RESEARCH Using avatar species to model the PAPER …depts.washington.edu/oldenlab/wordpress/wp-content/...priate avatar species and evaluate the performance of avatar-derived models

RESEARCHPAPER

Using avatar species to model thepotential distribution of emerginginvadersgeb_758 1114..1125

Eric R. Larson* and Julian D. Olden

School of Aquatic and Fishery Sciences,

University of Washington, Seattle, WA

98195-5020, USA

ABSTRACT

Aim Anticipating the potential distributions of emerging invasive species is com-plicated by the tendency for species distribution models to perform better whenboth native and invasive range data are available for model development. If invasiverange data are lacking, species models are liable to under-estimate distributions foremerging invaders, particularly for species that are not at equilibrium with theirnative range environment due to historical factors, dispersal limitation and/orecological interactions. We demonstrate the potential to use well-quantified nicheshifts from established ‘avatar’ (i.e. the remote or virtual manifestation of an entity)invaders to develop plausible distributions for data-poor emerging invaders con-tingent on niche shifts of similar magnitude or character.

Location Global.

Methods Using the globally invasive crayfishes Pacifastacus leniusculus and Pro-cambarus clarkii as our avatar invaders, we quantify how niche position, size andstructure differs between native and total ranges using Mahalanobis distance (ameasure of multivariate similarity) and the climate predictors of annual minimumand maximum air temperature. We then generalize patterns of niche shift fromthese species to the emerging crayfish invader Cherax quadricarinatus.

Results Some patterns of niche shifts were similar for Pacifastacus leniusculus andProcambarus clarkii, but niche shifts were of considerably greater magnitude forP. clarkii. When a native range model for C. quadricarinatus was modified withgeneralized niche shifts similar to Pacifastacus leniusculus and Procambarus clarkii,the potential global distribution for this species increased considerably, includingmany areas not identified by the native range model.

Main conclusions We illustrate the potential to use avatar invaders to providecautionary, niche shift-assuming species distribution models for emerging invad-ers. Many theoretical and applied implications of the avatar species concept requireadditional investigation, including the development of frameworks to select appro-priate avatar species and evaluate the performance of avatar-derived models foremerging invaders. Despite these research needs, we believe this concept will haveconsiderable utility for predicting vulnerability to invasion by data-poor species;this is a critical management need because shifting pathways of introduction andclimate change will produce many novel, emerging invasive species in the future.

KeywordsCrayfish, ecological niche model, invasive species, Mahalanobis distance, nicheconservatism, niche shift, risk assessment, species distribution model.

*Correspondence: Eric R. Larson, School ofAquatic and Fishery Sciences, University ofWashington, Seattle, WA 98195-5020, USA.E-mail: [email protected]

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Global Ecology and Biogeography, (Global Ecol. Biogeogr.) (2012) 21, 1114–1125

DOI: 10.1111/j.1466-8238.2012.00758.x© 2012 Blackwell Publishing Ltd http://wileyonlinelibrary.com/journal/geb1114

INTRODUCTION

The emergence of invasive species as a widespread threat to

biodiversity conservation, ecosystem services and human health

and economies has resulted in the development of a diverse suite

of statistical tools for characterizing and managing the invasion

process (Sakai et al., 2001; Lodge et al., 2006; Blackburn et al.,

2011). Perhaps the most common goal of these efforts is to

predict the potential distribution and spread of non-native

species at local, regional or global scales (Peterson & Vieglais,

2001). Numerous methodologies have been developed to meet

this objective, ranging from mechanistic models based on the

behaviour and physiology of invaders (Kearney et al., 2008) to

correlative approaches that apply datasets of environmental

conditions and species occurrences to predict potential ranges

(Peterson, 2003), resulting in a growth research enterprise.

Although conceptual and methodological debates over these

approaches continue in the literature, the value of species

distribution models (also called ecological niche models) in

anticipating and characterizing vulnerability to invasion is

undeniable.

One consistent outcome of this research to date is that

approaches to forecasting susceptibility to invasion improve if

occurrences from both the native and invasive range are simul-

taneously incorporated into the species distribution model

(Broennimann & Guisan, 2008; Jiménez-Valverde et al., 2011).

For example, past research has found that distribution models

developed using only native range data often fail to adequately

predict known invaded ranges and vice versa (e.g. Fitzpatrick

et al., 2007; Larson et al., 2010). Ecologists attribute this ten-

dency to either genuine niche shifts caused by mechanisms like

ecological release or rapid adaptation in an invaded range

(Broennimann et al., 2007), or alternatively to methodological

oversights or limitations in the distribution modelling process

(Rödder & Lötters, 2009; Peterson, 2011).

Native ranges may also fail to predict invasive distributions

because native ranges may be defined by geographic barriers or

historic geological events rather than by current abiotic or biotic

factors, and consequently species distribution models from the

native range may misrepresent the niche when these dispersal

limitations become irrelevant through the invasion process

(Soberón & Nakamura, 2009). Regardless of reason, the utility of

species distribution models as a precautionary tool for manag-

ing invasive species is considerably reduced if these models

require a species to already be widely invasive to anticipate

where a species may become invasive. If this is the case, then

these models will fail to adequately anticipate the potential dis-

tributions of newly emerging invaders that are early in the inva-

sion process and thus do not have extensive invaded range data

available for modelling.

In this study, we advance the novel concept of using well-

studied invasive species as ‘avatars’ to characterize the potential

future distribution of emerging invaders with little or no inva-

sion history. Originating in Hinduism, the word avatar initially

referred to the corporeal embodiment or incarnation of a god,

but has been widely appropriated by the virtual reality and

computer gaming communities to mean a virtual construct that

represents the user. We propose that avatar be applied as a

concept in ecology and biogeography to describe when infor-

mation from a well-studied species is used to anticipate the

distributional implications of anthropogenic or environmental

change (e.g. introduction, climate change, etc.) for a more data-

poor species. Just as in a video game or on the internet, it may be

possible for an avatar to be either a faithful or an inaccurate

representation of the user, and consequently researchers will

need to exercise rigour in selecting appropriate avatars under

our concept (see Discussion). However, we believe the avatar

concept offers a liberating diversity of scenarios to anticipate

and understand how species invasions may progress outside the

restrictive bounds of native range data only.

We propose that as species distribution models are increas-

ingly published, researchers should begin to generalize and syn-

thesize common patterns in distribution or niche shifts (sensu

Pearman et al., 2008) of invasive species between their native

and total (native and invasive) ranges. Common and recurring

attributes of such documented niche shifts should then be

applied to anticipate scenarios of range expansion for species

that are not yet widely invasive but are expected to become more

widespread due to their incipient invasion history or suite of

invader-prone ecological traits. In this regard, emerging invad-

ers can be subjected via avatars to the potential distributional

implications of the invasion process. We present an example of

this avatar invader concept by developing global species distri-

bution models for two major invasive crayfishes using occur-

rences from their native and total ranges, and then apply this

knowledge to model potential niche shifts (in terms of niche

position, size and structure) and predicted distributions for

another crayfish that is emerging as an important invasive

species. We aspire to initiate debate and inquiry into the poten-

tial for generalizing patterns of niche shifts between native and

total ranges in this burgeoning area of research, and the utility of

such ‘avatars’ in anticipating potential niche shifts and range size

for emerging invaders.

METHODS

Selection of study species

Crayfishes can be major invasive species capable of negatively

impacting freshwater populations, communities and ecosystems

through their omnivorous feeding habits and high population

densities (e.g. McCarthy et al., 2006; Matsuzaki et al., 2009;

Olden et al., 2011). Several species of crayfish have been widely

introduced through pathways including stocking for aquacul-

ture or wild harvest, use as live fishing bait and releases of

aquarium and biological supply organisms (Lodge et al., 2000;

Belle et al., 2011). The two most widely distributed invasive

crayfishes are the signal crayfish, Pacifastacus leniusculus, and the

red swamp crayfish, Procambarus clarkii, which are native to

disparate regions of North America and have established popu-

lations in Asia, Europe, North America and elsewhere (Hobbs

et al., 1989).

Avatar species for emerging invaders

Global Ecology and Biogeography, 21, 1114–1125, © 2012 Blackwell Publishing Ltd 1115

The well-documented invasion histories of Pacifastacus len-

iusculus and Procambarus clarkii may make these species ideal

avatars for emerging crayfish invaders with respect to anticipat-

ing niche shifts between native and total ranges and forecasting

potential distributions. For example, in a comprehensive review

of crayfish invasions two decades previously, Hobbs et al. (1989)

reported that Pacifastacus leniusculus was already established on

two continents and in seven countries, and Procambarus clarkii

had invaded five continents and 27 countries. By contrast, the

red claw crayfish, Cherax quadricarinatus, native to northern

Australia and southern New Guinea, was not reported to be

invasive anywhere in the world at that time (Hobbs et al., 1989).

Cherax quadricarinatus has become increasingly popular as an

aquaculture species in the intervening decades (King, 1994;

Jones & Ruscoe, 2000), and has recently been discovered as

isolated wild populations in locations ranging from Singapore

(Ahyong & Yeo, 2007), to Mexico (Bortolini et al., 2007), to the

Caribbean, where researchers are beginning to report negative

impacts on other freshwater organisms (Williams et al., 2001).

These localized C. quadricarinatus occurrences may represent

emergence of this crayfish as an important invasive species, but

provide data which are too sparse to be effectively applied in

modelling the potential global distribution of this species (e.g.

Papes & Gaubert, 2007).

We sought to characterize niche shifts (or their absence)

between native and total distributions for Pacifastacus leniuscu-

lus and Procambarus clarkii and apply this information to antici-

pate how the potential global range of C. quadricarinatus may

differ from that predicted using its native range occurrences

only. We adopt Pearman et al.’s (2008) relaxed definition of a

niche shift as any change in either the fundamental or realized

niche of a species regardless of mechanism (abiotic, biotic or

dispersal). The selection of Pacifastacus leniusculus and Procam-

barus clarkii as avatars in this context was based on their thor-

oughly documented invasion histories and introduction

pathways that are likely to resemble those responsible for

C. quadricarinatus range expansions (stocking for aquaculture

and wild harvest, release of pets and laboratory organisms; Belle

et al., 2011), as well as broadly similar physiological tolerances

and habitat preferences within freshwater ecosystems (Nyström,

2002; Reynolds, 2002). Alternative methods and suggestions for

selecting avatars are outlined in the Discussion.

Modelling methodology and predictor variables

Species distribution or ecological niche models have become

increasingly sophisticated in recent years, evolving from simple

climate envelopes to complex machine-learning approaches

(Guisan & Thuiller, 2005). We chose to model distributions for

our avatar (Pacifastacus leniusculus and Procambarus clarkii)

and emerging (C. quadricarinatus) invaders using a simple

methodology and a minimal selection of climatic predictors

for several reasons. First, sophisticated machine-learning

approaches to species distribution models can produce highly

idiosyncratic probability densities from predictor variables (e.g.

Capinha & Anastácio, 2011) which may be difficult to consis-

tently relate between one species (avatar) and another (emerg-

ing invader). In addition, our analysis is intended as a case study

illustrating the potential use of avatars in anticipating range

expansions for emerging invaders, and as such a simple and

transparent modelling methodology allows for demonstration

of the issues inherent to this concept.

We used Mahalanobis distance (Mahalanobis, 1936) based on

annual minimum and maximum air temperature to character-

ize the niche and model distributions for our three crayfish

species. Mahalanobis distance represents a powerful approach to

quantifying multivariate similarity, and is a commonly applied

methodology for modelling species distributions in presence-

only situations. Several attributes of this approach make it ideal

for our purposes (Farber & Kadmon, 2003; Tsoar et al., 2007).

Mahalanobis distance infers optimal conditions for a species

based on the means and variances of environmental variables at

species occurrences, as well as the covariance matrix between

these variables. As such, Mahalanobis distance elegantly cap-

tures the ways in which a niche shift may manifest as recognized

by Soberón & Nakamura (2009): a change in position (mean),

size (variance) or structure (relationships between niche com-

ponents; covariance) of the niche. Mahalanobis distance has also

been found to perform better than several alternative climate

envelope approaches and comparably to more complicated and

opaque machine-learning methodologies (Tsoar et al., 2007).

See Appendix S1 in the supporting information for a compari-

son of our Mahalanobis distance models to MaxEnt, a popular

machine-learning algorithm for species distribution models

(Phillips & Dudík, 2008).

We used minimum and maximum temperature as our two

climate variables, in part because previous studies have found

these to be influential predictors for determining crayfish distri-

butions (Larson et al., 2010; Capinha & Anastácio, 2011; Liu

et al., 2011). In addition, the inclusion of a large number of

predictors in species distribution models may result in ‘niche

shifts’ that are artefacts of over-fitting species occurrences to

high-dimensional climate space (Peterson, 2011). Consequently,

we opted to use the bounds of minimum and maximum tem-

perature as our only predictor variables due to their transparent

mechanistic value (determinant of growth and lethal limits to

survival; Nyström, 2002; Reynolds, 2002) and their capacity to

clearly illustrate patterns in and potential transferability of niche

shifts between established and emerging invaders.

Data sources

We used annual minimum and maximum air temperature (in

degrees Celsius) at a 5-arcmin resolution for the entire globe

from the WorldClim dataset (Hijmans et al., 2005). We com-

piled a comprehensive database of crayfish point occurrences

from museum records (e.g. the Carnegie Museum of Natural

History, the Illinois Natural History Survey, the Smithsonian

Institution), internet sources including the Global Biodiversity

Information Facility (http://www.gbif.org) and the US Geologi-

cal Survey Nonindigenous Aquatic Species database (http://

www.nas.er.usgs.gov), and species-specific published accounts

E. R. Larson and J. D. Olden

Global Ecology and Biogeography, 21, 1114–1125, © 2012 Blackwell Publishing Ltd1116

for Pacifastacus leniusculus (e.g. Usio et al., 2007; Larson &

Olden, 2011), Procambarus clarkii (e.g. Huner, 1977; Campos &

Rodriguez-Almaraz, 1992) and C. quadricarinatus (e.g. Macar-

anas et al., 1995; Baker et al., 2008). We used 202 native and 296

invasive occurrences for Pacifastacus leniusculus, 339 native and

434 invasive occurrences for Procambarus clarkii and 37 native

occurrences for C. quadricarinatus (Fig. S1). We also report 10

known invasive occurrences for C. quadricarinatus, which were

not used in our models, to illustrate the current global extent of

this emerging invader.

Modelling process, validation and application

We randomly withheld one-quarter of total occurrences (native

and invasive combined) for Pacifastacus leniusculus and Procam-

barus clarkii from model training as datasets for model testing

or validation, and generated an equal number of random global

pseudo-absences for model validation (see below) as per the

recommendations of Capinha et al. (2011). We developed

species distribution models for Pacifastacus leniusculus and Pro-

cambarus clarkii from the remaining three-quarters of both

native and total occurrences using a GIS package for calculating

Mahalanobis distance from species occurrences and environ-

mental layers (Jenness et al., 2011).

We converted Mahalanobis distance to c2 P-values, assuming

that crayfish responses to minimum and maximum temperature

approximate normal distributions (Clark et al., 1993), and used

P-values > 0.05 as a threshold for identifying locations suitable

for occurrence of these crayfishes. A number of metrics for

evaluating species distribution model performance require a

threshold delineating suitable from unsuitable habitats, and we

believe that a Mahalanobis c2 P-value � 0.05 is intuitive for

representing unsuitable habitat, although more restrictive

thresholds (e.g. P-value � 0.10) could be applied. We evaluated

model performance with one-tailed binary tests of omission

using the test dataset and area under the receiver operating

characteristic curves (AUC).

We characterized niche shifts for Pacifastacus leniusculus and

Procambarus clarkii as the percentage change in mean or vari-

ance of minimum and maximum temperature, as well as the

covariance structure between these variables, from the native to

expanded total range datasets. We then generalized these

observed patterns of change in niche position, size or structure

to project two scenarios of niche shift for C. quadricarinatus

starting from its native range niche. After developing a Mahal-

anobis distance model based on native occurrences for C. quad-

ricarinatus, modelled shifts using patterns of percentage change

from Pacifastacus leniusculus (Scenario 1) and Procambarus-

clarkii (Scenario 2) were applied to C. quadricarinatus to

project its potential distribution. We performed this analysis

using the Mahalanobis distance GIS package (Jenness et al.,

2011).

RESULTS

The extent of niche shifts between native and total ranges dif-

fered considerably for the crayfishes Pacifastacus leniusculus and

Procambarus clarkii. The Mahalanobis distance model based on

the native range for Pacifastacus leniusculus predicted 8.6% of

the global land surface as suitable for occupancy by this species

(Fig. 1), and only committed omission errors for 18.6% of test

occurrences with an AUC of 0.965. The total range model pro-

vided only marginal improvement, predicting 8.8% of the global

land surface suitable for occupancy (Fig. 1) with only 17.8%

omission errors and a comparable AUC of 0.967.

By contrast, for Procambarus clarkii the Mahalanobis distance

model based on native range occurrences performed poorly

relative to the total range model. The native range model pre-

dicted 5.4% of global land surface as suitable for this species

(Fig. 2) with an omission rate of 49.7% of test occurrences and

an AUC of 0.854. The total range model predicted a considerably

expanded 12.6% of global land surface as suitable for this species

(Fig. 2) with an improved omission rate of 13.5% and higher

AUC of 0.935.

Despite a minimal niche shift for Pacifastacus leniusculus and

sizeable niche shift for Procambarus clarkii, some changes in

niche position, size and structure between native and total

ranges were similar for these two crayfishes (Table 1). For

example, these species both experienced decreases in mean

maximum temperature (6.1 to 7.2%), increases in minimum

temperature variance (12.7 to 19.4%), and a reduction in cova-

riance between minimum and maximum temperature (60.0 to

68.2%) of similar magnitudes in their range expansion from

native to total occurrences. The large observed niche shift for

P. clarkii was probably attributable to a 600% increase in

maximum temperature variance from the native to total range

(Table 1, Fig. 2).

Both scenarios of niche shift applied to the C. quadricarinatus

native range model resulted in sizeable increases in global

surface area predicted as suitable for this species (Table 1,

Fig. 3). The native range model predicted 7.1% of global land

surface area as suitable. By contrast, Scenario 1 based on the

Pacifastacus leniusculus niche shift resulted in an increase to

10.8% of the global land surface area and Scenario 2 based on

the larger Procambarus clarkii niche shift resulted in an increase

to 19.2% of the global land surface area predicted as suitable

(Fig. 3). Expanded regions identified as vulnerable to invasion

by C. quadricarinatus under avatar scenarios included Southeast

Asia, tropical Africa and South America, and much of the

Caribbean and the southern Florida Peninsula of the USA.

DISCUSSION

We found some similar patterns underlying niche differences

between native and total ranges for the well-established invasive

crayfishes Pacifastacus leniusculus and Procambarus clarkii, but a

considerably larger magnitude niche shift for P. clarkii. The

niches of both species seemed more labile for position (mean)

or size (variance) of maximum temperature than for minimum

temperature, and both species experienced a decrease in struc-

ture (covariance) between these variables from native to total

ranges. We propose that it may be possible to generalize such

elasticity in niche attributes between native and total ranges for



invasive species within or even between taxonomic groups, and

that this information could be applied to model the potential

global distribution for emerging data-poor invasive species. We

demonstrated this avatar invader concept by modelling the

potential global distribution for the emerging invasive crayfish

C. quadricarinatus using both knowledge of its native range and

niche shift information from the best studied invasive crayfishes,

Pacifastacus leniusculus and Procambarus clarkii. When the

native range model for C. quadricarinatus was modified with

generalized niche shifts similar to Pacifastacus leniusculus and

Procambarus clarkii, the potential global distribution for this

species increased considerably, including many areas not iden-

tified by the native range model.

The trivial shift observed for Pacifastacus leniusculus and con-

siderable shift observed for Procambarus clarkii between the

niches of their native and total ranges is similar to results of

another global distribution modelling exercise for these cray-

fishes (Capinha et al., 2011), which documented poor perfor-

mance of native range models for predicting invasive

distributions of P. clarkii. A number of explanations for differ-

ences in the character and magnitude of niche shift between

these two crayfishes are plausible, including inherent differences

in physiological tolerances of these species, the nature of dis-

persal barriers (i.e. drainage boundaries) that constrain their

native ranges or disparate patterns of introduction pathways

and/or propagule pressure to different regions of the world

where they are invasive. Characterizing differences or common-

alities in niche shifts between many well-studied and well-

established invaders is a first step to both evaluating the need for

and transferability of avatar invaders to emerging invasive

species (Rödder & Lötters, 2009; Peterson, 2011). We recom-

mend that our illustrative case study here be followed with com-

prehensive syntheses evaluating the evidence for and nature of

niche shifts among a diverse suite of well-studied invasive

species, an exercise that would not only advance the avatar

invader concept but also our understanding of the prevalence of

niche conservatism.

Our avatar invader approach is inherently reliant on founda-

tional theory in ecology and biogeography, particularly the

niche conservatism hypothesis (Araújo & Pearson, 2005;

Pearman et al., 2008). Recently, researchers have been increas-

ingly interested in evaluating niche conservatism and shifts both

within (i.e. between native and invaded ranges) and between

species (i.e. phylogenetic niche conservatism; Losos, 2008), and

both aspects of the niche conservatism hypotheses are highly

relevant to implementing the avatar invader concept. First,

debate persists over the legitimacy of and evidence for climatic

niche shifts among invasive species, with Peterson (2011)

Figure 1 Climate suitability by minimum and maximum temperature for Pacifastacus leniusculus modelled as Mahalanobis distance(converted to c2 P-values) using native and total (native and invasive combined) occurrences (Fig. S1) projected as the potential globaldistribution for this species (P-values > 0.05).



Figure 2 Climate suitability by minimum and maximum temperature for Procambarus clarkii modelled as Mahalanobis distance(converted to c2 P-values) using native and total (native and invasive combined) occurrences (Fig. S1) projected as the potential globaldistribution for this species (P-values > 0.05).

Table 1 Data structure of annual minimum and maximum air temperature (°C) at three-quarters of native or total (native and invasivecombined) occurrences (Fig. S1) for Pacifastacus leniusculus and Procambarus clarkii, and all native occurrences for Cherax quadricarinatus.Percentage changes between native and total occurrences, with directional arrows indicating decreases (↓) or increases (↑), are reported forPacifastacus leniusculus and Procambarus clarkii. These values were used to generalize two potential global distribution scenarios forC. quadricarinatus, with the model Scenario 1 based on the Pacifastacus leniusculus native to total percentage change and the modelScenario 2 based on the Procambarus clarkii native to total percent change.

Min. temperature Max. temperature

CovarianceMean Variance Mean Variance

Pacifastacus leniusculus

Native –3.18 188.71 25.27 162.23 –88.25

Total –3.27 212.74 23.73 134.50 –35.34

% Change (↓↑) 2.83↓ 12.73↑ 6.09↓ 17.09↓ 59.96↓Procambarus clarkii

Native 0.73 127.42 33.38 15.56 15.74

Total 0.77 152.19 30.97 110.28 5.00

% Change (↓↑) 5.48↑ 19.44↑ 7.22↓ 608.74↑ 68.23↓Cherax quadricarinatus

Native 16.19 73.93 35.38 42.50 –44.39

Model Scenario 1 15.70 83.54 33.26 35.28 –17.76

Model Scenario 2 17.00 87.98 32.90 300.90 –14.21



arguing that no study to date has conclusively demonstrated a

genuine niche shift between native and invasive ranges. We agree

that a number of problems thwart attribution of niche shifts

from correlative species distribution models, but argue that even

if niche shifts are simply the product of species distribution

models improving with the addition of more (invasive) data

points, this semantic issue still leaves resource managers with

considerable uncertainty over whether or not emerging data-

poor invaders will be capable of establishing in their jurisdic-

tion. In response, the avatar invader concept provides a

framework for anticipating and generalizing the extent to which

native range data may under-estimate invaded ranges for emerg-

ing invaders.

We also recognize that not all taxonomic groups may require

or benefit equally from avatar species. Araújo & Pearson (2005)

observe that dispersal-limited species are unlikely to be at equi-

librium with their native range climate, and in this circumstance

species distribution models are liable to underestimate the cli-

matic conditions that a species can tolerate. Consequently,

avatar species may be most useful for dispersal-limited species,

Figure 3 Climate suitability by minimum and maximum temperature for Cherax quadricarinatus modelled as Mahalanobis distance(converted to c2 P-values) using native (Fig. S1) and modelled data structures (Table 2) projected as the potential global distribution forthis species (P-values > 0.05).



including many freshwater organisms like crayfish and small-

bodied fishes (Olden et al., 2010), and less useful for equilibrium

species, like many vascular plants and birds (Araújo & Pearson,

2005). In these equilibrium cases, direct climate matches

between native and prospective invasive ranges may remain an

appropriate modelling approach for emerging invaders (Mgidi

et al., 2007). Organisms that may benefit from avatar-modified

models should become more evident as more studies explore

and define the phylogenetic structure of niche conservatism and

the determinants of range size (Losos, 2008; Olalla-Tárraga

et al., 2011).

A central issue to our avatar invader concept is the question of

whether changes in niche structure between native and total

ranges are transferable from one species to another. Careful

consideration and selection of the avatar(s) used will be essential

to developing plausible species distribution models for emerg-

ing invaders (Table 2). We used Pacifastacus leniusculus and Pro-

cambarus clarkii because these were the best-studied invasive

crayfishes at a global scale and because their pathways of intro-

duction resemble those probably responsible for past and future

invasions of C. quadricarinatus (Belle et al., 2011). A number of

alternative justifications for selection of avatar invaders might

be considered (Table 2), and will depend in part on data avail-

ability that is often limited to a subset of invaders and geo-

graphic locations (Pyšek et al., 2008). Furthermore, advances in

our understanding of phylogenetic niche conservatism (i.e. the

correspondence between ecological and phylogenetic similarity;

Losos, 2008) can inform selection of appropriate avatar species.

If life history and ecological traits related to dispersal limitation

are phylogenetically structured, then phylogenetic similarity

may be an important consideration in selecting an avatar

species. Alternatively, if there is little phylogenetic inertia of such

traits in the group of interest, then avatars should be selected

based on ecological rather than phylogenetic similarity.

Researchers should exercise caution related to a number of

methodological challenges and pitfalls in applying avatar sce-

narios of niche shift to emerging invaders. For example, we

translated observed avatar niche shifts to an emerging invader

using percentage changes in mean, variance and covariance of

climate predictors, but acknowledge that this use of percentage

change could inflate niche shifts around zero values when trans-

lated to another species. The 5.48% increase in mean minimum

temperature for P. clarkii from 0.73 °C to 0.77 °C resulted in a

0.81 °C increase in mean minimum temperature for C. quadri-

carinatus (Table 1), although the large increase in minimum

temperature variance also meant that the native range for

C. quadricarinatus continued to be well-represented under this

avatar scenario (Figs 3 & S2). Regardless, absolute rather than

relative changes might be preferable for some applications or

niche predictors.

In some cases, avatar scenarios of niche shift may result in

predictions of reduced suitability in the native range for the

emerging invader. For example, although our native and Sce-

nario 2 models had similar rates of omission (5.4 and 2.7%,

respectively) for C. quadricarinatus native range occurrences,

our Scenario 1 model omitted 32.4% of these occurrences while

predicting considerable reduced suitability of the native range

for C. quadricarinatus (Figs 3 & S2). Such a result could be used

to justify rejecting an avatar scenario, although we emphasize

that ensemble models that average native range and multiple

avatar scenarios for an emerging invader might adjust for this

problem (Fig. 4). Ensemble models incorporating multiple

Table 2 Considerations in selecting among candidate avatars for modelling the potential distribution of emerging data-poor invasivespecies, and methodological recommendations (best-case) for implementing the avatar concept.

Consideration Recommendation

1. Data availability and quality for avatar(s)

Invasion history Widespread, well-established and thoroughly studied

Occurrence records Frequent in both native and invasive ranges

Minimal bias evident in distribution and reporting of records

Niche relationships Predictors with high ecological relevance and good model performance

Field or laboratory quantification of relationships (mechanistic)

2. Attributes of the avatar(s) in relation to emerging invader

Modes of introduction Similar pathways and vectors

Ecology and life history Similar preferences and tolerances

Native range Equivalent range size

Similar latitude or same biome

Invasive range Established where emerging invader proposed for import or prohibition

Phylogeny Similar ancestry

3. Modelling implementation and methodology

Number of avatars Maximum feasible to represent scenarios or build ensembles

Choice of niche predictors Minimize number to enhance interpretation

Use mechanistic niche predictors

Choice of modelling methodology Represent niche position, size and structure

Use ensembles to enhance predictability



avatar species could weight avatar scenarios based on factors like

phylogenetic relatedness, trait similarity between the emerging

invasive species of interest and the avatar invaders used or how

well each avatar model represents the native or known invasive

occurrences of the emerging invader.

Beyond ensemble models, we also suggest that Bayesian

species distribution models (e.g. Wintle et al., 2003) might be

able to use data from well-established invaders as informative

priors in modelling potential ranges of more data-poor emerg-

ing invaders. We do not advocate Mahalanobis distance based on

minimum and maximum temperature as the only means to

implement our proposed concept, but do suggest that this

approach benefits from mechanistic predictors and a transpar-

ent modelling methodology that makes its assumptions and

limitations clear. Other species distribution models like Ecologi-

cal Niche Factor Analysis or machine-learning methodologies

like MaxEnt may prove adaptable to the avatar invader concept

(Basille et al., 2008; Phillips & Dudík, 2008).

The avatar invader concept shares a great challenge with risk

assessment for invasive species in general: it is difficult or impos-

sible to evaluate models for events that have not yet happened.

Even direct climate matches for emerging invasive species, which

do not account for the potential of niche shift between native

and total ranges, have invoked controversy when they identify

areas as suitable for a species where it has not yet established

(e.g. Rodda et al., 2011). In the case of C. quadricarinatus, we felt

that the sparse distributional data from known invasions were

inadequate to either develop total range models or test our

avatar scenarios of niche shift. Furthermore, we propose the

avatar invader concept as a tool for managers who may be evalu-

ating a species as a prospective invader prior to its invasive

establishment anywhere in the world. How then might we evalu-

ate the merits of niche-shift assuming avatar models?

For individual species, we suggest that avatar models may be

evaluated against known native ranges (see above), that models

should be revisited and evaluated over time if invaded range

data accumulate and that avatar-based scenarios of niche shifts

might be used to provide predictions for mechanistic testing

using laboratory or field trials. However, time and resources may

not be available to develop such mechanistic niche models for

many of the world’s emerging data-poor invaders, and we also

believe that the use of avatar invaders may realistically capture

some components of the invasion process, such as rapid adap-

tation or ecological release, that are unlikely to be simulated or

anticipated from controlled laboratory trials of physiology.

Instead, we favour evaluating the avatar invader concept in

general by retroactively determining if the well-known and

quantified niche shifts for major invasive species can be repre-

sented by the niche shifts of other well-established avatar invad-

ers. Although beyond the scope of this paper, aggregating

evidence for and comparing patterns of niche shifts (or their

absence) for a diverse and comprehensive group of invasive

species will be critical in testing the generality and utility of our

proposed avatar invader concept.

Pathways of introduction and regions of origin for invasive

species change over time, and climate change will continue to

shift the regions where invasive species come from and where

they can establish (Hellman et al., 2008). As a result, new and

poorly studied invasive species will continue to emerge for the

foreseeable future. Scientists and resource managers will be chal-

lenged to anticipate if these emerging invaders can establish in

their jurisdiction when comprehensive invaded range informa-

tion is absent. In response, we have proposed here documenting

the extent of niche elasticity in important climate predictors for

well-studied invasive species, and then transferring this elasticity

as a precautionary boundary for scenarios of niche shifts in

emerging data-poor invaders. We offer this methodology as

another option in the toolbox for the preventive management of

species invasions, and hope that our simple case study here

provokes inquiry into the utility of the avatar invader concept.

ACKNOWLEDGEMENTS

E.R.L. was supported during analysis and writing at the Univer-

sity of Washington by a Victor and Tamara Loosanoff Fellowship

and Achievement Rewards for College Scientists. Additional

support to E.R.L and J.D.O. was provided by NOAA Fisheries

and NOAA Sea Grant. C. D. Hulsey generously provided space

for writing at the University of Tennessee, Knoxville, during

spring 2011. This manuscript benefited from conversations with

and comments from D. J. Currie, J. A. Diniz-Filho, J. J. Lawler, F.

Figure 4 An ensemble model of theaveraged native, Scenario 1 andScenario 2 models for Cheraxquadricarinatus (Fig. 3). Ensemblemodels offer an opportunity toevaluate avatar-derived niche shiftsfor emerging invaders withoutrejecting the initial native rangemodel and to compensate for nicheshifts that may under-represent thenative range (Fig. S2).



Leprieur, H. S. Rogers, B. Stewart-Koster, A. L. Strecker, R. D.

Woldruff and two anonymous referees.

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SUPPORTING INFORMATION

Additional Supporting Information may be found in the online

version of this article:

Appendix S1 Comparison with MaxEnt.

Figure S1 Native and invasive occurrences used for species dis-

tribution models for three crayfish species.

Figure S2 Difference maps comparing the first and second

avatar scenarios to the native range model for Cherax quadri-

carinatus.

As a service to our authors and readers, this journal provides

supporting information supplied by the authors. Such materials

are peer-reviewed and may be re-organized for online delivery,

but are not copy-edited or typeset. Technical support issues

arising from supporting information (other than missing files)

should be addressed to the authors.

BIOSKETCHES

Eric R. Larson is a PhD student at the University of

Washington School of Aquatic and Fishery Sciences. He

is interested in the management of aquatic invasive

species, the conservation of freshwater biodiversity and

the intersection of ecological theory with these applied

goals, with a taxonomic emphasis on freshwater

crayfish.

Julian D. Olden is an Associate Professor in the

School of Aquatic and Fishery Sciences at the University

of Washington. His research focuses on the ecology and

management of invasive species, environmental flows,

freshwater biogeography and the development of

conservation strategies in natural and built

environments.

Author contributions: both authors contributed ideas

that led to the manuscript concept. E.R.L. led the data

analysis, and both authors contributed significantly to the

writing of the paper.

Editor: José Alexandre F. Diniz-Filho



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