positive, while for the RAC BRT model it
was negative, and the probability of Snouter occurrence
decreased with increasing rain, as it should. The rela-
tive importance of variables (RI in Fig. 2), represented by
the number of times the variable is selected during the
BRT fitting procedure, was high for the autocovariates
in both the standard autologistic and RAC approaches
(86.6 to 93.4 autologistic model, 86.3 to 94.0 RAC
model), and low for the environment only model 0.32 to
13.3 (Fig. 2).
Mangrove data
Predictive ability (GLMs and BRT models)
Accounting for SAC by incorporating an autocovariate term
in models of mangrove species distribution improved model
predictive performance as indicated by improvements in
cross-validated AUC scores and in the percent of deviance
explained (Table 2). For the Ceriops and Rhizophora species,
Figure 2. The relationship between the predicted occurrence of the
simulated organism and explanatory variables, as indicated by the
fitted functions shown for three BRT models (environment only,
autologistic and RAC) for the tenth simulated dataset. The relative
importance of variables (RI) was calculated for each simulated data-
set, and the range of values shown.
Table 4. The ability of three models (environment only, autologistic Parameter estimation bias (GLMs)
and RAC, implemented as GLMs and BRTs) to control spatial auto- The true values of the parameters describing the influence
correlation remaining in model residuals, as indicated by Moran’s I,
for three mangrove species. An index of 1 indicates high positive of environmental explanatory variables on mangrove species
autocorrelation; 0 no autocorrelation; 21 high negative autocorre- distributions are unknown and therefore model performance
lation. Spatial autocorrelation in the raw data is shown in the last can not be assessed by a comparison between actual and
line. estimated values of the parameters. Instead, the differences
Mangrove species in variables that were statistically significant in the environ-
Sonneratia Rhizophora Ceriops
ment only, autologistic and RAC models are compared; and
Model alba stylosa tagal incongruities identified between modelling methods in the
GLM environment 0.67 0.62 0.60
sign (positive or negative) of the parameters describing the
GLM autologistic 20.04 20.07 20.07 relationship between the response and explanatory variables.
GLM RAC 20.05 20.07 20.07 The RAC models retained a greater proportion of
BRT environment 0.41 0.48 0.47 environmental explanatory variables deemed statistically
BRT autologistic 20.08 20.08 20.08 significant in the environment only models, compared to the
BRT RAC 20.02 0.02 20.04 standard autologistic models (Table 5). For the Rhizophora
Raw data 0.77 0.68 0.62 and Ceriops species, all three environmental explanatory
variables were significant in the RAC and environment
only models, while only one of the three variables was
both types of autocovariate model had strong predictive considered statistically significant in the autologistic model.
performance with AUC scores in excess of 0.96 as com- The RAC model had a more stable variable selection, in
pared to environment only GLMs (0.65, 0.75 for Ceriops that the explanatory variables included in the environ-
and Rhizophora respectively). The AUC scores for ment only model tended to remain in the RAC model. For
the Sonneratia models were high for all three models Sonneratia alba however, both the standard autologistic
(0.95–1.00), and indicate that the fitted models achieve model and the RAC model had three significant environ-
almost perfect discrimination between occupied and unoc- mental explanatory variables while the environment only
cupied sites. Improvements in the percent of deviance model had two.
explained by the models were greater for the autologistic The sign of the relationship between the occurrence of
models than the RAC models, with the total percent of the target species and environmental variables was com-
deviance explained differing by 3–6% in the BRT approach, pared between the environment only, autologistic and RAC
and 10–12% in the GLM approach. models, and assessed for consistency. The autologistic model
for Rhizophora stylosa indicated a positive relationship
Spatial pattern in model residuals (GLMs and BRT models) between probability of occurrence and distance to water.
Residual SAC was high in both the GLM and BRT This relationship was negative under both the environment
environment only models, although the BRT models only and RAC models. Similarly for Ceriops tagal, the sign
showed a reduction in SAC in comparison to the GLMs of the parameter was negative for the standard autologistic
(Moran’s I, BRT: 0.41–0.48; GLM: 0.60–0.67). This indi- approach and positive for the two other methods (Table 5).
cates that the BRT approach can automatically capture The direction of relationships between the response and
some of the SAC present, although there was still suffi- explanatory variables were the same for RAC and environ-
cient SAC in the model residuals to violate assumptions of ment only models in all cases for all variables tested.
regression models. This residual spatial structure was effec-
tively reduced to zero when either type of autocovariate was Fitted functions (BRT models)
included in the distribution models of each of the three The fitted functions describing the relationship between the
mangrove species (Table 4). occurrence of Sonneratia alba and the explanatory variables

Table 5. The inferential performance of three models (environment only, autologistic and RAC, implemented as GLMs and BRTs) for three
mangrove species, as indicated by mean ( SE) of parameter estimates for the explanatory variables. ns: non significant, *p  0.01,
**p  0.001.
Explanatory variables
Mangrove species
Model Distance to nearest water Distance to outer harbour Elevation Autocovariate
Sonneratia alba
GLM environment 20.0379** 0.0000146 ns 20.1455**
GLM autologistic 20.00192* 20.000704** 20.263** 14.57**
GLM RAC 20.0453** 20.0000267** 20.388** 5.55**
Rhizophora stylosa
GLM environment 20.00428** 0.0000378** 20.06367**
GLM autologistic 0.001067** 20.00000914 ns 20.000684 ns 12.573**
GLM RAC 20.0069** 0.0006759** 20.1318** 5.20**
Ceriops tagal
GLM environment 0.0015** 0.0000119** 20.0492**
GLM autologistic 20.0007808** 20.000000197 ns 0.00539 ns 12.15**
GLM RAC 0.00246** 0.0002571** 20.0986** 5.121**

885
(distance to water, distance to harbour, elevation and the
autocovariate) illustrate how the autocovariate in the stan-
dard autologistic model overwhelms the other explanatory
variables (Fig. 3). For the environment only model, the
fitted function illustrating the relationship between occur-
rence of S. alba and the distance to water variable (Fig. 3a)
shows that the probability of occurrence is highest at  200 m
from water followed by a smooth, steep decline to zero
around 500 m inland. The relative importance of the three
variables is similar (distance to water 37.9, elevation 27.2
and distance to harbour 34.9), and the model is strongly
performing (deviance explained 72.64%, AUC 0.99).
Although the standard autologistic model for S. alba was
also strongly performing (deviance explained 92.1%, AUC
1.00), the fitted functions are flat and approximately zero
across the range of all three variables, including distance to
water (Fig. 3d–f ). The relative importance of the explana-
tory variables dropped to between 0.2 and 0.4, leaving the
autocovariate as the most powerful predictor of Sonneratia
occurrence in the autologistic model (relative importance of
99.2). Much of the information previously contained in the
environmental explanatory variables has been absorbed by
the autocovariate term.
In contrast, in the RAC model, the environmental
explanatory variables still play a role, in particular distance
to water which retains a similar shape in the fitted function
(Fig. 3c). Furthermore, although the RAC autocovariate had
a relative importance of 85.3 and is still the most influential
explanatory variable, the three explanatory variables have a
relative importance of 8.3 for distance to water, 3.5 for eleva-
tion and 2.9 for distance to harbour, much greater values
than in the autologistic model. This shows that the RAC
Figure 3. The relationship between the predicted occurrence of the mangrove tree species Sonneratia alba and explanatory variables,
shown for three BRT models (environment, autologistic and RAC) as indicated by the fitted functions. RI is the relative importance of
variables.
886
model allows the environmental explanatory variables to
contribute to deviance reduction in the model while remov-
ing the spatial autocorrelation in the model residuals.
Discussion
In this study we show that an extension of the standard
autologistic model, where the autocovariate is calculated
from model residuals instead of from the response variable,
outperforms both standard autologistic and environment
only models when evaluated against four criteria: cross-
validated predictive performance, removal of residual spatial
autocorrelation, reduction in parameter estimation bias and
the correct identification of statistically significant variables.
This new approach (residuals autocovariate, RAC) performs
as well as or better than the two other approaches when
applied within GLMs and BRT modelling frameworks,
using both synthetic and field datasets.
Spatial autocorrelation in the response variable does not
always generate bias in parameter selection and estimation
(Diniz-Filho et al. 2003), and it is only the SAC in model
residuals that violates the assumptions of statistical models
(Legendre 1993). While the standard autologistic model has
good predictive performance in comparison to models that
do not account for SAC (Hoeting et al. 2000, Wintle and
Bardos 2006, Betts et al. 2009) it can produce biased para­
meter estimates (Carl and Kühn 2007, Dormann 2007b,
Dormann et al. 2007). This is largely because the autologistic
approach accounts for SAC in the response variable before
fitting the explanatory variables, whereas there are sources
of SAC that can be explained by the explanatory variables
and potentially eliminate any SAC in model residuals.
Spatial autocorrelation in biological data arises from exog-
enous sources such as from the environment (e.g. rain-
fall, temperature and soil type) (Legendre et al. 2002) and
endo­genous sources related to characteristics of the target
species itself, such as limits to dispersal or breeding
aggregations (Legendre 1993, Keitt et al. 2002, Wintle and
Bardos 2006). The advantage of the RAC approach over the
autologistic approach is that the explanatory variables are
fitted first and have an opportunity to account for SAC in
species distributions. By deriving the autocovariate from
model residuals, only the variance unexplained by the
explanatory variables is incorporated, and therefore the RAC
model better captures the true influence of these explana-
tory variables, resulting in stronger inferential performance
than the autologistic approach. This was demonstrated for
the datasets used in this study where the RAC model para­
meter estimates were more accurate than those of the stan-
dard autologistic model, and significant variables were
correctly identified and retained in the models.
The two modelling frameworks, GLM and BRT, applied
here for the RAC approach are complementary. Generalized
linear models are easy to interpret, are widely applied in ecol-
ogy and produce parameter estimates that can be used in
meta-analyses or in Bayesian learning (McCarthy and Master
2005). The strength of BRT lies in their ability to automati-
cally capture complex, non-linear relationships with sharp
disjunctions (De’ath 2007, Elith et al. 2008). For the man-
grove data we found that the environment only BRT models
were able to reduce SAC in model residuals, although sub-
stantial residual SAC remained. The RAC BRT models for
mangrove species were superior to the RAC GLM models,
as shown by an increase in deviance explained. This indi-
cates that the advantages of the BRT approach, evident in
the environment only models are also present in the RAC
models. The combination of a residuals autocovariate model
(RAC) with a tree-based modelling method (BRT) results
in superior model predictive performance. However, the
BRT method automatically fits interactions between vari-
ables while such interactions must be explicitly defined and
included in the GLM approach. If we had explicitly included
these interactions in the GLM’s their performance, most
likely, could have been improved.
There are advantages to using both synthetic and actual
data to test model prediction and inferential ability (or per-
formance) as shown by the comparison of GLM and BRT,
and autologistic and RAC model performance. Synthetic
data, where the actual values of the parameters are known,
enables identification of bias in the recovery of parameter
estimates. However, synthetic data is necessarily structurally
simplistic and does not replicate the complexity of field data
(Betts et al. 2009, Bini et al. 2009). The field data used here
for mangrove species is complex and strongly spatially auto-
correlated and we found that the BRT models had stronger
predictive performance than the GLMs for all approaches.
These differences were not evident in results from the syn-
thetic data probably because the data were simulated via
a simple linear relationship with no interactions and was,
therefore, well modelled by a simple linear GLM. Much of
the advantage of BRT models lies in the ability to handle
complex interactions and non-linearities, qualities that fre-
quently occur in actual data, but less so in synthetic data-
sets. This underscores the importance of testing modelling
approaches on both synthetic and actual data.
Models are widely used in ecology and conservation. A
model can represent our mechanistic understanding of the
causal relationship between explanatory and response vari-
ables (Crawley 2007). In correlative statistical modelling,
incorrect parameter estimation can lead to a poor under-
standing of the system and to poor predictions. Under- or
over-estimation of the importance of explanatory variables
can lead to misunderstandings about the role of natural
and anthropogenic processes in ecology and result in poor
decisions and policies that may jeopardize the persistence
of species. Given that virtually all geo-referenced ecological
datasets contain SAC (Lennon 2000), and that the presence
of spatial autocorrelation in model residuals can cause infer-
ential problems in statistical analyses, it is important that
species distribution modelling methods account for spatial
autocorrelation, while remaining straight forward to apply
and simple to interpret. We have demonstrated the advan-
tages of an approach that reduces bias in parameter estima-
tion and increases predictive performance of models fitted to
spatially autocorrelated observation data. A practical advan-
tage of the RAC model over others accounting for SAC is
that it is simple to apply and can be implemented within the
very widely used GLM approach, or to enhance predictive
performance further, within a BRT framework.
Acknowledgements – We extend our gratitude to Peter Brocklehurst
for providing the mangrove distribution datasets, to Michael Bode
and Yacov Salomon for assistance in preparation of the equations
and to Jane Elith, Mark Burgman, Alan Andersen and Anna
Richards for their thoughtful comments on the manuscript.
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