DEMOGRAPHY BEYOND THE POPULATION

Confronting species distribution model predictions with

species functional traits
Marion E. Wittmann1,2, Matthew A. Barnes1,3,4, Christopher L. Jerde1,2,3, Lisa A. Jones5 &
David M. Lodge1,3
1

Department of Biological Sciences, University of Notre Dame, Notre Dame, Indiana 46556
Department of Biology, University of Nevada Reno, Reno, Nevada 89509
3
Environmental Change Initiative, University of Notre Dame, Notre Dame, Indiana 46556
4
Department of Natural Resources Management, Texas Tech University, Lubbock, Texas 79409
5
Fisheries and Oceans Canada, Great Lakes Laboratory for Fisheries and Aquatic Sciences, Burlington, ON L7S 1A1, Canada
2

Keywords
Environmental niche model, grass carp,
managed species, Maxent, model validation,
species biogeography, species functional
traits.
Correspondence
Marion E. Wittmann, Department of Biology,
University of Nevada Reno, Reno, NV 89509.
Tel: (+1) 805 448 8259;
Fax: 775 784 1302;
E-mail: mwittmann@[Link]
Funding Information
This research was funded by Environmental
Protection Agency Great Lakes Restoration
Initiative and NOAA Center for Sponsored
Coastal Ocean Research: NA09NOS4780192,
NA10NOS4780218.
Received: 7 August 2015; Revised: 22
November 2015; Accepted: 25 November
2015
Ecology and Evolution 2016; 6(4):
873880

Abstract
Species distribution models are valuable tools in studies of biogeography, ecology, and climate change and have been used to inform conservation and
ecosystem management. However, species distribution models typically incorporate only climatic variables and species presence data. Model development or
validation rarely considers functional components of species traits or other
types of biological data. We implemented a species distribution model (Maxent) to predict global climate habitat suitability for Grass Carp (Ctenopharyngodon idella). We then tested the relationship between the degree of climate
habitat suitability predicted by Maxent and the individual growth rates of both
wild (N = 17) and stocked (N = 51) Grass Carp populations using correlation
analysis. The Grass Carp Maxent model accurately reflected the global occurrence data (AUC = 0.904). Observations of Grass Carp growth rate covered six
continents and ranged from 0.19 to 20.1 g day 1. Species distribution model
predictions were correlated (r = 0.5, 95% CI (0.03, 0.79)) with observed growth
rates for wild Grass Carp populations but were not correlated (r = 0.26, 95%
CI ( 0.5, 0.012)) with stocked populations. Further, a review of the literature
indicates that the few studies for other species that have previously assessed the
relationship between the degree of predicted climate habitat suitability and species functional traits have also discovered significant relationships. Thus, species
distribution models may provide inferences beyond just where a species may
occur, providing a useful tool to understand the linkage between species distributions and underlying biological mechanisms.

doi: 10.1002/ece3.1898

Introduction
Understanding the distribution of species and ecosystems
as well as the underlying biological mechanisms is essential to the sustainable management of natural resources.
The study of biogeography, however, has largely developed separately from ecosystem ecology, which has led to
conceptual and technical difficulties in incorporating species interactions, dispersal limitations, and species adaptations into predictive models (Violle et al. 2014).

Functional components of biodiversity, for example, the

distribution of species forms and functions, have recently
been recognized as important linkages between observed
species distributions and the associated abiotic and biotic
conditions of ecosystems (Wardle et al. 2004; Violle et al.
2014). The study of these relationships has also benefitted
applications in conservation biogeography and other fields
(Franklin 2010, Griffith et al. 2016).
Observed species distributions are the result of the
abiotic and biotic conditions and processes affecting the

This article forms part of the British Ecological Society journals Demography Beyond the Population special feature [Link]
BES_demography
2016 The Authors. Ecology and Evolution published by John Wiley & Sons Ltd.
This is an open access article under the terms of the Creative Commons Attribution License, which permits use,
distribution and reproduction in any medium, provided the original work is properly cited.

873

Modeling Species Distributions

species. Most of the tools that have been developed to

model species distributions rely on the concept of the
environmental niche and thus focus on the abiotic conditions affecting species distributions (Busby 1991; Guisan
and Zimmermann 2000; Phillips et al. 2006). Termed
environmental niche model or SDM (species distribution model), these predictive models combine known
occurrences of a species with local environmental data
(often, climate-based data such as temperature or precipitation) to predict potential species geographic distribution
(i.e., the fundamental niche (Hutchinson 1958) including areas where the species is known to occur as well as
areas where it does not). SDMs have been used in a wide
range of applications such as habitat selection for species
introductions and conservation (Schwartz et al. 2012),
predicting invasive species spread (Jim
enez-Valverde et al.
2011; Sobek-Swant et al. 2012), and estimating response
to global climate change (Guisan and Thuiller 2005). An
implicit assumption of SDMs is that in sites predicted to
be highly suitable, species would have higher fitness compared to sites predicted to be poorly suitable (Guisan and
Thuiller 2005); however, this relationship is rarely tested.
Despite demonstrations of SDM accuracy in predicting
species occurrence (e.g., Chen et al. 2006; Herborg et al.
2007), skepticism remains about how accurate we might
expect predictions to be given the lack of ecological or
biological information in most SDM applications. First,
because SDMs are based on the concept of the environmental niche and focus on the abiotic conditions affecting species distributions, model outputs are more
representative of the potential species distribution, rather
than the realized or observed species distribution that has
been shaped by biotic conditions and ecological processes. Second, niche conservatism, a major tenet of ecological niche modeling of nonindigenous species,
hypothesizes that a species will spread primarily into
areas within which its climatic niche is similar to that of
its native range (Pearman et al. 2008). However, counterexamples exist (Broennimann and Guisan 2008; Tingley
et al. 2014), potentially due to ecological or evolutionary
niche shifts, landscape heterogeneity, model selection,
choice of environmental variables used to train models
(Peterson and Nakazawa 2007; R
odder and L
otters 2009,
Teller et al. 2016), or interspecific interactions (Sinclair
et al. 2010). Further, historical conditions also influence
observed species distributions and can make predicting
distributions problematic using only environmental variables.
For one widely distributed species, we tested whether
climate habitat suitability predictions resulting from
Maxent analyses are correlated with observations of
growth rate. Specifically, we used Grass Carp
(Ctenopharyngodon idella), a widely distributed aquacul-

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M. E. Wittmann et al.

ture and nuisance aquatic plant control species (but

also an invasive species in some regions and ecosystems), to test whether the degree of predicted climate
habitat suitability correlates positively with observations
of individual growth rate.

Methods
Model organism
Grass Carp is a large cyprinid fish with a native range
extending from northern Vietnam to the Amur River
along the RussiaChina border (Fuller et al. 1999). It has
been widely introduced for nuisance aquatic plant control
and is also cultivated in China and other countries worldwide as a food source. Recently in North America, concern about its persistence and potential unwanted impacts
has increased because of a growing number of captures of
feral individuals in unintended locations (Wittmann et al.
2014).

Species distribution model implementation

We predicted Grass Carp climate habitat suitability at the
global scale using Maxent because in many applications it
has better performance than other SDM methods and
because it is the most widely used SDM software implementation (Elith et al. 2006; Phillips et al. 2006; Fitzpatrick et al. 2013). Full details of Maxent
implementation are presented in Appendix S1, including a
description of occurrence data preparation, environmental
data, and the results of a pilot tuning experiment. Briefly,
we rarified Grass Carp occurrence data and incorporated
bias grids (Elith and Kearney 2010) to avoid reporting
biases, which could influence model performance (Barnes
et al. 2014). We used only temperature layers (omitting
precipitation layers) of the WorldClim climate data set
(Hijmans et al. 2005) as the source of environmental data
for this study. As an aquatic species, Grass Carp establishment can occur only in aquatic habitats. Adapting SDM
implementation methods used in (Barnes et al. 2014), we
did not include any indicators of water availability in the
environmental layers used to train our models because
even in regions where standing water is not plentiful, such
as the southwestern United States, Grass Carp could establish if introduced into riverine backwaters, oases, or water
gardens, and we did not want our model to miss suitable
habitat in such areas. Model performance was assessed
directly in our pilot tuning experiment through iterative
omission of random subsets of 20% of occurrence data
for testing of predictive strength using area under the
receiver operating characteristic curve (AUC). To
maximize data availability for the main purpose of this

2016 The Authors. Ecology and Evolution published by John Wiley & Sons Ltd.

M. E. Wittmann et al.

study the comparison of Maxent output with Grass

Carp growth data we ran Maxent with all available
occurrence data. We present only this all-data model in
the main text.

Modeling Species Distributions

growth rate for each age class with available data. These
last two tests were carried out to avoid spurious correlations between growth rate and climate habitat suitability.
Hypothesis testing is reported using 95% confidence
intervals of the correlation coefficient.

Grass Carp growth rate

Data to summarize observed growth rates of Grass Carp
were obtained from the primary and gray literatures using
ISI Web of Science and Google Scholar keyword search
terms: grass carp and Ctenopharyngodon idella. Studies were retained if they quantified growth rates of Grass
Carp under natural conditions (either wild or naturalized
populations) (termed wild below) or under conditions
in which Grass Carp were stocked for nuisance plant control and the experimental period in which fish were monitored was as least 6 months (termed stocked below).
Studies originally published in Russian and not available
in English were translated (Bogutskaya et al. In Press).
Situations in which Grass Carp were artificially fed, supplemented (e.g., protein pellets or other non-natural food
sources such as terrestrial plants or feed), or were from
artificial tanks, mesocosms, or laboratory enclosures were
excluded to avoid bias in growth rates associated with
non-natural habitat or feeding conditions. Growth was
calculated in grams per day (g day 1). In cases where
there were multiple age classes or cohorts, growth rates
were averaged over all classes. See Appendix S2 for a full
list of all observations used.

Correlation analyses
We used Pearsons correlation to assess the relationship
between Grass Carp individual growth rate and the predicted degree of climate suitability from Maxent (i.e., the
logistic output of the Maxent model). Two independent
tests were performed on the relationship between predicted climate habitat suitability and individual growth
rate: growth rates from wild captures and growth rates
for stocked Grass Carp. The null hypothesis was that no
correlation exists between observed growth rate and climate habitat suitability, r = 0. We hypothesized a positive, significant relationship, especially for the wild
populations. We expected the relationship to be weaker
or nonexistent for the stocked Grass Carp because they
may have high and/or rapidly changing resource abundance (e.g., if stocked to reduce or eliminate nuisance
macrophytes) or they may experience unusually large
densities as part of the initial stocking conditions, such
that density dependence may restrict individual growth.
Because density of stocked populations, and age of both
stocked and wild populations, may be correlated with
growth rate, we also tested the correlation of density with

2016 The Authors. Ecology and Evolution published by John Wiley & Sons Ltd.

Literature review
We conducted a literature review to summarize other
documented examples of the relationship between species
functional traits and species distribution model outputs.
Data were obtained from the primary literature using ISI
Web of Science and Google Scholar searches for studies
that assessed the relationship between any kind of species distribution model (not just Maxent but also
boosted regression trees, generalized additive models,
and others). Search terms used included species distribution model and environmental niche model. Information collected from each study included organism
type, species, location, model(s) used, traits evaluated,
relationship (positive, negative, or none), and reference
information.

Results
Species distribution model
Overall, Maxent accurately captured the known global
occurrences of Grass Carp (AUC = 0.904). Predicted
highly suitable habitat occurred within Grass Carp native
range in eastern Asia between the Amur River and the
northern regions of the Cambodian peninsula (Fig. 1).
Similar areas of high suitability occurred in coastal
regions of Australia and the coasts of the Mediterranean
Sea, southeastern regions of North America, including
large portions of the United States and Mexico, as well as
southern Brazil and large portions of Uruguay, Paraguay,
and Argentina in South America. Predicted climate habitat suitability was low along the equator and north of the
Arctic Circle (Fig. 1).

Grass carp growth rate

We found 68 unique records from six continents of Grass
Carp growth rate that ranged from 0.19 to 20.1 g day 1
(Appendix S2). Seventeen of 68 records were considered
wild or feral populations and were observed in Russia,
Kazakhstan, Uzbekistan, Turkmenistan, New Zealand,
and the United States. The remaining 51 records were
widely distributed stocked Grass Carp populations measured in canals, ponds, lakes, and river or reservoir systems. Fish ages ranged from yearling to greater than
9 years.

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Modeling Species Distributions

M. E. Wittmann et al.

Habitat suitability
High : 0.82
Low : 0.00

Figure 1. Global projection of suitable Grass Carp (Ctenopharyngodon idella) habitat based on occurrences records with spatial extent of 50 km
or less. Shading indicates the logistic output of the model. See Appendix S2 for Grass Carp occurrence records.

Correlation analysis
For observed stocked populations, neither the stocking
density (r = 0.07, 95% CI ( 0.32, 0.19), n = 58), nor fish
age (r = 0.02, 95% CI ( 0.24, 0.28), n = 59) correlated
with growth rate. Similarly with wild populations, age did
not correlate with growth rate (r = 0.35, 95% CI ( 0.76,
0.25), n = 13), giving us confidence that any correlations
between the degree of climate habitat suitability and growth
are not spurious. For stocked Grass Carp populations, the
correlation of growth rate and degree of climate habitat
suitability was not significant (r = 0.26, 95% CI ( 0.5,
0.012), n = 51). However, as predicted, the correlation for
wild Grass Carp was positive and significant (r = 0.5, 95%
CI (0.03, 0.79), n = 17) (Fig. 2).

Literature review
Few studies in the published literature compared species
distribution model estimates with species functional trait
observations (Table 1). We found four published studies
that evaluated 22 species including evergreen trees (n = 1
species), grassland plants (n = 4), common alpine plants
(n = 16), and crayfishes (n = 1). There were nine species
functional traits evaluated including genetic diversity,
asymmetry, leaf weight, fecundity, and others (Table 1).
Nineteen of 22 species evaluated had significant positive
or negative relationships between SDM output and measured functional trait.

Figure 2. Scatterplot of growth rate (g day 1) and Maxent-predicted

habitat suitability of Grass Carp from stocked (n = 51, open
diamonds) and wild captures (n = 17, black circles). Pearsons
correlation coefficient testing revealed only wild captured had a
significant (95% CI: 0.03, 0.79) and positive (r = 0.5) correlation
between growth rate and habitat suitability. The black line indicates
the positive relationship of the wild population correlation.

Our model species, Grass Carp, provided an opportunity

to test hypotheses concerning SDM predictions on a global

scale. Because of the widespread distribution of Grass

Carp, and its status as both a beneficial (e.g., as a stocked
species for food and/or biocontrol) and nuisance species
(e.g., when feral populations have unwanted impacts to
ecosystems) data exist worldwide related to its occurrence
and growth. This is in contrast to most other species
where observations of species functional traits, such as
growth, are limited to small empirically based laboratory
or field settings. Although the sample size of wild grass
carp populations is small (n = 17), the records are the best
available information of georeferenced measurements of

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2016 The Authors. Ecology and Evolution published by John Wiley & Sons Ltd.

Discussion

M. E. Wittmann et al.

Modeling Species Distributions

Table 1. Summary of studies showing relationship between variation in habitat suitability and species functional traits. Organism type, species
name, region in which relationships were tested, modeling platform used, and specific traits evaluated are given in columns 15. Relationships
between traits evaluated by trait and/or by species indicated in column 6 (Relationship): +, positive relationship; , negative relationship; 0, no
relationship. Study reference given in last column. Number of species with habitat-specific relationships determined.
Organism(s)

Species

Location

Model(s) used

Traits evaluated

Relationship

Reference

Evergreen
Tree

Myristica malabarica

Western
Ghats,
India

Bioclim (DIVA GIS v 7.3)

Maxent (v 3.3.2)

Bromus madritensis

Coastal
California,
USA

Boosted Regression
Tree (R v 2.3.1)
Artificial Neural
Network (R v 2.3.1)

+
+
+
+
+

Nagaraju et al.
(2013)

Grassland
plants

Regeneration ability
Genetic diversity
Fluctuating asymmetry
Specific leaf weight
Fecundity

Geranium dissectum

Common
Alpine
Plants

Crayfish

Freshwater
fish

Lupinus nanus
Vulpia microstachys
Carex sempervirens
Dactylis glomerata
Dryas octopetala
Festuca paniculata
Geum montanum
Juniperus sp.
Larix deciduas
Leucanthemum vulgare
Pinus sp.
Polygonum viviparum
Rhododendron
ferrugineum
Sesleria caerulea
Salix herbacea
Silene nutans
Trifolium alpinum
Vaccinium myrtillus
Pacifastacus
leniusculus
Ctenopharyngodon
idella (stocked)
Ctenopharyngodon
idella (wild)

Elmendorf and
Moore (2008)

0
0
+

Central
French and
Western
Swiss Alps

Pacific
Northwest,
Japan
Global

Leaf dry matter content

(17/21)
+ (4/21)

Leaf Nitrogen content

(15/21)
+ (6/21)

Maximum vegetative
height

(12/21)
+ (9/21)

Maxent (v 3.3.3e)

Trophic position (d13C)

Larson et al. (2010),

Larson pers comm

Maxent (v 3.3.3k)

Growth rate

This study

Generalized Additive
Model (R v 2.8.2)

Thuiller et al. (2010)

grass carp growth rates outside of manipulated or stocked

situations, and represent independent populations.
For stocked populations of Grass Carp, the lack of
correlation between habitat suitability and growth rates
was expected, and the reasons for this may be relevant
to some applications of SDM to other nonindigenous
species. One assumption of ecological niche theory typically disregarded in SDM implementation is that species
distributions are static in space and time, that is, the
species occurrence is in equilibrium with its environment (Guisan and Thuiller 2005). During range expansion, however, populations of nonindigenous species are
not at equilibrium if dispersal limitation exists or sink
populations occur (Dullinger et al. 2009, Uriarte et al.
2016). It is possible that the stocked populations of

Grass Carp were in flux with their environment due to

an initially high abundance of macrophytes that may
decline over time as biocontrol populations have the
desired impact. Other Grass Carp-induced changes in
the environment, such as altered turbidity, nutrient concentrations, or species dynamics may also cause growth
rates to change over time. Additionally, it is possible
that a number of the stocked grass carp population were
diploid, triploid, or a mix of both, potentially affecting
their growth. Previous work has indicated that triploid
and diploid grass carp have similar growth rates (Wiley
and Wike 1986). However, it has also been shown that
diploid grass carp have higher growth rates when in the
presence of triploid grass carp (Cassani and Caton
2011). Here, the lack of both population-specific

2016 The Authors. Ecology and Evolution published by John Wiley & Sons Ltd.

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Modeling Species Distributions

information on grass carp ploidy and a relationship for

stocked populations reinforces the need for caution in
analyses of dynamic populations in flux (Henning-Lucass
et al. 2016, Visser et al. 2016).
Only a few studies have assessed the relationship
between the degree of SDM predicted climate habitat
suitability and species functional traits (Table 1). These
previous results indicate that correlations between climate
habitat suitability model outputs and species traits exist,
but vary by species type, landscape, and functional trait.
Differences in results among studies have been attributed
to dynamics occurring with individuals, communities, or
micro-habitats (e.g., adaptation, disturbance, community
composition, and variability in abiotic response) (Elmendorf and Moore 2008; Larson et al. 2010; Thuiller et al.
2010; Nagaraju et al. 2013).
Our study adds the first fish example to this growing
body of support that SDM outputs can indicate more
than simply potential range extent and/or densities (Oliver et al. 2012) of species ranges and may capture species
functional traits, such as growth rate, which may be an
indicator of fitness. However, the evidence to support the
notion that the degree of habitat suitability predicted by
SDM applies to biological performance in addition to
potential occurrence remains sparse and should be
expanded in future SDM studies (Gallien et al. 2010). We
are not suggesting that at this point SDM estimates may
be used to infer traits. However, if more studies demonstrate that climate habitat suitability is correlated with
species functional traits, such as growth rate, then ecology, conservation biology, aquaculture, and other applications may benefit from future SDM efforts.
These results represent a call for increased diligence in
producing climate habitat suitability models and utilizing
them to evaluate the relationship between species functional traits and distributions. With so much effort being
put into the refinement of modeling approaches on the
one hand, and criticism of methodological assumptions
and initial conditions on the other hand, there has been
insufficient attention to evaluating the biological meaning
of SDM output. Confronting the output of SDMs with
biological performance data can provide new analyses
with which to evaluate limitations and/or new potential
uses of SDM. If correlations between climate habitat suitability and other biological factors exist, then ecologists
and spatial scientists can be better positioned to offer
broader inferences from SDMs beyond where species may
occur.

Acknowledgments
M. Budhathoki and K. Park provided technical assistance.
E. Pachepsky and L. Pachepsky provided Russian transla-

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M. E. Wittmann et al.

tion. This research was funded by Environmental Protection Agency Great Lakes Restoration Initiative and NOAA
Center for Sponsored Coastal Ocean Research:
NA09NOS4780192, NA10NOS4780218. This is a publication of the Notre Dame Environmental Change Initiative.

Conflict of Interest
None declared.
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Appendix S1. Detailed methods of Maxent implementation.

Appendix S2. Grass Carp growth rate occurrences,
growth rate occurrence descriptive table and associated
references.

Supporting Information
Additional Supporting Information may be found in the
online version of this article:

880

2016 The Authors. Ecology and Evolution published by John Wiley & Sons Ltd.