Journal of Pest Science

https://doi.org/10.1007/s10340-017-0938-9

ORIGINAL PAPER

Considering biology when inferring range‑limiting stress mechanisms

for agricultural pests: a case study of the beet armyworm
Tania Yonow1,2   · Darren J. Kriticos1,2 · Natalia Kirichenko3,4 · Noboru Ota5

Received: 26 October 2016 / Revised: 10 August 2017 / Accepted: 20 November 2017

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Abstract
Reliable niche models are a cornerstone of pest risk analyses, informing biosecurity policies and the management of biologi-
cal invasions. Because species can invade and establish in areas with climates that are different from those that are found in
their native range, it is important to accurately capture the range-limiting mechanisms in models that project climate suitabil-
ity. We examined a published niche model for the beet armyworm, Spodoptera exigua, to assess its suitability for bioeconomic
analyses of its pest threat, and identified issues with the model that rendered it unreliable for this purpose. Consequently, we
refitted the CLIMEX model, paying close attention to the biology underpinning the stress mechanisms. This highlighted the
necessity of carefully considering how the different stress mechanisms operate, and to select mechanisms which align with
knowledge on the species’ biology. We also identified the important role of irrigation in modifying habitat suitability. The
refitted model accords with both distribution data and our understanding of the biology of this species, including its seasonal
range dynamics. The new model identifies establishment risks to South America, Africa, the Middle East and Asia, and
highlights that under current climate, Europe is only climatically suitable during warm seasons when crops are available.
The modelling exercise reinforced the importance of understanding the meaning of a location record (e.g. persistent versus
ephemeral populations) and of carefully exploring the role of habitat-modifying factors, such as irrigation, in allowing spe-
cies to persist in otherwise inclement localities.

Keywords  Bioclimatic modelling · CLIMEX · Niche modelling · Pest risk · Spodoptera exigua

Key message

Communicated by B. Lavandero.
• We refit the existing CLIMEX model of this species by
Electronic supplementary material  The online version of this explicitly considering how different stress mechanisms
article (http​s://doi.org/10.1007​/s103​40-017-0938​-9) contains
work to restrict range distribution.
supplementary material, which is available to authorized users.
• Robust niche models demand the simultaneous consid-
* Tania Yonow eration of species’ distributions and their biology in rela-
Tania.Yonow@csiro.au tion to climatic range-limiting factors.
* Darren J. Kriticos • The new model emphasizes the critical role of irrigation
Darren.kriticos@csiro.au in extending the potential range of Spodoptera exigua
1 into xeric environments, and the role of migration in
HarvestChoice, InSTePP, University of Minnesota, St. Paul,
MN 55108, USA extending the threat into seasonally suitable habitats.
2
• The potential distribution and biosecurity risk of this pest
CSIRO, GPO Box 1700, Canberra, ACT​ 2600, Australia
extend significantly beyond its current distribution.
3
Forest Zoology Department, Siberian Branch of the Russian
Academy of Sciences, Sukachev Institute of Forest,
Akademgorodok 50/28, Krasnoyarsk, Russia 660036
4
Siberian Federal University, 79 Svobodny Pr., Krasnoyarsk,
Russia 660041
5
CSIRO, Private Bag 5, Wembley, WA 6913, Australia

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Introduction
The potential range of an invasive species is critical to pest
risk analyses and in the establishment of appropriate sani-
tary and phytosanitary measures (e.g. Baker et al. 2000;
FAO 2006; Sutherst 2014; Venette et  al. 2010). Niche
models are commonly used to estimate the potential geo-
graphical range of species and are a critical component of
pest risk analyses. Niche models should be preferred over
correlative species distribution models (SDMs) for this
task because of the challenge of assessing the climatic
suitability in novel environments (Sutherst and Bourne
2009; Webber et al. 2011). The literature abounds with
examples of correlative species distribution models that
appear to fit the native distribution well, but give spurious
results when extrapolated to novel climates (Elith et al.
2013; Rodda et al. 2009; Zhu et al. 2012).
Correlative SDMs typically define species range lim-
its in terms of Bioclim variables. There are many such
variables to choose from, including such factors as mean
annual temperature, minimum temperature of the coldest/
wettest/driest quarter, maximum monthly temperature, etc.
(Kriticos et al. 2014). In contrast, CLIMEX uses a library
of well-studied stress mechanisms that draw from on a
solid foundation of experimental biology. Consequently,
parameter values for stresses in CLIMEX models have, to
a greater or lesser extent, biological or ecological mean-
ing. When appropriate information is available, the stress
mechanisms can be selected, and associated parameter val-
ues adjusted to accord with experimental observations,
allowing the model to be applied in a deductive manner.
However, this necessary information is rarely available,
and the dominant range-limiting processes may not be
immediately apparent. In such circumstances, it may be
necessary to infer the mechanism and its parameters from
a range of information sources, including distribution
data and phenological observations (e.g. De Villiers et al.
2013).
What sets CLIMEX apart from correlative SDMs when
estimating pest risk in novel climates is the biological rel-
evance of the stress functions, the ability to make use of
phenological observations, and the ability to interpret and
challenge parameter values based on theoretical or other
grounds. There are more than 630 CLIMEX publications,
estimating the potential range of pests and pathogens (Krit-
icos 2016). In many cases, these model projections have
been validated, providing reliable prognoses of their future
expansion and indicating the regions at risk (Hall and Wall
1995; Kriticos et al. 2003b, 2015b, 2007; Sutherst and
Bourne 2009; Yonow et al. 2013). CLIMEX is a mecha-
nistic bioclimatic modelling platform, supporting a hybrid
inferential and deductive approach in estimating species’
13
Journal of Pest Science
responses to climatic variables. Parameters can be inferred
by fitting stress functions to accord with distribution data,
or parameters can be derived from experimental observa-
tions of laboratory or field data or theoretical principles
(Kriticos et al. 2015a; Lawson et al. 2010; Van Klinken
et al. 2009), and any conflicts between information derived
from different knowledge domains can be investigated and
resolved using the method of multiple competing hypoth-
eses (Chamberlin 1965). CLIMEX calculates an Ecocli-
matic Index (EI) that describes the suitability of locations
for population growth and survival. The EI is defined by
variables that reflect conditions during the growing season
(Growth Index) combined with variables that describe the
effects of stresses accumulated during inclement seasons
(Stress Index).
It should be possible for any model to be reproduced.
This is a relatively simple matter with a CLIMEX model,
which is sufficiently structured, enabling environmental
tolerances to be clearly inferred (Venette et  al. 2010).
Any published CLIMEX model can easily be recreated
by another user, and assuming that there were no errors
or omissions in the published values, the results should
be identical.
The beet armyworm S. exigua (Hübner 1808) (Lepidop-
tera: Noctuidae) is a major agricultural pest, originating
from southern Asia. During the last century, it has spread
throughout tropical and temperate regions of Africa, Asia,
Europe, and North America (Feng et al. 2003; Zheng et al.
2011a). This highly fecund and long-distance migratory spe-
cies attacks various cultivated crops in greenhouses and open
fields, including maize, cotton, soybeans, beet, tomato, cab-
bage, alfalfa etc., causing serious economic losses (Adam-
czyk et al. 2003; Feng et al. 2003). The insect’s life cycle
takes about 3 weeks, with up to six generations possible per
year in warmer climates (Wilson 1932). Spodoptera exigua
lacks a diapause mechanism (Kim and Kim 1997); there-
fore, it can only overwinter successfully in relatively warm
regions (e.g. Adamczyk et al. 2003; Zheng et al. 2011a).
Zheng et al. (2012) present a CLIMEX model for S. exi-
gua identifying potential overwintering regions of the pest in
China. However, when we use their published parameter val-
ues with both the CliMond meteorological dataset (Kriticos
et al. 2012) and the standard CLIMEX point dataset, we are
unable to replicate the delineation between overwintering
and non-overwintering locations reported in Fig. 3 in Zheng
et al. (2012) (see Fig. 1).
In this paper, we refit a CLIMEX model for S. exigua,
focussing on the process of selecting amongst the available
stress mechanisms. We provide a rationale for the choice
of all parameter values that we adjusted, and discuss the
importance of setting these values and selecting stress mech-
anisms based on an understanding of the species’ biology
and ecology.
Journal of Pest Science
Fig. 1  Figure  3 from Zheng et  al. (2012), published as an Open
Access paper in the Journal of Insect Science under the Creative
Commons Attribution 3.0 license. Overwintering regions of S. exigua
under current climate in China. The map was constructed by Arc-GIS
using the Ecoclimatic Indices (El) obtained from CLIMEX param-
eters in Table  1. In these areas covered colour with green indicates
perennial damage regions and covered with grey indicates overwin-
Materials and methods
The CLIMEX compare locations model (Kriticos et  al.
2015a; Sutherst and Maywald 1985) calculates, inter alia,
an annual index of climatic suitability, the Ecoclimatic
Index (EI). The EI reflects the overall climatic potential for
population persistence, accounting for growth during favour-
able periods and survival during stressful periods (Eq. 1).
The Annual Growth Index ­(GIA) describes the potential
for growth as a function of average weekly soil moisture
(Moisture Index; MI) and temperature (Temperature Index;
TI) (Eq. 2; weekly Growth Index, G ­ IW = TI × MI). Four
parameters define both the MI and TI: a lower threshold
below which growth cannot occur; a lower optimum and
an upper optimum that define the range in which the maxi-
mum growth rate is achieved; and an upper threshold above
which no growth occurs. These nonlinear growth response
functions conform with the law of tolerance (reviewed in
Shelford 1963), and they are combined in a manner that
accords with the law of the minimum (reviewed in van der
Ploeg and Kirkham 1999).
Stress indices describing cold stress (CS), wet stress
(WS), heat stress (HS), and dry stress (DS) and their inter-
actions can be used to describe the species’ response to
tering regions (gray shades indicated suitable areas according to the
El values, and the darker the color is, the more suitable the area). Red
dots represent the site of fieldwork during winter. 1, Sanya; 2, Guang-
zhou; 3, Longnan; 4, Nanchang; 5, Yongxiu; 6, Yibin; 7, Wuhan; 8,
Jurong; 9, Nanjing; 10, Xi’an; 11, Tai’an; 12, Anqiu; 13, Zhangqiu;
14, Beijing
climatically unfavourable conditions. The individual com-
ponents of stress are combined into a stress index (SI) and
a stress interaction index (SX) (Eqs. 3, 4; CDX = cold–dry
stress, CWX = cold–wet stress, HDX = hot–dry stress and
HWX = hot–wet stress) (Kriticos et al. 2015a). Stresses
largely define a species’ potential range and are primarily
informed by geographical distribution data.
EI = GIA × SI × SX (1)
52
∑
GIA = 100 TGIW ∕52 (2)
i−1
SI = (1 − CS/100)(1 − DS/100)(1 − HS/100)(1 − WS/100)
(3)
SX = (1 − CDX/100)(1 − CWX/100)(1 − HDX/100)(1 − HWX/100).
(4)
The EI ranges from 0 at locations where the species is
unable to persist, to 100 at locations that are optimal for
the species year round. In practice, EI values above 50
only occur in highly climatically stable environments near
the equator. It is important to appreciate that the EI only
has meaning as an annual summary statistic, related to
13

population persistence. In order to better understand the
biosecurity threat posed by a species, in addition to looking
at the EI, it is necessary to explore the potential for popu-
lation growth as indicated by the ­GIW variable, the stress
indices, and also to consider the effects that cultural factors
such as irrigation (De Villiers et al. 2016; Yonow et al. 2017)
or glasshouses may have on these life history components
(Sutherst 2003).
CLIMEX is a model of moderate complexity, designed to
explore the effects of climate on a species’ distribution and
phenology. It combines the strengths of correlative mod-
elling methods (allowing stress parameters to be fitted to
geographical location data) and deductive modelling meth-
ods (allowing growth functions to be informed by labora-
tory studies and phenological observations) (Kriticos et al.
2015a).
We used the parameter values given by Zheng et  al.
(2012) to recreate their CLIMEX model. With both the
standard meteorological dataset that comes with CLIMEX
and the CliMond dataset (Kriticos et al. 2012), we obtain
results similar to Fig. 2 in Zheng et al. (2012) (see Fig. 2).
However, when we add a shapefile of overwintering and
non-overwintering locations for S. exigua in China, geo-
coded according to the coordinates given by Zheng et al.
(2012), the resulting maps (Fig. 3) indicate that three of the
known overwintering sites (Nanchang, Yongxiu and Wuhan)
in China are modelled as unsuitable, as is Baýramaly in
Turkmenistan, a known overwintering site (Kurdov 1986;
Zheng et al. 2011a).
Location records for China were taken from the coor-
dinates given by Zheng et al. (2012), and coordinates for
Baýramaly, Turkmenistan, were taken from Google Earth,
and other location records were downloaded from the Global
Biodiversity Information Facility (GBIF) and the Atlas of
Living Australia (ALA, 6 December 2013). All CLIMEX
parameter values are provided in Table 1.
Using the CliMond CM10_1975H_V1.1 dataset (Kriti-
cos et al. 2012), we adjust parameter values so as to fit the
Chinese data (Zheng et al. 2012) and the most northerly
known overwintering site, Baýramaly (Kurdov 1986; Zheng
et al. 2011a). The CliMond dataset comprises 30-year aver-
ages of monthly values for daily minimum and maximum
temperature (°C), relative humidity (%) at 09:00 and 15:00,
and monthly rainfall total (mm). To validate the final model,
we examine the projections in Europe and North America,
where there is some information on the occurrence of this
species.
Soil moisture
Moisture plays an important role in the survival and growth
of S. exigua, particularly in the pre-pupal and pupal stages.
The lower soil moisture threshold (SM0) of 0.03 set by
13
Journal of Pest Science
Zheng et al. (2012) is well below the permanent wilting point
of plants, which is typically about 0.1 using the CLIMEX
100 mm bucket soil moisture model (Kriticos et al. 2003a).
SM0 is therefore increased to 0.1. Zheng et al. (2012) set
the lower optimum soil moisture threshold (SM1) to 0.31.
However, Fye (1978) reports that pre-pupae preferred soils
of < 20% moisture, and Zheng et al. (2013) find that pupa-
tion and survival decrease as soil moisture increases from
10 to 30%. As dry soils are preferable to wet ones, SM1 is
decreased to 0.2, to improve dry-tolerance. No changes are
made to the other soil moisture parameters.
Temperature
Most of the temperature parameters of Zheng et al. (2012)
are adjusted. The developmental threshold for the vari-
ous life stages of S. exigua is estimated to be between 12
and 16 °C (Ali and Gaylor 1992; Butler 1966; El-Refai
and Degheele 1988; Han et al. 2002; Hogg and Gutierrez
1980; Karimi-Malati et al. 2014a; Xu et al. 1999; Zheng
et al. 2012). The change to the development threshold (DV0)
is thus minimal: the value is simply rounded down from
15.06 to 15 °C. The level of accuracy obtained by includ-
ing two decimal places is unwarranted given that CLIMEX
uses average meteorological data, and because the literature
(see above) merely suggests that this value lies somewhere
between 12 and 16 °C. The value of the lower optimum
temperature (DV1) is left at 26 °C, as various authors used
26–28 °C for mass rearing of S. exigua (Jiang et al. 2001,
2011; Karimi-Malati et al. 2012), and Xu et al. (1999) indi-
cate that greatest fecundity occurs between 24 and 28 °C.
The upper optimum temperature (DV2) is increased from 29
to 32 °C, since various authors obtain good development and
survival of all stages at temperatures between 32 and 35 °C
(Ali and Gaylor 1992; Butler 1966; Fye 1978; Han et al.
2002; Xu et al. 1999), and Xu et al. (1999) calculate that the
highest Ro occurred at 32 °C. Finally, the upper threshold
for development (DV3) is increased from 36 to 38 °C as Ali
and Gaylor (1992) obtain full development and survival of
all stages at 38 °C, and Guerra and Ouye (1968) find that 4 h
at 43.3 °C does not affect egg hatch. However, Ali and Gay-
lor (1992) do not specify that reproduction occurs at 38 °C
(only that they obtained full development and survival at this
temperature), and Karimi-Malati et al. (Karimi-Malati et al.
2014a, b) failed to get development or egg hatch at 36 °C.
The value of 38 °C for DV3 in our model is a consensus of
the evidence from the literature regarding both heat stress
and development (Ali and Gaylor 1992; Guerra and Ouye
1968; Jiang et al. 2011; Karimi-Malati et al. 2014a, b). It
is selected in preference to 36 °C to increase the suitability
at Baýramaly (under an irrigation scenario) as insects were
captured in light traps throughout the year here (Kurdov
1986).
Journal of Pest Science
Fig. 2  Figure  2 from Zheng et  al. (2012), published as an Open
Access paper in the Journal of Insect Science under the Creative
Commons Attribution 3.0 license. CLIMEX map of overwintering
regions of S. exigua in China inferred from its known world over-
Cold stress
Since the cold stress (CS) mechanism used by Zheng et al.
(2012) precludes persistence at three known overwintering
locations (Online Resource 1), we sought to identify a bet-
ter range-limiting mechanism. We exported and plotted the
wintering sites after importing total of 758 meteorological stations.
Crosses indicate unsuitable overwintering locations. Spots represent
El’s greater than zero. The larger spots indicate that the climate at the
station is more suitable for overwintering of this species
climate data from CLIMEX for the grid cells containing
overwintering and non-overwintering sites in China (Zheng
et al. 2012) and Baýramaly (Kurdov 1986; Zheng et al.
2011a). The average weekly minimum temperature at Baýra-
maly (overwintering site, − 1.7 °C) is lower than that at the
two warmest, most southerly Chinese non-overwintering
13
 Journal of Pest Science

13
 Journal of Pest Science
◂Fig. 3  Modelled climate suitability of Asia for S. exigua, using the
parameters given by Zheng et al. (2012), a using the CliMond mete-
orological dataset, b using the standard point location dataset that
comes with CLIMEX
sites (Jurong, − 1.2 °C; and Nanjing, − 1.4 °C) (Online
Resource 2), thereby making it impossible to use the tem-
perature threshold model of CS to distinguish between over-
wintering and non-overwintering sites. Using a minimum
temperature threshold model would necessarily preclude
overwintering at Baýramaly before impacting the Chinese
non-overwintering sites.
Figure  4 suggests that it should be possible to use a
degree-day model of CS to distinguish between the overwin-
tering and non-overwintering sites, as the two warmest non-
overwintering sites in China (Jurong and Nanjing, Zheng
et al. 2012) have the fewest degree-days above 15 °C, both at
the end and at the beginning (Fig. 4) of winter. Another key
non-overwintering site (Xi’an) warms up relatively quickly
in spring, with the number of degree-days > 15 °C match-
ing those at a couple of overwintering sites, but becomes
colder earlier in the autumn (Fig. 4). The parameter values
ultimately selected for this CS mechanism (Table 1) result
in some CS accumulating in all of the Chinese overwin-
tering sites, relatively high CS (76–83) in the four coldest
Chinese overwintering sites, and a CS value of 73 at Baýra-
maly (Fig. 5a). These CS values, when combined with the
­GIA values, correctly result in a positive EI at all known
overwintering sites.
Because the maximum temperatures at Baýramaly are
in fact reasonably high, we explored the average tempera-
ture cold stress mechanism. Jurong and Nanjing (the two
warmest Chinese non-overwintering sites) have the coldest
average temperatures in winter (Online Resource 3). It is
possible to parameterise the average temperature mechanism
for CS to correctly distinguish between overwintering and
non-overwintering sites, and to only have a small amount of
CS (CS = 19) at Baýramaly (Fig. 5b). However, as it makes
little biological sense to use an average weekly temperature
threshold (TTCSA) of 4 °C to trigger CS, given the apparent
cold-hardiness of S. exigua (Jiang et al. 2001; Kim and Kim
1997; Zheng et al. 2011b), we reject the average temperature
CS mechanism in favour of the degree-day CS mechanism.
Heat stress
Because the upper temperature threshold (DV3) is increased
to 38 °C, and HS cannot begin to accumulate whilst the
temperature is still suitable for growth (Kriticos et al. 2005;
Van Klinken et al. 2009; Yonow et al. 2017), the HS thresh-
old (TTHS) must be increased from the Zheng et al. (2012)
value of 36 °C. Jiang et al. (2011) indicate a high tolerance
to temperatures in excess of 40 °C, and the original model of
Zheng et al. (2012) is based on a threshold of 40 °C. Thus,
the temperature threshold (TTHS) is increased to 40 °C,
and the rate of stress accumulation (THHS) is decreased to
0.01 week−1, rounded down from the Zheng et al. (2012)
original value of 0.0177 week−1. These changes to the HS
parameters increase the overall modelled climate suitability
of much of Asia. We explore the degree-day mechanism of
HS, and the parameter values given in Table 1 result in mini-
mal difference to the accumulation of HS when compared to
the temperature threshold mechanism or to the model results
overall: EI values increase by a maximum of three in a few
isolated spots in Africa.
Dry stress
The dry stress (DS) parameters of Zheng et al. (2012) are
increased. The threshold soil moisture (SMDS) is increased
from 0.02 to 0.1, to be in line with SM0, and the stress
accumulation rate parameter (HDS) is decreased from
− 0.005 to − 0.01 week−1, increasing how quickly the stress
accumulates.
Setting the threshold soil moisture (SM0) and DS thresh-
old (SMDS) at 0.1 means that Baýramaly experiences a cer-
tain degree of DS (DS = 38), which in combination with the
relatively high CS experienced here (CS = 73), is sufficient
to preclude the persistence of S. exigua (both stresses com-
bined give a total stress > 100, therefore EI = 0). Such a
result is contrary to the knowledge that S. exigua is a pest
here, and that Baýramaly is a known overwintering site
(Kurdov 1986). The CliMond climate data exported for this
area indicate that rainfall is very low, but both Google Earth
and Google Maps images indicate that this is a major water
catchment area, with an extensive series of canals and water-
ways clearly supporting any agriculture that occurs here.
Adding a moderate amount of irrigation to the simulation
(2.5 mm day−1 added as top-up throughout the year) is suf-
ficient to completely remove DS and make Baýramaly suit-
able (EI = 7). These parameters ensure that in the absence of
irrigation practices S. exigua is prevented from establishing
and persisting in areas that are otherwise too dry.
Wet stress
The wet stress (WS) threshold (HWS) is decreased to be in
line with the upper soil moisture threshold (SM3 = 2) and
because of evidence that excessive moisture is not conducive
to pupation (Fye 1978; Zheng et al. 2013).
Number of generations
The number of degree-days above the developmental thresh-
old of DV0 (PDD) is increased from 265.6 to 300 °C days.
PDD represents the annual thermal accumulation needed to
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 Journal of Pest Science

Table 1  CLIMEX parameter values for S. exigua 

Parameter Description Zheng et al. (2012) values This study

Moisture
 SM0 Lower soil moisture threshold 0.03 0.1
 SM1 Lower optimum soil moisture 0.31 0.2
 SM2 Upper optimum soil moisture 1 1
 SM3 Upper soil moisture threshold 2 2
Temperature
 DV0 Lower threshold 15.06 °C 15 °C
 DV1 Lower optimum temperature 26 °C 26 °C
 DV2 Upper optimum temperature 29 °C 32 °C
 DV3 Upper threshold 36 °C 38 °C
Cold stress
 TTCS Cold stress temperature threshold 3.2 °C 0
 THCS Temperature threshold stress accumulation rate − 0.2 week−1 0
 DTCS Degree-day stress cold stress threshold (CS accumulates if there are 8
fewer than the threshold number of degree-days above DV0)
 DHCS Degree-day stress cold stress accumulation rate − 0.00048 week−1
 TTCSA Cold stress average temperature threshold 0 4 °Ca
 THCSA Average temperature stress accumulation rate 0 − 0.065 week−1a
Heat stress
 TTHS Heat stress temperature threshold 36 °C 40 °C
 THHS Temperature threshold stress accumulation rate 0.0163 week−1 0.01 week−1
or or or
 DTHS Degree-day heat stress threshold (HS accumulates if there are more than 2.5 °C days
the threshold number of degree-days above DV3)
 DHHS Degree-day heat stress accumulation rate 0.005 week−1
Dry stress
 SMDS Soil moisture dry stress threshold 0.02 0.1
 HDS Stress accumulation rate − 0.005 week−1 − 0.01 week−1
Wet stress
 SMWS Soil moisture wet stress threshold 2.5 2.0
 HWS Stress accumulation rate 0.002 week−1 0.01 week−1
Threshold heat sum
 PDD Number of degree-days above DV0 needed to complete one generation 265.6 °C days 300 °C days
Irrigation scenario 2.5 mm day−1 as top-up throughout the year

Values that differ from those of Zheng et al. (2012) are given in bold
a
 These values are not used in the final model, but do provide a delineation between known overwintering and non-overwintering sites (see
Fig. 5a, b)

Fig. 4  Number of degree-days
above 15 °C plotted by week
for selected overwintering and
non-overwintering sites in
China (Zheng et al. 2012) and
at Baýramaly (Kurdov 1986;
Zheng et al. 2011a). O indicates
overwintering site; NO indicates
non-overwintering site; grid
cell number included; number
in parentheses matches location
number in Zheng et al. (2012)
(Fig. 1)

13
Journal of Pest Science

Fig. 5  Cold stress maps

for S. exigua a using the
degree-day threshold mecha-
nism, with DTCS = 8 and
DHCS = − 0.00048, b using the
average temperature mecha-
nism, with TTCSA = 4 and
THCSA = − 0.065. Triangles
represent overwintering sites;
squares represent non-overwin-
tering sites (Zheng et al. 2012)

complete a full generation and for successful reproduction We adjust the value to arrive at approximately the correct
to occur. When the value of PDD exceeds the threshold, number of generations in different locations. A PDD value of
the excess contributes to the development of subsequent 300 degree-days above 15 °C provides for seven generations
generations. at Gainesville (Florida, USA) which is close to Wilson’s

13

(1932) claim of six generations in northern Florida (no spe-
cific location given), and it provides seven generations in
Fuzhou (Fujian Province, China) which is close to the eight
overlapping generations reported by Xu et al. (1998). These
differences could easily be accounted for by the fact that
we are using long-term average data rather than data for
a specific year. We also used other data presented in the
literature for development times at different temperatures
and converted these into a common format. We opt for days
taken to complete a generation at 25 °C, in accordance with
results presented by Farahani et al. (2012). Our PDD value
of 300 equates to 30 days for a generation to be completed at
25 °C, which falls well within the range (25–42.4 days) pro-
vided by numerous authors (Ali and Gaylor 1992; Farahani
et al. 2012; Greenberg et al. 2001; Han et al. 2002; Hogg and
Gutierrez 1980; Lee et al. 1991; Zheng et al. 2012).
Irrigation
Because many cropping areas are irrigated (e.g. in Google
Earth, irrigation patterns are clearly visible around Baýram-
aly), a 2.5 mm day−1 irrigation scenario was added as top-up
throughout the year. In other words, irrigation is only applied
when rainfall is less than 2.5 mm day−1. A composite cli-
mate suitability map was created by combining the natural
rainfall and irrigation scenario results using the irrigation
pattern data from (Portmann et al. 2010).
Results
In Asia (Fig. 6), the model accords with known overwin-
tering and non-overwintering locations (Kurdov 1986;
Zheng et al. 2011a, 2012). The results corroborate all the
evidence provided for Turkmenistan by Kurdov (1986):
CLIMEX shows a positive EI at overwintering localities;
a peak in the population growth in May, corresponding
to the most damaging second generation; and population
growth until November, in accordance with the observa-
tion that adults fly from April to November. Furthermore,
the results accord with what is known of the distribution
in Iran, with the appropriate number of generations (six)
in Shiraz (Eghtedar 1989), and winter growth in Khuz-
estan (Atapour and Moharramipour 2014). Khuzestan is
modelled as having an EI value of zero due to excessive
HS, but S. exigua is known to be a migratory species (e.g.
Jiang et  al. 2011; Mikkola 1970; Zheng et  al. 2011a),
and Atapour and Moharramipour (2014) do not indicate
that it occurs 3 year round, only that it overwinters there.
Although the EI value is zero, the Growth Index ­( GI A)
is positive, and growth is estimated to occur in winter at
Khuzestan. Under the natural rainfall scenario, neither
Qazvin nor Khorasan (Atapour and Moharramipour 2014)
13
Journal of Pest Science
has a positive EI, as the combination of both DS and CS
exceeds 100. However, as in Baýramaly, irrigation is used
to sustain agriculture, enabling both of these locations to
sustain permanent populations (Fig. 6a). It is also possible
for overwintering to occur in these locations, as suggested
by Khanjani (2005, in Atapour and Moharramipour 2014).
In Northern Europe, although the EI values are unsuit-
able (Fig. 6a), the G­ IA is positive for much of the region
(Fig.  6b). This is consistent with observations that S.
exigua does not persist there, but rather, migrates from
warmer overwintering regions in the south (e.g. French
1969; Mikkola 1970; Mitchell 1979). There are some
potential discrepancies through the alpine regions of
Northern Italy, Switzerland, and Austria. Location records
in these alpine areas are apparently unsuitable year round
because the temperatures are too cool to support popu-
lation growth, as they rarely exceed 15  °C, the lower
developmental threshold. The distribution records may
have been collected during an abnormally warm year, or
it is possible that the CliMond dataset does not represent
the climate here with sufficient topographic precision:
the nature of this region is such that there are very great
changes in altitude (and thus climate) in very short dis-
tances, which cannot be accurately represented with 10′
datasets (Kriticos and Leriche 2010).
For North America (Fig. 6a), the EI pattern accords
with Zheng et al.’s (2011a) map of overwintering and per-
ennial damage sites, and the ­G I A matches the potential
range this species can achieve in summer (Fig. 6b). Spo-
doptera exigua has established permanent populations in
Florida, California, and southern Arizona (e.g. Carlson
2010; Fye and Carranza 1973; Hogg and Gutierrez 1980;
Sparks and Riley 2015; Trumble and Baker 1984), which
agrees with the model projections.
There are a number of location records in central
Australia with corresponding EI and G ­ IA values of zero
(Fig. 6a, b). Examination of these records indicates that
most were collected between 1960 and 1980, with the bulk
having been collected in 1972 and 1978. When the S. exi-
gua model was used in the latest version of CLIMEX,
using compare years/locations and the monthly sequence
of meteorological data from 1960 to 1990 in the WFDEI
dataset (Weedon et al. 2014) under natural rainfall condi-
tions, the resulting series of maps indicates that there is
great annual variation in the areas where EI and GI are
positive or not. In other words, in some years it would be
possible for S. exigua to both grow (positive ­GIA) and per-
sist to the following year (positive EI) in these locations,
whilst in other years both of these indices have a value of
zero. These location records therefore probably indicate
seasonal migrations and/or transient populations that did
not survive in subsequent years when climatic conditions
became unfavourable.
Journal of Pest Science
Fig. 6  Modelled climate suitability of the world for S. exigua. a Eco-
climatic Index, b Annual Growth Index (­GIA). Climate suitability
is a composite of natural rainfall and irrigation based on the irriga-
tion areas identified in Portmann et  al. (2010). Location records for
Europe, the Americas, and Africa downloaded from GBIF (6 Decem-
Discussion
Several critical issues regarding the modelling of a species’
distribution arise from our analysis of Zheng et al.’s (2012)
CLIMEX model for S. exigua. Whilst we are bound to dis-
cuss issues with this previous model, we do so in the spirit
of promoting good modelling practises.
The discrepancy between Figs. 2 and 3 in Zheng et al.
(2012) (see Figs. 2 and 1) appears to be the result of the krig-
ing process that they used on the CLIMEX output. Kriging
ber 2013); for Australia downloaded from the Atlas of Living Aus-
tralia (6 December 2013); for China were taken from Zheng et  al.
(2012); and for Baýramaly were geo-coded from Google Earth coor-
dinates. Triangles represent overwintering sites; squares represent
non-overwintering sites; crosses represent GBIF and ALA locations
is an interpolation technique used to estimate a value for an
unmeasured location. In this particular case, the CLIMEX EI
output for specific location points was interpolated to obtain
a surface of suitability. The authors state that they used this
process to provide “…a visual description showing species
ranges rather than simple points, particularly for poorly sam-
pled regions…”. However, this is not a valid methodology
to use on CLIMEX output, as kriging assumes that the spa-
tial variation in the data is homogenous across the surface,
which is not, and cannot be, the case for a climate suitability
13

model, as climate does not vary equally or evenly across any
surface. The spatial interpolation techniques used to cre-
ate gridded climate surfaces typically use thin-plate splines
that include topographic factors as covariates to account for
important processes, such as adiabatic lapse (Hutchinson
et al. 2009). The kriging process (Fig. 3 in Zheng et al. 2012)
(see Fig. 1) has produced a continuum of estimated climate
suitability, whilst the CLIMEX output based on gridded
climate data (Fig. 3 above and Fig. 2 in Zheng et al. 2012)
clearly shows an isolated patch of suitability in the central
region (site 6, Yibin, in Zheng et al. 2012). To avoid point
location mapping (Fig. 2), these authors should instead have
used any one of the many gridded climate surfaces available
(see Kriticos et al. 2012 for a discussion on other datasets
available), rather than interpolate between EI values.
Another error with Fig. 3 in Zheng et al. (2012) (see
Fig. 1) lies in the categorization of EI values. The kriging
process has produced interpolated, non-integer, EI values.
A suitable EI is designated in that paper to be any value
above 0.1, and all areas with an EI value ranging from 0.1
to five are shaded the same. In CLIMEX, an EI value of
less than one is considered unsuitable for establishment. The
classification system in Zheng et al. (2012) makes it impos-
sible to know whether sites 4 (Nanchang), 5 (Yongxiu) and
7 (Wuhan) are in fact suitable with the kriging process (see
Fig. 1): they may well have EI values less than one and be
climatically unsuitable.
Critical to model construction is the choice of appropriate
parameter values. Zheng et al. (2012) set both the soil mois-
ture threshold (SM0) and the dry stress threshold (SMDS)
excessively low, at 0.03 and 0.02, respectively. Unless there
is specific evidence to suggest that highly drought-stressed
host plants result in a herbivorous pest species doing better
(e.g. increased reproduction, more rapid development, bet-
ter survival, increased colonization), as in the case of Phe-
nacoccus manihoti (Ezumah and Knight 1978; Herren and
Neuenschwander 1991; Singh 1982), the lower soil moisture
threshold for growth (SM0) is generally set at the permanent
wilting point of plants, which for shallow-rooted crops is
around 0.1 using the CLIMEX 100 mm bucket soil moisture
model (Kriticos et al. 2003a). Similarly, the DS threshold is
normally at the same level. Setting SM0 and SMDS at 0.1
means that Baýramaly experiences a certain degree of DS
(DS = 38), which in combination with the relatively high
CS experienced here (CS = 73), is sufficient to preclude
the persistence of S. exigua under natural rainfall conditions
(both stresses combined give a total stress > 100, therefore
EI = 0). This result is clearly at odds with the fact that not
only is S. exigua a pest here, but that Baýramaly is also a
known overwintering site (Kurdov 1986).
By considering the impact of irrigation in sustaining
agriculture in certain areas, we are able to set moisture and
DS parameters that would otherwise preclude S exigua from
13
Journal of Pest Science
known locations of persistence. It is clear from both Google
Earth and Google Maps images that Baýramaly and its sur-
rounds are irrigated: Google Earth images clearly show this
area to be green by comparison to the surrounding desert,
and fed by a series of dams and rivers, and Google Maps
shows a series of rivers and dams, and numerous irriga-
tion canals through the town itself. Similarly, Google Earth
images indicate that agriculture in both Qazvin and Kho-
rasan (Iran) is sustained by irrigation. The irrigation scenario
in CLIMEX enabled us to use DS parameters to preclude the
distribution of S. exigua in these areas under natural rainfall
conditions, whilst allowing it to persist with the applica-
tion of a moderate amount of irrigation. This highlights the
importance of considering how distribution data contribute
to our understanding of a species’ biology, and of trying to
understand those aspects of the location records that make
them suitable for the persistence of an invasive species.
It is also essential to consider the choice of mechanisms
available for modelling stresses. We clearly demonstrate
that the temperature threshold mechanism of CS would
not be able to correctly distinguish between overwintering
and non-overwintering sites (Online Resource 1), although
both of the other CS mechanisms (degree-days above the
developmental threshold and average temperature) are able
to discriminate successfully between these types of sites
(Fig. 5). With the degree-day mechanism, CS accumulates
if there are fewer than the designated number of degree-days
above DV0 (developmental threshold): i.e. there is insuffi-
cient warmth. With the average temperature mechanism, CS
accumulates when the average temperature drops below the
designated threshold. This mechanism, with parameter val-
ues of TTCSA = 4 °C and THCSA = − 0.065 week−1, only
provides for marginal CS at Baýramaly (Fig. 5b), whilst the
degree-day mechanism (Table 1) provides a high level of CS
in all of the known overwintering sites (Fig. 5a), though still
allowing persistence. The degree-day mechanism is retained
because it is the more biologically reasonable, given what
is known about this species. In the first instance, it makes
no sense to use an average weekly temperature of 4 °C to
trigger CS, given the apparent cold-hardiness of S. exigua
(Jiang et al. 2001; Kim and Kim 1997; Zheng et al. 2011b).
Secondly, as Zheng et al. (2012) point out, “temperature gen-
erally affects the distribution in the north–south direction”.
The degree-day cold stress mechanism clearly does this, pro-
viding a north–south gradient in the CS (Fig. 5a), and there-
fore also in the EI values (Fig. 6a). In contrast, the average
temperature mechanism provides a very sharp delineation
between areas that do or do not experience CS (Fig. 5b),
resulting in relatively uniform EI values. So although both
mechanisms can distinguish between known overwinter-
ing and non-overwintering sites, the parameter values and
the output from the average temperature mechanism do not
accord with what we know of how S. exigua responds to low
Journal of Pest Science
temperatures or with our understanding of how CS might
affect S. exigua overwintering.
The choice of HS mechanism makes little difference to
the model. With the temperature threshold mechanism, HS
accumulates when the maximum temperature exceeds the
designated threshold. With the degree-day mechanism, HS
accumulates if the threshold number of degree-days above
DV3 (the upper threshold for development) is exceeded. As
with the Queensland fruit fly (Yonow and Sutherst 1998),
it is possible to use either mechanism to model HS in S.
exigua: the degree-day HS mechanism provides marginally
less HS in a few isolated areas of Africa and in central India,
allowing the EI value to increase by a maximum of three
units. The choice of HS mechanism and the parameter values
used are linked to the value of DV3, the upper temperature
threshold for development. With DV3 = 38 °C, there is lit-
tle to choose between the HS mechanisms given in Table 1,
and it is not evident that one mechanism should be used in
preference to the other. Were DV3 to be reduced back down
to 36 °C as per the model of Zheng et al. (2012), this would
be a different matter, and there would be a stronger argument
for using the degree-day mechanism of HS in preference to
the temperature threshold mechanism, as there would be a
4 °C disparity between DV3 (36) and TTHS (40 °C). We can
think of no biologically plausible reason that S. exigua devel-
opment would cease at 36 °C, but that HS would not begin to
accumulate until the temperature increased by another 4 °C.
The results of Guerra and Ouye (1968) indicate that there is
no difference in the egg hatching rate or development time of
S. exigua kept for varying lengths of time at 43.3 °C and then
returned to 26.7 ± 2.2 °C. It would appear therefore that it is
not high temperatures per se that are limiting, since returning
the life stages to a more moderate temperature resulted in
normal development. This argues in favour of a degree-day
mechanism of HS, where more than a designated number of
degree-days above the maximum developmental threshold
results in the accumulation of HS. Thus, whilst both HS
mechanisms produce virtually identical results, limited evi-
dence suggests that might in fact be more correct to use the
degree-day mechanism. Clearly, this is an area where more
research could help refine the model.
From the analyses on HS and CS, it is evident that the
distribution data contain a fingerprint of stress mechanisms.
Even with relatively few location records for S. exigua in
China, we were able to distinguish between CS mechanisms,
and select ones that make biological sense. Similarly, Kriti-
cos et al. (2003b) use CLIMEX to determine appropriate
mechanisms to limit the southerly distribution of prickly aca-
cia (Acacia nilotica) in Australia, and Yonow and Sutherst
(1998) examine how different CS mechanisms restrict the
distribution of the Queensland fruit fly (Bactocera tryoni).
The different HS mechanisms in CLIMEX do not differenti-
ate a species’ response as easily. Yonow and Sutherst (1998)
also obtain similar results for B. tryoni using the two differ-
ent HS mechanisms. Here, we produced virtually identical
results using both the temperature threshold mechanism and
the degree-day mechanism of HS, but selected the degree-
day mechanism because it makes more biological sense.
Nonetheless, these analyses all indicate that CLIMEX pro-
vides different ways of looking at how temperature stresses
may limit the distribution of a species, and that it is impor-
tant to consider the results and implications of each mecha-
nism. Even the small sample of Chinese overwintering and
non-overwintering locations (Zheng et al. 2012) provides
sufficient information upon which to select an appropriate
CS mechanism, again highlighting the importance of trying
to understand what distribution data are telling us about a
species’ occurrence and the stress mechanisms that limit
further expansion.
Whilst S. exigua may be precluded by climate from per-
sisting in many regions of the world (Fig. 6a), it is capable
of sustaining seasonal growth across a much larger area
(Fig. 6b). Because it is a migratory species (French 1969;
Mikkola 1970; Mitchell 1979), this analysis highlights the
very real threat that seasonal invasions could cause damage
across substantially larger areas in the future, particularly
where irrigation is practised. A vast proportion of the Amer-
icas, Europe, and Asia is modelled as having a climate suit-
able for seasonal growth of this polyphagous pest (Fig. 6b).
As CLIMEX has previously correctly predicted areas at
risk from future expansion of pests and pathogens (Hall and
Wall 1995; Kriticos et al. 2003b, 2007, 2015b; Sutherst and
Bourne 2009; Yonow et al. 2013), it will be interesting to
note if the current projections of potential range expansion
and seasonal infestation by S. exigua are proven correct.
For a pest of such significance as S. exigua, we discovered
a remarkable paucity of information on its distribution and
impacts, outside of Europe and North America, highlighting
the need for better biosecurity information infrastructure in
developing regions.
Conclusions
We have produced a new model of the potential distribution
of S. exigua that addresses the errors found in the model pre-
sented by Zheng et al. (2012). In fitting this new model, we
carefully explored both CS and HS mechanisms. We were
able to provide a biologically plausible and appropriate CS
mechanism with which to limit distribution. The new CS
parameter values correctly distinguish between known over-
wintering and non-overwintering sites in China. The ­GIA
patterns in the new model correctly identify areas where
populations cannot persist (EI = 0), but where migrations
can result in seasonal occurrences of this pest. Although we
find that both of the two HS mechanisms produce similar
13

results for this species, it is more likely that the degree-day
heat stress mechanism is constraining the range of this spe-
cies. We have adjusted other parameter values to make them
more biologically meaningful—for example, we increase the
lower soil moisture threshold so that population growth of
S. exigua does not occur below the permanent wilting point
of plants. To compensate for the increased soil moisture
threshold, we examine the impact of irrigation on reduc-
ing DS and enabling population persistence in otherwise
unsuitable environments (i.e. Turkmenistan and Iran). In
refitting parameters, we had to consider how the new values
and stress mechanisms related to the biology and ecology
of S. exigua. As the parameter values in our model are all
supported by published evidence, we have a high degree of
confidence that the model correctly characterises this spe-
cies’ response to climatic variables, and thus that projections
made outside of its known range are likely to be reason-
able. This new model highlights the potential for S. exigua
to cause damage well outside of its current known range, and
reveals a more important role for seasonal migration in the
pest risk patterns than the previous model.
Author contributions
TY did the literature survey, fitted the model, and wrote
the manuscript. DJK developed the composite irrigation
method, assisted in parameter fitting and writing the man-
uscript. NK translated the Kurdov papers and assisted in
writing the manuscript. NO generated shapefiles used in the
analyses and created all maps. All authors read, modified,
and approved the manuscript.
Acknowledgements  This work was led by InSTePP (International
Science and Technology Practice and Policy), University of Minne-
sota, and CSIRO (Commonwealth Scientific and Industrial Research
Organization, Australia), and was funded by the Bill and Melinda Gates
Foundation by way of the HarvestChoice Project. Thanks are due to
Philip Pardey and Jason Beddow for supporting the work, and to Matt
Hill and Dean Paini for comments on the draft manuscript.
Funding  Work on this Project was funded by the Bill and Melinda
Gates Foundation. Award No. 2010X446.UMN. Award title: Har-
vestChoice: Supporting Strategic Investment Choices in Agricultural
Technology Development and Adoption.
Compliance with ethical standards  tion, Rome
Conflict of interest  All authors declare that they have no conflict of
interest.
Research involving human participants and/or animals  This article
does not contain any studies with human participants or animals per-
formed by any of the authors.
Informed consent  Informed consent was obtained from all individual
participants included in the study.
13
Journal of Pest Science
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