Research Article

Received: 30 April 2019 Revised: 18 October 2019 Accepted article published: 13 November 2019 Published online in Wiley Online Library: 3 December 2019

(wileyonlinelibrary.com) DOI 10.1002/ps.5684

Potential distribution of two invasive

pineapple pests under climate change
Jiufeng Wei,a Lingfei Peng,b Zhiqiang He,c Yunyun Lua and Fang Wangd*

Abstract
BACKGROUND: The number of global invasive species has significantly increased during the past two centuries due to
globalization. The understanding of species invasion under climate change is crucial for sustainable biodiversity conservation,
community dynamics, ecosystem function, and resource distribution. Two invasive species, Dysmicoccus brevipes (Cockerell)
and D. neobrevipes (Beardsley) have greatly expanded their ranges during recent years. These insects are now considered as
extremely serious pests for various plants, especially pineapple. In addition, they are the primary vectors for pineapple wilt
associated virus. However, the potential distribution range and management strategies for these pests are unclear.

RESULTS: In this study, potential risk maps were developed for these pests with MaxEnt (maximum entropy) based on occurrence
data under different environmental variables. The potential distributions of these pests were projected for 2050s and 2070s
under three climate change scenarios as described in the Special Report on Emissions Scenarios of the Intergovernmental Panel
on Climate Change. Results showed that both pests have similar potential distributions, with high environmental suitability
in South America, Africa and South Asia. In addition, potential range expansions or reductions were predicted under different
climate change scenarios. The annual mean temperature was the most important factor, accounting for 43.4% of D. brevipes
distribution. The minimum temperature of coldest month and mean temperature of coldest quarter was found to be responsible
for 90.3% of D. neobrevipes distribution.

CONCLUSION: This research provided a theoretical reference framework to develop policies in the management and control of
these invasive pests.
© 2019 Society of Chemical Industry

Supporting information may be found in the online version of this article.

Keywords: climate change; invasive pests; MaxEnt; scale insect; species distribution model

1 INTRODUCTION The pink pineapple mealybug (PPM) was first described by

Various invasive insect species have been recently introduced to
new areas through trade and transport of goods, and have success-
fully thrived outside of their native regions.1–3 Most of these insects
are herbivores, including more than 450 alien insects that have
colonized forests and urban trees and 14% of these insects have
caused considerable damage to the trees.4 In addition, invasive
species pose considerable threats to global agriculture. Among
invasive insects, scale insects are major agricultural pests that
cause serious problems when introduced into new regions with-
out natural predators and more than 23% of the species of all
scale insects were introduced in the United States.5 The pineapple
mealybug (Hemiptera: Pseudococcidae) Dysmicoccus spp. mainly
includes two species: pink pineapple mealybug (PPM) D. brevipes
(Cockerell), and gray pineapple mealybug (GPM) D. neobrevipes
Beardsley, which pose serious threats to commercial pineapple
production.6,7 These two species are considered invasive in many
countries and are native to tropical areas in Central and South
America.8 Moreover, they exhibit quite similar external morpho-
logical characteristics, including discoidal pores near the eyes, ven-
tral multilocular pores restricted to segments VI, VII and VIII, and
absence of oral rim tubular ducts.9 Due to these similarities, the
two species have been considered as biparental and partheno-
1652
Cockerell in Jamaica on pineapple plant (Ananascomosus (L.) Merr.)
in 1893.10 PPM not only feed on ornamental plants, fruits, and
vegetable crops, but also can act as a vector for transmitting
cacao mottle leaf virus (CMLV), cacao swollen shoot virus (CSDV)
and cacao Trinidad virus (CTV).11,12 Gray pineapple mealybug
(GPM) was first reported by Beardsley in Hawaii (1959) and was
later detected in other areas, including Mexico, Sicily, and other
Neotropical countries.13,14 Tanka et al. discovered this species on
Japan’s Ishigaki Island.15 In China, GPM was first reported on sisal
∗
Correspondence to: F Wang, Hebei Key Laboratory of Animal Physiology,
Biochemistry and Molecular Biology, College of Life Sciences, Hebei Normal
University, Shijiazhuang, Hebei 050024, China. E-mail: wangf0110@163.com
a Department of Entomology, Shanxi Agricultural University, Taigu, Shanxi,
China
b State Key Laboratory of Ecological Pest Control for Fujian and Taiwan Crops,
Biological Control Research Institute, Fujian Agriculture and Forestry University,
Fuzhou, China
c College of Plant Science, Tarim University, Alar, China
d Hebei Key Laboratory of Animal Physiology, Biochemistry and Molecular

genetic forms of the same species.9 Biology, College of Life Sciences, Hebei Normal University, Shijiazhuang, China

Pest Manag Sci 2020; 76: 1652–1663 www.soci.org © 2019 Society of Chemical Industry
Potential distribution of Dysmicoccus brevipes and D. neobrevipes
hemp in the Hainan Province of China in 1998 and Guangdong and
Guangxi Province in 2008.15–17 In addition, GPM was considered
as a vector of wilt-associated viruses, which severely reduced
pineapple yields.18 Both PPM and GPM can survive on pineapple
and are primary vectors of pineapple mealybug wilt associated
virus.19 PPM is mostly found on the root, crown and lower stem of
pineapple plants, and GPM is usually observed on the upper parts
of plants, such as leaf whorls and developing fruits.7,20
Thailand, the Philippines, Brazil, China, and India are major
pineapple producers in the world. The global pineapple produc-
tion was 13 444 000 metric tons in 2000.21 The largest pineapple
production is located in Hawaii, accounting for more than half of
the global production and has an estimated value of 100 million
dollars (US).8,22 However, pineapple production is seriously threat-
ened by PPM and GPM. PPM created a serious economic prob-
lem in pineapple farming, resulting in 40% reduction in the yield
due to transmission of PMWaV-3 (Pineapple Mealybug Wilt asso-
ciated Virus-3) disease in Cuba.23 In Central Uganda, the incidence
of pineapple mealybug wilt disease ranged from 15% to 100% in
the production fields, which was observed in 2013.24 Moreover,
PPM has expanded to 126 countries outside of its native region
and has been recorded on more than 140 genera in 58 families of
plants.14 GPM afflicted serious damage to sisal hemp by inhibit-
ing its growth, leading to death. Almost 6700 ha of sisal hemp
was damaged by GMP, causing 30% production loss in the Guang-
dong province of China in 2008.17 Since 2006, GPM distribution
was increased from 2670 ha to 6700 ha in China.17 To date, GPM has
been reportedly distributed in 41 countries and feeds on 64 gen-
era in 39 families of plants, including banana, pineapple, sweet-
sop, oranges, grape.14 Thus, there is an urgent need to control and
manage these pests due to their ongoing global spread and wide
host range.
Currently, no effective control treatments have been developed
for these pests. Therefore, an alternative approach is to implement
strict quarantine measures in countries where PPM and GPM are
yet to be detected. In addition, increasing evidence suggested that
climate change will further aggravate the impacts of naturalization
and subsequent invasion of alien species into new ecosystems and
communities.25,26 Climate change can influence the distribution
and abundance of invasive insects directly (e.g., by altering the
occurrence of species and hosts) and indirectly (e.g., via changes
in population growth rates, propagule pressure, and spread).27
Therefore, modeling how climate change impacts invasive pests,
can provide vital information for controlling and managing the
spread of these pests.
Several studies have used species distribution models (SDMs)
to predict the potential impact of invasive species in order to
facilitate planning and mitigation of future impacts.28,29 In this
study, current and future potential distributions of PPM and GPM
were estimated based on occurrence data using MaxEnt software.
The objectives of this study were: (i) to identify the major climatic
variable that restricts the potential distribution of these pests; (ii)
to predict the trends of suitable habitat ranges under different
climate change scenarios; (iii) to provide a theoretical reference
framework for policy-making to manage and control these two
invasive pests.
2 MATERIALS AND METHODS
2.1 Occurrence data and sample bias
The distribution data of D. brevipes (Cockerell) and D. neobrevipes
Beardsley used in this study were obtained from the following
Pest Manag Sci 2020; 76: 1652–1663 © 2019 Society of Chemical Industry
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sources: the Centre of Agriculture and Bioscience International
(CABI, https://www.cabi.org/), the Global Biodiversity Information
Facility (GBIF, https://www.gbif.org/) and previously published
sources (see supporting information, Table S1). Accurate geo-
graphical coordinates for each distribution location were either
obtained from the literature or by using Google Earth coordinates.
Duplicate occurrences and potential errors in distribution data
(such as outside of baseline climate or baseline map) were cau-
tiously checked and excluded. Data indicating country locations
were removed, and the data referring to county, city and town
were used. One hundred and nineteen georeferenced occurrences
for PPM (42 native range and 77 invasive range points), and 40
occurrences for GPM (seven native and 33 invasive range points)
were assembled in this study.
A distribution site is usually biased to the regions that are easily
accessible for humans, or nearby cities and other areas of human
settlement.30,31 Thus, distribution site data can significantly influ-
ence the outcome of a model due to spatial autocorrelation.32,33
In order to reduce spatial autocorrelation and sample bias among
occurrence data, all occurrences for these two pests were filtered
according to workflow based on the previously described method
of Li et al.34,35 A coarse resolution (a grid cell size of 1 × 1 km, simi-
lar to the resolution of environment variables) was generated and
a single point was randomly selected from each cell that included
one or more sampling points. One hundred and nineteen locations
for PPM and 35 for GPM remained after the filtering process. The
distribution list and maps of the locations for PPM and GPM used
in this study are presented in Figure 1 and Table S2 (see support-
ing information). The workflow was conducted in ArcGIS 10.1 (ESRI,
Redlands, CA, USA) (http://www.esri.com/).
2.2 Environmental data
Climate and topographical information are the main factors used
to reflect ecological niches in environmental variables. At large
spatial scales, climatic variables are primary factors that deter-
mine species niches and have been frequently used for insect
niche modeling.28,36,37 The species distribution is usually corre-
lated with two principal climate factors, such as precipitation and
temperature at a large scale.38 The 19 climatic datasets, includ-
ing a combination of means, extremes and seasonal differences,
were obtained from WorldClim Global Climate Database (http://
www.worldclim.org) for current climate.31 Current climate condi-
tions were represented by minima, maxima and average values
of monthly, quarterly and annual ambient temperature, and pre-
cipitation values were recorded from 1950 to 2000. Topographic
variables represented by altitude (ALT) were derived from National
Geophysical Data Center (http://www.ngdc.noaa.gov/mgg/topo/
globe.html). All data were represented by 1 km2 (30 arc-seconds)
spatial resolution in the present study.
Multicollinearity among climate variables could hinder the anal-
ysis of species-environment relationships.39 Thus, Pearson’s cor-
relation coefficient was used for each pairwise comparison of all
19 environmental variables to minimize multicollinearity. Highly
correlated variables (r2 ≥ |0.8|) for PPM and GPM were removed
from original environmental variables, which filtered those below
the threshold values for final analysis (see supporting informa-
tion, Table S3-1 and S3-2). Multicollinearity was examined using
ENMTools version 1.0.40 Seven climate variables remained for
PPM: Bio1 (annual mean temperature), Bio2 (mean diurnal range),
Bio7 (temperature annual range), Bio14 (precipitation of driest
month), Bio17 (precipitation of driest quarter), Bio18 (precipitation
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of warmest quarter) and Bio19 (precipitation of coldest quarter).
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 www.soci.org J Wei et al.

Figure 1. The localities of Dysmicoccus brevipes and D. neobrevipes used in current modeling. The base map were created with Natural Earth Dataset (http://
www.naturalearthdata.com/). Gray, unsuitable habitat area; Yellow, low habitat suitability area; Blue, moderate habitat suitability area; Red, highly habitat
suitability area. (A) D. brevipes; (B) D. neobrevipes.

Similarly, six climatic variables remained for GPM: Bio1 (annual
mean temperature), Bio6 (min temperature of coldest month),
Bio11 (mean temperature of coldest quarter), Bio17 (precipitation
of driest quarter), Bio18 (precipitation of warmest quarter) and
Bio19 (precipitation of coldest quarter). In addition, the variable
altitude (ALT) was not included (note that Alt was not analyzed for
multicollinearity but was included in final analysis due to it is not a
climatic variable.
To predict the future potential distribution of these two pests
on a global scale, climatic variables for future projections (same
as current climate variables) were downloaded from WorldClim
database. Considering the uncertainty of future climate scenarios,
assessments of the impact should incorporate data from a range
of climate models that represent different climate sensitivities to
various possible future climate change projections.41,42 Thus, to
reduce this impact on global circulation models (GCMs) on which
the future climate datasets are based, an ensemble forecasting
procedure was used to estimate future distribution range.43 In this
study, three random GCMs were used: Hadley Global Environment
1654
Dynamics Laboratory Coupled Model V3 (GFDL-CM3) and the
Model for Interdisciplinary Research on Climate (MIROC5) for
the years 2050 (average for 2041–2060) and 2070 (average for
2061–2080) from the Coupled Model Inter-comparison Project
Phase 5 (CMIP5) of the fifth assessment of the International Panel
on Climate Change (IPCC).44
In 2013, the Fifth Assessment Report was published by the UN’s
Intergovernmental Panel on Climate Change (IPCC), with four rep-
resentative concentration pathways (RCPs, such as RCP 2.6, RCP
4.5, RCP 6.0 and RCP 8.5).45 Four possible greenhouse gas emis-
sion trajectories, ranging from lowest (RCP 2.6) to highest (RCP
8.5), equivalent to the increments in global radiative forcing val-
ues in the year 2100, relative to preindustrial values (2.6, 4.5, 6.0
and 8.5 w/m2 , respectively). The global mean temperature increase
ranges from 0.3 to 4.8 ∘ C across all RCPs.46 The high emission sce-
narios will likely have severe impacts on the future geographic
distribution of both PPM and GPM. Therefore, RCP 2.6 (the mini-
mum greenhouse gas emission scenario) and RCP 8.5 (the maxi-

Model 2-Atmosphere Ocean (HADGEM2-AO), Geophysical Fluid mum greenhouse gas emission scenario) for the years 2050 and

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Potential distribution of Dysmicoccus brevipes and D. neobrevipes
2070 were selected for potential distribution based on future cli-
mate variables. Overall, four climate change scenario/year combi-
nations were selected in the current study: RCP 2.6–2050 (average
for the years 2041–2060 under RCP 2.6), RCP 8.5–2050 (average for
the years 2041–2080 under RCP 8.5), RCP 2.6–2070 (average for
the years 2041–2080 under RCP 8.5), and RCP 8.5–2070 (average
for the years 2061–2080 under RCP 8.5). All future climate pro-
jection data were downloaded from the World Climate Database
(Http://www.worldclim.org/). All data used for the ENM had a spa-
tial resolution of 1 km2 (30 arc-second).
2.3 Modeling approach
Various software packages, such as CLIMEX, BIOCLIM, DOMAIN,
GARP, GLMs and GAMs have been used to simulate the poten-
tial distribution for invasive species.47 However, MaxEnt (maximum
entropy) was one of the mostly frequently used for present-only
SDMs for modeling and projecting current and future distribu-
tions of invasive species.48,49 Compared with other software (GARP,
Mahalanobis typicalities, and random forests), MaxEnt has out-
performed other methods for estimating potential species dis-
tributions, regardless of the number or geographical range of
species records.31,50 Thus, MaxEnt (version 3.4.1) was used for final
analyses.51
Feature types and a regularization multiplier were included in
MaxEnt to optimize the models and control overparameteriza-
tion. These feature types represented different transformations
of the covariates and included linear, product, hinge, threshold,
and quadratic features, allowing the software to be optimized
for selected species to prevent oversimplified or overcomplicated
models.52 The R package ‘ENMeval’, an automated method to exe-
cute models using an user-specified range of regularization mul-
tiplier (RM) value, and feature combinations (FCs) was used to
improve the performance of MaxEnt and avoid overfitting.53 The
RM range from 0.5 to 4, with the increments of 0.5 and 8 FCs,
were examined for two invasive species: (i) Linear (L); (ii) Linear
(L) and Quadratic (Q); (iii) Linear (L), Quadratic (Q) and Hinge (H);
(iv) Linear (L), Quadratic (Q), Hinge (H), and Product (P); (v) Lin-
ear (L), Quadratic (Q), Hinge (H), Product (P), and Threshold (T);
(vi) Quadratic (Q), Hinge (H) and Product (P); (vii) Quadratic (Q),
Hinge (H), Product (P), and Threshold (T); (viii) Hinge (H), Prod-
uct (P) and Threshold (T). The ENMeval package was executed in
R (v 3.1.3).54 The ‘checkerboard2’ approach was applied by cal-
culating the standardized Akaike information criterion coefficient
(AICc), and lowest delta AICc scores were selected to run the final
MaxEnt models. The results are shown in Fig. S1 and Tables S4
(see supporting information). Thus, RM = 4, and FC = LQH (Linear,
Quadratic, Hinge) were selected for D. brevipes in final software
configuration. Similarly, for D. neobrevipes, RM = 2 and FC = LQH
(Linear, Quadratic,Hinge) were selected. The logistic output of
MaxEnt was used for all analyses. The suitable and unsuitable habi-
tats or binary presence/absence maps for the two invasive species
were defined by a 10th percentile training presence logistic thresh-
old. This threshold has been widely applied in species distribu-
tion modeling, especially when data were collected by different
collectors.55 In order to explain the reasonable simulated results
of two invasive species, the potential distribution map was reclas-
sified into four levels: < threshold, unsuitable habitat (no risk);
threshold-0.4, low habitat suitability (low risk); 0.4–0.6, moderate
habitat suitability (medium risk); and 0.6–1, high habitat suitability
(high risk). Finally, 10-fold cross-validation was used to run MaxEnt
to prevent random errors from predicted samples. In addition, a
final suitability map was generated by averaging the maps from all
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Table 1. Relative contribution of each environmental variables to
Maxent model for two invasive species
Variable PPM GPM
Annual mean temperature (Bio1) 43.4 1.0
Mean diurnal range (Bio2) 6.4 –
Min temperature of coldest month (Bio6) – 80.9
Temperature annual range (Bio7) 39 –
Mean temperature of coldest quarter (Bio11) – 9.4
Precipitation of driest month (Bio14) 1.0 –
Precipitation of driest quarter (Bio17) 2.5 2.5
Precipitation of warmest quarter (Bio18) 1.4 3.1
Precipitation of coldest quarter (Bio19) 3.8 2.6
ALT 2.5 0.5
The first two most contributing environmental variables are shown in
bold
future climate scenarios in order to reduce variations among gen-
eral climate circulation models (GCMs).
2.4 Model evaluation
The area under the receiver operating characteristic curve (AUC)
has been extensively applied to measure the performance of
MaxEnt.28,29,33 However, there are disadvantages to this approach
due to equal weighting of omission and commission errors, and
even AUC cannot provide information on the spatial distribution
of model errors.56–58 Therefore, an alternative partial receiver oper-
ating characteristic (ROC) metric method was developed to evalu-
ate the model performance,59 which was implemented using the
NicheToolbox site with 1000 replicates and E = 0.05 (http://shiny
.conabio.gob.mx:3838/nichetoob2/).
3 RESULTS
3.1 Model performance for two invasive species
The model performance for both invasive species demonstrated a
significant predictive ability of partial ROC tests (see supporting
information, Fig. S2). The mean value for partial AUC at 0.05 is
0.951461 for PPM (P < 0.001) and 0.949562 for GPM (P < 0.001).
A ‘10th percentile training presence logistic threshold’ value of
0.2637 and 0.2386 were obtained for D. brevipes and D. neobrevipes,
respectively. These values indicated unsuitable habitat for both
PPM and GPM.
3.2 Environments that constrain the model
The analysis of single variable contribution showed that annual
mean temperature (Bio1) (43.4%) and temperature annual range
(Bio7) (39%) were major factors, influencing the model perfor-
mance for PPM (Table 1). Other contributing factors were mean
diurnal range (Bio2, 6.4%), precipitation of coldest quarter (Bio19,
3.8%) and precipitation of driest quarter (Bio17, 2.5%). Minimum
temperature of the coldest month and mean temperature of cold-
est quarter showed a total contribution of 90.3% for GPM. Similarly,
precipitations of warmest quarter (Bio18), driest quarter (Bio17),
and coldest quarter (Bio19) contributed to the model by 3.1%,
2.5% and 2.6%, respectively. Interestingly, altitude is less affected
in the process of forming a potential distribution map for two
pests, 2.5% for PPM and 0.5% for GPM. These results showed that
thermal conditions influenced the modeled distribution for both
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PPM and GPM much more than precipitation.
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 www.soci.org
Table 2. Area with suitability different climate scenarios (km2 )
Range Level Current RCP2.6–2050
PPM 0.2637–1 ∼4.50 × 107 ∼4.42 × 107 (−1.8%)
0.2637–0.4 ∼1.55 × 107 ∼1.53 × 107
0.4–0.6 ∼2.31 × 107 ∼2.26 × 107
0.6–1 ∼6.40 × 106 ∼6.27 × 106 (−2.0%)
GPM 0.2386–1 ∼2.20 × 107 ∼2.36 × 107 (7.2%)
0.043–0.4 ∼9.82 × 106 ∼1.17 × 107
0.4–0.6 ∼8.69 × 106 ∼8.94 × 106
0.6–1 ∼3.53 × 106 ∼2.92 × 106 (−17.2%)
3.3 Current invasive pattern
Based on distribution records and existing environmental vari-
ables, current potential distribution map of PPM and GPM are illus-
trated in Figure 1(A) and (B).
MaxEnt predictions indicated that the potential distribution
range of PPM was almost globally distributed, with the main
potential distribution areas located in South America, Africa and
Asia (Fig. 1(A)). In about approximately 4.50 × 107 km2 of the
world’s land mass, approximately 6.40 × 106 km2 (∼14.2% of total
potential invasive area) exhibited high habitat suitability (high
risk) and 2.31 × 107 km2 (∼51.3% of total potential invasive area)
showed moderate habitat suitability. In Asia, largest high habi-
tat suitability areas under current climate scenarios were located
in Southern China, Vietnam, Laos, Thailand, Burma, Malaysia, the
Philippines, a small part of India, and Indonesia. Northeastern
Australia showed high habitat suitability in the model’s projec-
tions for PPM potential distribution under current climate. In addi-
tion, Nicaragua, Costa Rica, Panama, Columbia, Uruguay, and a
small part of Brazil showed high habitat suitability within cen-
tral and South America. Further, Africa, Madagascar, Liberia, Ivory
Coast, Ghana, Nigeria, Cameroon, Congo, Angola, and south of
the Republic of South Africa also exhibited high habitat suitability
(Fig. 1(A), Table 2).
Similarly, the potential distribution map showed that all habi-
tat suitability for GPM were located from near north latitude of
40∘ to near south latitude of 33∘ , which is mainly concentrated
within Asia, Africa, and Central and South America (Fig. 1(B)).
Within approximately 2.20 × 107 km2 of this area, approximately
3.53 × 106 km2 (∼16.0% of total potential invasive area) exhibited
high habitat suitability (high risk), and 8.69 × 106 km2 (∼39.5% of
total potential invasive area) showed moderate habitat suitabil-
ity (Table 2). Southern and Central America, Southeast of Mex-
ico, Guatemala, Nicaragua, Costa Rica, Panama, Cuba, Columbia,
Venezuela, and northeast Brazil exhibited high habitat suitabil-
ity under current climatic conditions. Further, Liberia, Ivory Coast,
Ghana, Nigeria, Cameroon, Gabon, and Congo also showed high
habitat suitability within Africa. Another high habitat suitability
region was found in Southern Asia, including the Southern India,
the Southern coastal zone of China, Vietnam, Malaysia, Indonesia,
and the Philippines (Fig. 1(B),Table 2).
The response curves (Fig. 2) of distribution model of PPM indi-
cated high probability of occurrence of this species in regions
with the temperature annual range (Bio7) of 12 to 18 ∘ C, pre-
cipitation of warmest quarter (Bio18) of 400 to 1800 mL, precip-
itation of coldest quarter (Bio19) of 300 to 2700 mL,altitude of
below 300 m. However, Bio1, Bio2, Bio14 and Bio17 showed no
relation to high habitat suitability in the model for PPM. Similarly,
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there was a high probability of GPM in areas with annual mean
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J Wei et al.
RCP8.5–2050 RCP2.6–2070 RCP8.5–2070
∼4.38 × 107 (−2.66%) ∼4.41 × 107 (−2.0%) ∼3.92 × 107 (−12.8%)
∼1.58 × 107 ∼1.54 × 107 ∼1.71 × 107
∼2.21 × 107 ∼2.25 × 107 ∼2.14 × 107
∼5.8 × 106 (−10.3%) ∼6.13 × 106 (−4.2%) ∼3.92 × 106 (−38.75%)
∼2.55 × 107 (15.9%) ∼2.38 × 107 (8.1%) ∼2.99 × 107 (35.9%)
∼1.36 × 107 ∼1.18 × 107 ∼1.47 × 107
∼9.22 × 106 ∼8.99 × 106 ∼1.22 × 107
∼2.72 × 106 (−22.9%) ∼2.96 × 106 (−16.1%) ∼3.06 × 106 (−13.3%)
temperature (Bio1) of 27 to 32 ∘ C, minimum temperature of coldest
month (Bio6) of 20 to 24 ∘ C, mean temperature of coldest quar-
ter (Bio11) of 25 to 27 ∘ C, precipitation of driest quarter (Bio17)
between 180 to 650 mL, precipitation of warmest quarter (Bio18)
between 400 to 1700 mL, precipitation of coldest quarter between
480 to 2200 mL(Fig. 3). However, Alt showed no strong relation to
high habitat suitability in the model for GPM.
3.4 Future invasive area
The MaxEnt models for potential distribution of PPM and GPM
under future climate change scenarios RCP 2.6 and RCP 8.5 for the
years 2050 and 2070 are illustrated in Figures 4 and 5.
3.4.1 PPM
The total potential distribution of PPM showed that areas of suit-
ability would decrease in 2050 under emission scenario RCP 2.6 by
approximately 4.42 × 107 km2 of the world’s land mass, account-
ing for approximately 1.8% of current predicted area (Fig. 4(A) and
Table 2). Further, the total predicted range would also decrease
by approximately 3.26%, which is approximately 4.38 × 107 km2
under RCP 8.5–2050 (Fig. 4(C) and Table 2). Meanwhile, high suit-
ability areas would decrease to approximately 6.27 × 106 km2
and approximately 5.80 × 107 km2 , which appropriates to approx-
imately 2.0% and 10.3% reduction of current predicted area under
the RCP 2.6–2050 and RCP 8.5–2050, respectively.
Similarly, the potential distribution range of all suitable habi-
tats would expand to approximately 4.41 × 107 km2 under RCP
2.6–2070 (a ∼2.0% decrease compared to the current suitable
habitat). In addition, the area of high suitability habitats declined
in some regions to approximately 6.13 × 106 km2 (a decrease of
∼4.2% compared to the current range) (Fig. 4(B) and Table 2). In
2070, the potential distribution area would decrease to approx-
imately 3.92 × 107 km8 under RCP 8.5–2070 (an decrease of
∼12.8% compared to the current suitable habitat), meanwhile,
highly suitable habitat would also reduce to approximately
3.92 × 107 km6 under RCP 8.5–2070 (decrease of ∼38.75%)
(Fig. 4(D) and Table 2).
3.4.2 GPM
Under RCP 2.6, it was estimated that the total area of habitat suit-
ability would increase in 2050 and would expand to approximately
2.36 × 107 km2 (an increase of ∼7.2% over the current suitable
area) (Fig. 5(A) and Table 2). However, the potential distribution
area with highly suitable habitat decreased under RCP 2.6–2050,
with a decrease of approximately 17.2% compared to current
highly suitable habitat. MaxEnt predicted that the area of suitable
habitats under RCP 2.6 would be approximately 2.38 × 107 km7 in
Pest Manag Sci 2020; 76: 1652–1663
Potential distribution of Dysmicoccus brevipes and D. neobrevipes
Figure 2. Response curves showing the relationships between the probability of presence of Dysmicoccus brevipes and eight bioclimatic variables. Values
shown are average over 10 replicate runs: blue margins show ± SD calculated over 10 replicates.
2070, which is an increase of approximately 8.1% compared to
the current area. However, highly suitable areas would decrease
to 2.96 × 106 km6 (∼16.1% decrease) (Fig. 5(B) and Table 2).
Similarly, under RCP 8.5–2050, the potential distribution area
would increase to approximately 2.55 × 107 km2 , which is an
increase of approximately 15.9% of the current suitable area.
Yet, the potential area of distribution with highly suitable habi-
tat decreased in this scenario (a decline of ∼22.9% over the cur-
rent area) (Fig. 5(C) and Table 2). Under RCP 8.5–2070, suitable
habitat now covered approximately 2.99 × 107 km7 , showing an
increase of approximately 35.9% over the current suitable habi-
tat area. However, highly suitable area would decrease to approxi-
mately 3.06 × 106 km7 (a decrease of ∼13.3% over the current area)
(Fig. 5(D) and Table 2).
In summary, the results obtained in this study suggested that
the potential distribution of PPM would decrease and GPM would
increase under future climate change scenarios. In addition, highly
suitable habitats would decrease in most regions for both PPM and
GPM under future climate change.
4 DISCUSSION
D. brevipes (PPM) and D. neobrevipes (GPM) have been regarded
as the pests of economically important plants in some parts of
the world.6,60 These species are native to South America and are
considered potential pests for agricultural crops and forests.61
Therefore, the potential distribution maps of their expansion
are urgently needed for economic and quarantine purposes
Pest Manag Sci 2020; 76: 1652–1663 © 2019 Society of Chemical Industry
www.soci.org
worldwide, especially for Asia, Australia and Africa. The unsuitable
areas for the current distribution of these two pests showed that
they were inhibited by extreme temperatures or rainfall and these
areas are expected to either increase or decrease as the climate
changes.
In this study, the results indicated that thermal conditions were
the most important environmental variables limiting the distri-
bution map of PPM and GPM. Temperature is the driving force
for mealybug development and survival, although developmen-
tal times and thresholds might differ among species.60,61 Annual
mean temperature (Bio1) is the most important climatic vari-
able that defines the current global distribution of PPM. Previous
study on the temperature threshold for PPM demonstrated that
28.6 ∘ C was the optimal temperature for the survival of its nymphal
stage.62 However, the most suitable temperature for PPM develop-
ment was 30 ∘ C.62 Further, the mean temperature range of 8–35∘ C
were estimated for the life cycle of PPM, which suggested that
this species can thrive in different table grape-producing areas in
Brazil. The simulated results showed that PPM population would
increase within the temperature range of 12–18∘ C of a year. Labo-
ratory temperature results were different from field temperatures,
which can be attributed to the complexity of natural conditions in
field environments. The temperature values for the most suitable
climatic conditions for PPM growth and some current unsuitable
habitats (especially Yangtze River banks) may become highly suit-
able in the future because the temperature of current unsuitable
areas are increasingly hot due to global warming. On the contrary,
1657
few areas, such as Southern China and Northern Australia may
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 www.soci.org J Wei et al.

Figure 3. Response curves showing the relationships between the probability of presence of Dysmicoccus neobrevipes and seven bioclimatic variables.
Values shown are average over 10 replicate runs: blue margins show ± SD calculated over 10 replicates.

become unsuitable as a result of global warming. The reduction in
habitat suitability in these potential regions might limit the spread
and further development of PPM outside its current suitable range.
In addition, our model showed that several environmental vari-
ables could explain the current distribution of GPM worldwide. The
results of potential distribution for GPM suggested that their popu-
lation would increase at minimum temperature of 20–24 ∘ C in the
coldest month, and the mean temperature for highly suitable areas
would be 25–27 ∘ C in the coldest quarter. A lab study in China
showed that 29 ∘ C was the most suitable temperature for GPM sur-
vival from first instar nymph to adult stage. Similarly, a previous
laboratory study indicated that most suitable temperature range
for GPM was 23-29 ∘ C, which was consistent with our results.6
Another study indicated that the adult female exhibited highest
fecundity at 29 ∘ C.63 Further, Chen and his colleagues reported that
GPM population increased at 20 to 36 ∘ C, and the suitable temper-
ature for GPM development was 24 to 28 ∘ C in China.64 The map
also showed that the potential distribution model did not reveal
altitude as crucial factor for two pests (2.5% for PPM and 0.5%
for GPM).
Various studies have reported that global warming would greatly
influence species distributions by causing expansion, shifts, or
contractions in the species ranges.28,65 Our model suggested that
the proportion of both highly suitable habitat and the suitable
habitat for PPM in all four future climatic scenarios would decrease
relative to the current area (Table 2). It was observed that, for
PPM, low habitat suitability would decrease by 2070, and moderate
1658
suitable habitat and moderate suitable would increase in all four
scenarios relative to the current area. The model developed in this
study to predict the changes in PPM and GPM distribution patterns
on a global scale would provide a platform to develop monitoring
strategies to detect future infestations in currently non-infested
regions. The early warnings for invasive species spread and mon-
itoring the direction of spread are critical processes. Distribution
modeling of invasive species is a cost-effective method to iden-
tify the potential distribution areas of pests, which can help in the
development of strategies to control them within these areas.66
Our models suggested that Africa and Australia have suitable habi-
tats for the survival of GPM and Europe for PPM. However, various
data and information or hazard records have not been reported in
these regions at present. To date, GPM has not been reported in
Africa, but there was an outbreak of pineapple mealybug wilt dis-
ease in Central Uganda.67 Therefore, these areas should formulate
strict quarantine measures as in Australia and Europe, especially
within vulnerable pineapple productions that have suitable habi-
tat for PPM and GPM. However, some countries in Sub-Saharan
Africa, such as Liberia, Ivory Coast, Ghana, Nigeria, Cameroon, and
Gabon, strict quarantine policies are highly unlikely to succeed
due to limited resources.68 Early detection of new invasions is an
important step in any prevention strategy. Incomplete data on
the distribution of invasive species often hamper early detection
and other efforts to minimize their impacts.69 Citizen science is
an alternative method, which encourages the public to help col-
lect large volumes of information by conducting surveys for target

suitable habitat would decline in all four scenarios. For GPM, low invasive pest species.70 This method was effective in monitoring

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Potential distribution of Dysmicoccus brevipes and D. neobrevipes www.soci.org

Figure 4. Future species distribution models of Dysmicoccus brevipes on global scale under different climate scenarios predicted by MaxEnt. Gray,
unsuitable habitat area; Yellow, low habitat suitability area; Blue, moderate habitat suitability area; Red, highly habitat suitability area. The base map
was created with Natural Earth Dataset (http://www.naturalearthdata.com/). (A) RCP 2050-2.6; (B) RCP 2070-2.6; (C) RCP 2050-8.5; (D) RCP 2070-8.5.

new invasions and determining new areas where treatments were
required, such as South Africa,71 USA70 and Australia.72 In addi-
tion, the results showed that PPM and GPM have many overlapping
areas of potential distribution, so they can be dealt together when
Pineapple is a tropical fruit with an abundant source of vitamins
(especially vitamin C), minerals, substantial calcium, potassium
and fiber contents.73 The major pineapple growing countries in the
world are Brazil, Thailand, the Philippines, Costa Rica, China, India,
1659

developing control and quarantine measures. and Indonesia.73 Our model indicated that east of Brazil, south

Pest Manag Sci 2020; 76: 1652–1663 © 2019 Society of Chemical Industry wileyonlinelibrary.com/journal/ps
 www.soci.org J Wei et al.

Figure 5. Future species distribution models of Dysmicoccus neobrevipes on global scale under different climate scenarios predicted by MaxEnt. Gray,
unsuitable habitat area; Yellow, low habitat suitability area; Blue, moderate habitat suitability area; Red, highly habitat suitability area. The base map was
created with Natural Earth Dataset (http://www.naturalearthdata.com/). (A) RCP 2050-2.6; (B) RCP 2070-2.6; (C) RCP 2050-8.5; (D) RCP 2070-8.5.

of Thailand, the northern portion of the Philippines, Costa Rica,
South China and South India showed high potential distribution
ranges for PPM and GPM. It was further observed that the suitable
area for PPM in these countries would increase under climate
change scenarios. Both suitable area and highly suitable area
would increase in Brazil from 2050 to 2070 under the RCP-2.6.
1660
and Brazil from 2050 to 2070 under the RCP-2.6. Therefore, it
is necessary to strengthen the quarantine measures for these
two pests in these countries with large pineapple production
industries.
Interestingly, results showed that these two morphologically
similar pests could occupy similar potential distribution ranges

For GPM, the suitable area would also increase in south China with great overlap in many regions, such as South America

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Potential distribution of Dysmicoccus brevipes and D. neobrevipes
(Colombia, Venezuela, Ecuador, Eastern Brazil), Asia (Southern
India, Vietnam, Malaysia, Indonesia and the Philippines), and
Northern Australia. Further, the potential distribution area of PPM
and GPM showed high suitability in Africa. Thus, based on the
results of this study, it can be inferred that species with similar mor-
phological or phenotypic characteristics might have similar poten-
tial distributions, especially for high suitability areas.
All models in this study showed an expansion in the poten-
tial distribution range for PPM and GPM under climate change.
Results were found to be consistent with other studies, espe-
cially for invertebrates.74 Several studies suggested that some
invasive species are likely to experience range reductions due
to climate change.28,45,75 The range contractions as predicted in
this study should provide important information for the man-
agement and eradication of these two pests. Actually, reduced
climatic suitability on currently invaded areas may reduce the
competitiveness of these invasive species, which may ultimately
lead to their decline.74,76 In addition, some other abiotic and/or
biotic factors, which were not included in the models, might
have rapidly changed over time elucidating significant range con-
traction of the species. There are many factors that can influ-
ence and limit the potential distribution of invasive species. In
this study, only the constraints caused by climate variables were
considered, but other biotic factors, including host-plant avail-
ability were not considered.77 Pineapple is one of the hosts for
both GPM and PPM, thus, their distribution range is affected by
the distribution of pineapple. Human-mediated transport or trade
might be another factor, which increases the invasive risk of alien
species.78 Another possible factor is a species’ dispersal capacity,
which also influenced the distribution range of these two inva-
sive species. 72 The process of invasion itself may induce strong
selection pressure on the dispersive abilities of species, resulting
in increased dispersal during the colonization of novel regions.79,80
Interspecific interactions can also influence the accuracy of fore-
casted models by affecting the species range expansion rates.81
In addition, other variables also influence the result of simulated
models, such as geographic barriers, land use and cultivation
practices of host plants. These factors should be considered in
future research.
Control methods and reliable management strategies are key
approaches for preventing the spread of invasive species. Various
factors should be considered, including climate change, land use,
and human activity.76 Along with strict quarantine measures, other
approaches and management strategies for controlling PPM and
GPM have been proposed as follows, based on the results of
current and future potential distribution studies.
Firstly, insecticides can be an alternative method to control PPM
and GPM. Insecticides, such as soaps, tobacco extract, mercury,
sulfur, and oils have been recommended in field applications.8 It
has been reported that Sicilian lemon oil was highly effective to
control PPM.82
Secondly, the discovery of natural predators of PPM and
GPM can be an effective approach to reducing their spread.
Entomopathogenic nematodes (Heterorhabdtis indica Poliner,
Karunakar & David) have great potential to control PPM due
to their high mortality rates upon PPM infection.83 One natural
predator of GPM was evaluated for its effectiveness in controlling
GPM. On the other hand, there are 24 natural enemies belonging
to 13 genera in 7 families for PPM, including Rhinoleucophenga
capixabensi, which is a potential predator of PPM.84 However, no
biological control field studies have been performed within the
PPM infected areas.
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www.soci.org
Thirdly, PPM and GPM have been associated with various ant
species. This mutualistic relationship between ants and pineapple
mealybugs helps in increasing their population in the pineapple
fields because ants protect them from their natural enemies.85
The ant genera Pheidole and Solenopsis are mainly associated with
PPM,85 and Pheidole and Tetramorium are associated with GPM
in some areas.15 Thus, the control of ants associated with GPM
and PPM could be another strategy for their management and
treatment.86 Previous studies suggested that the control of ants
in the pineapple or crop fields can significantly reduce mealybug
populations, especially PPM.85,87
5 CONCLUSION
In brief, regions that have been invaded by PPM and GPM should
manage and control their spread through different pest manage-
ment and surveillance strategies. This study provided the first
potential distribution map of PPM and GPM based on current and
future climate scenarios. The range of suitable habitats will con-
tinue to increase under future climate conditions compared to the
current climate conditions. The present study provided a reference
to manage the pests and develop policies for their control. More-
over, strict quarantine measures should be used in areas where
PPM and GPM have not yet been reported based on the results of
current research. Different variables, such as host-plant availabil-
ity and species’ dispersal capacity should be considered in future
studies to develop a concrete strategy for the control of these inva-
sive pests.
ACKNOWLEDGEMENTS
This study was supported by the National Natural Science Foun-
dation of China (31802001) and Shanxi Agricultural University of
Science and Technology Innovation fund projects (2015YJ03).
SUPPORTING INFORMATION
Supporting information may be found in the online version of this
article.
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