insects

Article
Incidence of the El Niño–Southern Oscillation Cycle on the
Existing Fundamental Niche and Establishment Risk of Some
Anastrepha Species (Diptera-Tephritidae) of Horticultural
Importance in the Neotropics and Panama
Arturo Batista Degracia 1,2, *, Julián Ávila Jiménez 3 , Anovel Barba Alvarado 2,4, *, Randy Atencio Valdespino 2,4
and Mariano Altamiranda-Saavedra 2,5

1 Instituto de Innovación Agropecuaria de Panamá (IDIAP) PA 0739, C. Carlos Lara 157,

Ciudad de Panama 0843-03081, Panama
2 Centro de Investigaciones Agroecológicas del Pacifico Central (CIAPCP-AIP), Panama Ciudad,
Ciudad de Chitre 0601-00062, Panama; randy.atencio@gmail.com (R.A.V.);
maltamiranda2@gmail.com (M.A.-S.)
3 Facultad de Ciencias, Universidad Pedagógica y Tecnológica de Colombia, Avenida Central del Norte 39-115,
Tunja 150003, Colombia; julianleonardo.avilajimenez@gmail.com
4 Institute of Agricultural Innovation of Panama/National Research System of Senacyt-Panama,
Panama City 0816-02852, Panama
5 Grupo de Investigación Bioforense, Tecnológico de Antioquia Institución Universitaria,
Medellín 050005, Colombia
* Correspondence: arturobatista196@gmail.com (A.B.D.); anovelbarba@gmail.com (A.B.A.)

Simple Summary: Previous studies following this research allow us to contribute to the importance of
potential distribution models of species and ecological niches. The Anastrepha genus, considered one
Citation: Degracia, A.B.; Ávila of the most important at a quarantine level, demands a constant search for information to understand
Jiménez, J.; Alvarado, A.B.; different ecological dynamics. We characterised the fundamental niches of four Anastrepha species
Valdespino, R.A.; in different El Niño–Southern Oscillation (ENSO) episodes (El Niño, El Neutro and La Niña) with
Altamiranda-Saavedra, M. Incidence ecological niche modelling in NicheA software 3.0. The results of a comparison of the ellipsoids that
of the El Niño–Southern Oscillation represent the fundamental niche existing for the species showed changes in the El Niño, El Neutro
Cycle on the Existing Fundamental and La Niña episodes. Furthermore, when making a comparison between Anastrepha species and the
Niche and Establishment Risk of
different ENSO climatic episodes, we found that they share great environmental similarity between
Some Anastrepha Species
them. Finally, our results present different levels of risk of establishment of these species in the
(Diptera-Tephritidae) of Horticultural
Neotropics, which will allow us to develop efficient plans for integrated pest management.
Importance in the Neotropics and
Panama. Insects 2024, 15, 331.
Abstract: To compare the environmental space of four Anastrepha species in different ENSO episodes
https://doi.org/10.3390/
insects15050331
(El Niño, El Neutro and La Niña), we built ecological niche models with NicheA software. We
analysed the fundamental niche and the combined establishment risk maps of these species devel-
Academic Editor: Bernard D. Roitberg
oped with the ArcGisPro combine geoprocess. A comparison of the ellipsoids that represent the
Received: 3 April 2024 fundamental niche existing for the species showed changes in the El Niño, El Neutro and La Niña
Revised: 30 April 2024 episodes. For A. grandis in the El Niño vs. El Neutro episodes, there was a Jaccard index of 0.3841,
Accepted: 1 May 2024 while the comparison between the La Niña vs. El Neutro episodes presented a Jaccard index of
Published: 4 May 2024 0.6192. A. serpentina in the El Niño vs. El Neutro and La Niña vs. El Neutro episodes presented
Jaccard indices of 0.3281 and 0.6328, respectively. For A. obliqua, the comparison between the El
Niño vs. El Neutro and La Niña vs. El Neutro episodes presented Jaccard indices of 0.3518 and
0.7472, respectively. For A. striata, comparisons between the episodes of El Niño vs. El Neutro and La
Copyright: © 2024 by the authors.
Niña vs. El Neutro presented Jaccard indices of 0.3325 and 0.6022, respectively. When studying the
Licensee MDPI, Basel, Switzerland.
comparison between Anastrepha species and the different ENSO climatic episodes, we found that
This article is an open access article
distributed under the terms and
in the El Niño episode, the comparisons with the best environmental similarity were A. obliqua vs.
conditions of the Creative Commons A. striata and A. obliqua vs. A. serpentina, with higher Jaccard indices (0.6064 and 0.6316, respectively).
Attribution (CC BY) license (https:// In the El Neutro episode, the comparisons with the best environmental similarity were A. serpentina
creativecommons.org/licenses/by/ vs. A. striata and A. obliqua vs. A. striata, which presented higher Jaccard indices (0.4616 and 0.6411, re-
4.0/). spectively). In the La Niña episode, the comparisons that presented the best environmental similarity

Insects 2024, 15, 331. https://doi.org/10.3390/insects15050331 https://www.mdpi.com/journal/insects

Insects 2024, 15, 331 2 of 16

were A. obliqua vs. A. serpentina and A. obliqua vs. A. striata, with higher Jaccard indices (0.5982 and
0.6228, respectively). Likewise, our results present the risk maps for the establishment of these species
throughout the Neotropics, allowing us to predict the level of risk in order to develop integrated pest
management plans.

Keywords: Anastrepha grandis; A. serpentina; A. obliqua; A. striata; distribution

1. Introduction
Studies on how environmental conditions vary at different temporal and spatial scales
have increased in recent years [1–3]. It is argued that the use of the word “niche” in an
ecological context has theoretical bases, from 1917 to the present [4–8]. For this reason,
niche studies are constantly updated and evolving, and insect species of the Tephritidae
family, faced with this climatic variability, can vary their establishment patterns since they
inhabit a wide variety of environments [9]. The family Tephritidae, to which the fruit
fly belongs, is the most economically important, comprising approximately 4000 species
distributed in tropical and subtropical areas [10–12]. Those known as fruit flies belong to
various genera, including Dacus, Rhagoletis, Ceratitis, Bactrocera, Anastrepha and Zeugoda-
cus [13,14]. Seven Anastrepha species are economically important in the Neotropical region
due to their wide range of commercial host plants and distribution. These species include
Anastrepha ludens (Loew) (Mexican fruit fly), A. obliqua (Macquart) (the West Indian fruit fly),
A. fraterculus (Wiedemann) (South American fruit fly), A. suspensa (Loew) (Caribbean fruit
fly), A. serpentina (Wiedemann) (Sapotaceas fly), A. striata Schiner (guava fly) and A. grandis
(Macquart) (melon fly) [15]. These flies cause direct physical damage to the fruit pulp due
to larvae and secondary damage caused by the entry of pathogenic microorganisms. There
are also indirect implications, such as quarantine measures and export restrictions, thus
limiting the development of various economies dedicated to fruit production [16–19].
Insects are vulnerable to extreme climate variability and fluctuations in climate com-
ponents, such as temperature and precipitation, during certain periods of time [20]. Heat
waves and seasonal temperature variations affect the development, movement, repro-
duction and behaviour of many organisms [21]. In recent years, insects have become a
good model for evaluating the relationship between variations in environmental temper-
ature and various traits of their life history [22]. This has allowed researchers to predict
their responses to global warming and understand the physiological mechanisms that
allow them to cope with temperature variations, such as changes in respiration, the use
of antioxidants and certain proteins that protect them from heat [23]. Furthermore, the
effects on their life cycles, genetic composition, hybridisation, distribution, and popula-
tion abundance have been determined [24]. This is particularly true for members of the
Tephritidae family, who inhabit a wide variety of environments [10–12]. In recent years, the
production of fruits and vegetables has intensified considerably because of new patterns in
the international economy (characterised by the globalisation of markets and technological
development), changes in consumption patterns and competition between the different
actors involved [25]. The harvested area of fruits and vegetables has grown worldwide in
the last 30 years, reaching an average annual growth rate (AGR) of 3.33% between 1990
and 2019 [26–28].
Recent studies by the Atlantic Oceanographic and Meteorological Laboratory (AOLM)
of the National Oceanic and Atmospheric Administration (NOAA) project variations in the
El Niño–Southern Oscillation (ENSO) cycle due to the accumulation of greenhouse gases.
The greenhouse effect predicts global climate impacts on temperatures and precipitation
towards the second half of the 21st century [29]. Furthermore, a future pattern of changes in
sea surface temperature (SST) equal to the La Niña phenomenon will increase the zonal tem-
perature gradient and zonal advective feedback in the central equatorial Pacific, potentially
increasing the frequency and amplitude of strong events of the El Niño phenomenon [30].
Insects 2024, 15, 331 3 of 16

It is expected that, over the next few years, climate variability will cause alterations in the
geographical distribution of insects because of the rearrangement of climatic zones [31,32].
Therefore, the magnitude of these impacts will be associated with the phenomenon of
climate variability. The regions of Latin America, South America and the Caribbean are
among the most vulnerable areas to climate variability since the majority of the species that
live there are endemic or restricted to a specific tropical ecosystem [33–36]. Evaluations
of how the environmental space available for a species can change in the face of climate
variability can be used to improve integrated pest management (IPM) plans and production
systems in different countries. Therefore, it is relevant to understand the impact of the
ENSO on the ecological niche of Anastrepha species in the Neotropics and Panama. Due to
the above, we have developed work on the potential distribution of these species in order
to form groups of recordings on this topic and strengthen their applications in the scientific
field [37].

2. Materials and Methods

2.1. Investigation Area
The study area was defined in the American Neotropics due to the economic impor-
tance of fruit activities and the occurrence of the species to be studied [8,38–40]. For spatial
analyses, we used the ecoregion maps of the World Wildlife Fund (WWF), and the extension
area between latitudes 30◦ N and 30◦ S was defined [37,41–45].

2.2. Species Presence

We used four species of the genus Anastrepha as study models (A. grandis, A. serpentina,
A. obliqua and A. striata) due to their importance in horticulture at the Neotropical level
and the need to understand their environmental requirements [37,46–48]. We obtained
records of the presence of these species from the following sources: the Global Biodiversity
Information Facility (GBIF), Species Link, the Centre for International Agricultural Bio-
science (CABI) and the National Directorate of Plant Health of the Ministry of Agricultural
Development (MIDA) [37,49,50].

2.3. Climate Data

We analysed climate information in the Pacific Ocean from agencies specialising in
atmospheric variability phenomena, which are the cause of uncertainty in environmental
patterns today [37]. The agencies included NOAA in the United States (National Weather
Service, Los Angeles, CA, USA, 2018), the Australian Government Meteorological Office
(Bureau of Meteorology, Melbourne, Australia, 2018) and the Tokyo Climate Center in
Japan (Japan Meteorological Agency, Tokyo, Japan, 2019). The information analysed from
2000 to 2019 allowed these 3 agencies to reach a consensus: 5 El Niño episodes, 3 Neutral
episodes and 6 La Niña episodes [37]. These episodes were characterised by four rasters
(minimum, maximum, medium and range), for which each of the environmental layers
included the improved vegetation index (EVI, monthly Modis-Terra MOD 11C2v006), the
temperature of land surface (LST, Modis-Terra MOD 11C3v006 monthly), the near-real-time
precipitation rate (NRTPR, 3 h TRMM 3B42RTv7) and the normalised differential vegetation
index (NDVI, Modis-Terra MOD 11C2v006 monthly). We selected these variables based on
knowledge of the biology and natural history of the species, and 16 environmental layers
were created for each episode with a spatial resolution of 0.25◦ or 25 km at the equator,
allowing us to evaluate the behaviour of the ENSO cycle episodes [51–59].

2.4. Characterisation of the Existing Fundamental Niche

To compare the environmental space of the four Anastrepha species in the different
ENSO episodes (El Niño, El Neutro and La Niña), we built ecological niche models with
NicheA software ver 3.0, defining them as ellipsoids of minimum volume on an envi-
ronmental background represented by a cloud of points in a three-dimensional grilled
plane. NicheA first represents the studied space and constructs ellipses with the available
Insects 2024, 15, 331 4 of 16

occurrences as approximations of all the suitable environments of a species [60,61]. By

projecting this ecological background with the 16 environmental variables of each episode,
8 datasets were constructed using the following criteria for selection: all variables (set 1);
a Pearson’s correlation coefficient analysis to reduce collinearity (set 2) [57], where vari-
ables with a correlation value >|0.8| were removed using the corrplot package of R 3.6.0
statistical software [58,59]; a Jackknife analysis in MaxEnt [62] to assess the individual
contribution of variables without spatial autocorrelation to the models, which included
variables contributing ≥80% (set 3) [59]; variables with a variance inflation factor (VIF)
<10 (set 4); all variables related to the NDVI (set 5); all variables related to the EVI (set 6);
all LST-related variables (set 7); and all variables related to precipitation (set 8). The en-
vironmental dataset that met the selection of optimal parameterisations according to the
Kuenm package [63] was sectioned to represent the environmental space of the species in
each climatic episode. Subsequently, these were cut to the extent of the Neotropical region,
being individually normalised to avoid the effect of the scale of each of them in the 3D
representation (sequence in NicheA software [64]: >> Toolbox >> Utility Functions >> Nor-
malisation/standardisation of variables), and with these, a principal component analysis
(PCA) was created (sequence in NicheA software: NicheA >> Toolbox >> Background data
> Component analysis main). Finally, this PCA was uploaded to NicheA to generate the
background in the 3D representation (sequence in NicheA software: NicheA >> Toolbox >>
Background data >> Draw Background Cloud Folder).
When characterising the niches of the species in each of the ENSO episodes, the
occurrences were loaded (sequence in NicheA software: NicheA >> Toolbox >> Niche
appearance >> Generate N(s) from occurrences) to design the corresponding folder that
contained the niche attributes for each species in each context. Afterwards, the resulting
folder was loaded in the background (sequence in NicheA software: NicheA >> Toolbox
>> Niche Appearance >> Open N(s)) to graphically describe the realised niche through a
minimum-volume ellipsoid representing the realised niche, and the points represent the
environmental values of the episodes. To evaluate whether there were changes in the niches
of the species, in the different episodes evaluated, the environmental spaces of each of
these species built in the different episodes were set up on the background of the El Neutro
episode, which was taken as a reference for all species comparisons. The result was three
ellipsoids of minimum volume for each species: one for the El Niño episode, one for La
Niña and another for average Neutral conditions. The comparison was performed using
the niche overlap function (sequence in the NicheA software: NicheA >> Toolbox >> Niche
Analysis Tools >> Quantify Niche Overlap), which performs paired contrasts by calculating
the volumes of the ellipsoids and the portion of these that overlap in the multidimensional
space. In addition, a modified Jaccard index was used to quantify niche overlap.

2.5. Establishment Risk Maps

Establishment risk maps were created with the product of binary maps that repre-
sented the potential distribution of each species in each climate episode [37,65–68]. By
developing combined maps using the ArcGisPro combine geoprocess [69,70], this process
generated a table of information for each created raster. Using the combinations of the
Neutral episode, which is the one that presents the greatest number of combinations, the
list of classes was produced and used to reclassify the three rasters using the reclassify
geoprocess. An attempt was made to establish an order based on the names of the species
(grandis, obliqua, serpentina and striata) according to the order in which they were combined.
This established 16 possible combinations, which were then numbered for reclassification.
New reclassification values were obtained, with which the shapes or layers were reclassi-
fied. When converting the classified raster layers to vector or shape file format to better
work on the arrangement or grouping of classes, the raster to polygon geoprocess was
used. When converting to vector data or shape files, thousands of polygons were generated
for the 16 classes. After obtaining the shape files, the generated polygons were dissolved
using the dissolve geoprocess. New fields were then added to the data tables of the three
 reclassified. When converting the classified raster layers to vector or shape file forma
better work on the arrangement or grouping of classes, the raster to polygon geopro
Insects 2024, 15, 331 was used. When converting to vector data or shape files, thousands of polygons
5 of 16 were
erated for the 16 classes. After obtaining the shape files, the generated polygons were
solved using the dissolve geoprocess. New fields were then added to the data tables o
threeto
dissolved shapes dissolved
describeshapes to describe
the 16 classes and the 16 classes
to create newand to for
maps create
thenew maps for
Neotropics the Neotro
and
and
Panama [71–73]. Panama [71–73].

3. Results 3. Results
The comparison The of the ellipsoids
comparison thatellipsoids
of the represent that
the fundamental
represent theniche existing for
fundamental the existing
niche
species showed changes in the El Niño, El Neutro and La Niña episodes. For A.
the species showed changes in the El Niño, El Neutro and La Niña episodes. For A. gra grandis
in the El Niño vs. ElElNiño
in the Neutro episodes,
vs. El there wasthere
Neutro episodes, a Jaccard
was a index
Jaccardofindex
0.3841,
of while
0.3841,the
while the c
comparison parison
betweenbetween
the La Niña
the Lavs.Niña
El Neutro episodes
vs. El Neutro presented
episodes a Jaccard
presented index index
a Jaccard of of 0.6
0.6192 (Figure 1A). Anastrepha
(Figure serpentina
1A). Anastrepha in theinElthe
serpentina Niño vs. Elvs.
El Niño Neutro and La
El Neutro andNiña vs. Elvs. El Ne
La Niña
Neutro episodes presented
episodes Jaccard
presented indices
Jaccard of 0.3281
indices and 0.6328,
of 0.3281 respectively
and 0.6328, (Figure
respectively 1B). 1B). Fo
(Figure
For A. obliqua,
obliqua, the comparison between the El Niño vs. El Neutro and La Niña vs. El
the comparison between the El Niño vs. El Neutro and La Niña vs. El Neutro
Neutro episodes
sodespresented
presentedJaccard
Jaccardindices
indicesofof0.3518
0.3518andand0.7472,
0.7472,respectively
respectively(Figure
(Figure1C).
1C). For A.
For A. striata,ata,
comparisons
comparisons between
betweenthethe
episodes
episodesof of
El El
Niño
Niñovs.vs.
ElEl
Neutro
Neutroand LaLa
and Niña
Niña vs.vs. El Ne
El Neutro presented
presented Jaccard
Jaccardindices of of
indices 0.3325 and
0.3325 and0.6022, respectively
0.6022, (Figure
respectively 1D).
(Figure 1D).

Figureecological
Figure 1. Estimated 1. Estimated
nicheecological
models forniche modelsgrandis
Anastrepha for Anastrepha grandis (A),
(A), A. serpentina (B), A.
A. serpentina
obliqua (C)(B), A. ob
(C) and
and A. striata (D) andtheir
A. striata (D) and their
superposition superposition
in environmental in environmental
space. space.
The axes are the mainThe axes are the main c
components
ponents of the 16 bioclimatic variables that describe the background of average
of the 16 bioclimatic variables that describe the background of average conditions of the projection conditions o
projection area, and the ellipsoids represent El Niño (blue), El Neutro (yellow), La Niña (green)
area, and the ellipsoids represent El Niño (blue), El Neutro (yellow), La Niña (green) and niches in
niches in the respective average conditions.
the respective average conditions.

When making the comparison between Anastrepha species and the different ENSO
climatic episodes, we found that in the El Niño episode, the comparisons with the best
environmental similarity were A. obliqua vs. A. striata and A. obliqua vs. A. serpentina,
 Insects 2024, 15, x FOR PEER REVIEW 6

Insects 2024, 15, 331 6 ofdifferent

16
When making the comparison between Anastrepha species and the EN
climatic episodes, we found that in the El Niño episode, the comparisons with the
environmental similarity were A. obliqua vs. A. striata and A. obliqua vs. A. serpentina, w
with higher Jaccard indices (0.6064
higher Jaccard indices and 0.6316,
(0.6064 andrespectively) (Figure 2A).
0.6316, respectively) In the
(Figure 2A).ElIn
Neutro
the El Neutro
episode, the sode,
comparisons with the best environmental similarity were A. serpentina
the comparisons with the best environmental similarity were A. serpentina vs. vs
A. striata andstriata
A. obliqua vs. A. striata, which presented higher Jaccard indices (0.4616
and A. obliqua vs. A. striata, which presented higher Jaccard indices (0.4616and
0.6411, respectively) (Figure 2B). In(Figure
0.6411, respectively) the La Niña episode,
2B). In the La the comparisons
Niña episode, thethat presented the
comparisons that prese
best environmental similarity were A. obliqua vs. A. serpentina and A. obliqua
the best environmental similarity were A. obliqua vs. A. serpentina vs. A. striata,
and A. obliqua vs
with higher Jaccard indices
striata, with (0.5982
higher and 0.6228,
Jaccard indicesrespectively) (Figurerespectively)
(0.5982 and 0.6228, 2C). (Figure 2C).

Figure 2. Estimated
Figure ecological niche
2. Estimated ecological for Anastrepha
models niche models forspecies and overlap
Anastrepha speciesinand
environmental
overlap in environm
space. The axes are principal
space. The axescomponents
are principalofcomponents
16 bioclimatic variables
of 16 that variables
bioclimatic describe the
thatbackground
describe the backgro
of average conditions
of averageof the El Niñoof(A),
conditions theElElNeutro (B) El
Niño (A), and La Niña
Neutro (B)(C)
andprojection
La Niña (C)areas, and theareas, and
projection
ellipsoids
ellipsoids represent represent
the species the species
A. grandis A. grandis
(yellow), (yellow),
A. serpentina A. serpentina
(green), (green),
A. obliqua (blue) andA.A.obliqua
striata (blue) an
(red) under thestriata (red) under
respective averagethe respective average conditions.
conditions.

When
When analysing theanalysing
risk mapstheforrisk
themaps for theinneotropics,
neotropics, the El Niñoinevent,
the El the
Niño event,
high riskthe high
levels in the combination of A. grandis,of
levels in the combination A.A.obliqua and
grandis, A.A. striataand
obliqua occurred in central
A. striata Mexico,
occurred in central Mex
central Guatemala,
central the western coastal
Guatemala, area of
the western Colombia,
coastal area ofeastern Brazil,
Colombia, coastal
eastern areascoastal
Brazil, of area
Peru and thePeru
central
andarea of Argentina.
the central area of The combination
Argentina. of A. grandis,
The combination A. grandis,
of A. serpentina and
A. serpentina an
A. striata occurred in western Guatemala, central Colombia, southern Peru, western central
Bolivia, southeastern Brazil, southern central Uruguay, central Chile and the central part of
eastern Argentina. The combination of A. obliqua, A. serpetina and A. striata was present
Insects 2024, 15, 331 7 of 16

in points in the north, west and south of Mexico, the west coast of Guatemala, north
Nicaragua, north Costa Rica, central Panama, north Colombia and Venezuela, central and
southern Brazil and northern central Argentina. The very high risk level of establishment
in all combinations of A. grandis, A. obliqua, A. serpentina and A. striata was present in
Insects 2024, 15, x FOR PEER REVIEW
southeastern Mexico, Guatemala, Belize, northern Honduras, Nicaragua, northern 8 ofCosta
16
Rica, much of Panama, Colombia, Venezuela, Ecuador, Peru, Guyana, Suriname, Brazil,
southern Bolivia, Paraguay, northern Argentina and Uruguay (Figure 3A).

Figure3.3.Combined
Figure Combined risk risk maps
maps of of establishment
establishmentfor Anastrephaspecies
forAnastrepha species
in in
thethe American
American Neotropics,
Neotropics,
ininepisodes
episodes of El Niño
of El Niño(A),(A),
El El Neutro
Neutro (B) (B)
and and
La Niña La Niña (C).
(C). The The legend
legend specifiesspecifies the following:
the following: draw-
drawing—border of countries,
ing—border of countries, colours—Anastrepha
colours—Anastrepha species,species, numbers—level
numbers—level of establishment,
of risk of risk of establishment,
and
united
and unitedletters—different
letters—different species. Synthesis:
species. grey—No
Synthesis: grey—No Data, black—0,
Data, NP—No
black—0, NP—No Presence; letters:
Presence; letters:
GR—A.grandis,
GR—A. grandis,OB—A.
OB—A. obliqua,
obliqua, SE—A.
SE—A. serpentina,
serpentina,ST—A.
ST—A.striata.
striata.Numbers
Numbers with different
with colours
different colours
represent the level of establishment risk of the species: 1, green—low establishment risk; 2, low to
represent the level of establishment risk of the species: 1, green—low establishment risk; 2, low to high
high shades of blue—medium establishment risk; 3, low to high shades of orange—high establish-
shades of blue—medium
ment risk; 4, red—very high establishment
establishment risk;
risk.3, low to high shades of orange—high establishment
risk; 4, red—very high establishment risk.
By analysing the cut for Panama, it was found that medium risk levels of establish-
mentIn were
the Elpresented
Neutro event,in thea El
high
Niñoriskepisode
of establishment was presented
with the combination of A.bygrandis
the combination
and A.
A. grandis,
ofserpentina A. obliqua and A. serpentina in coastal areas of the Yucatán
in western Panama (Bocas del Toro). A high irrigation level was observed and western Mexico,
with
central Guatemala,
the combination of central eastern
A. grandis, Panama,
A. obliqua and A. northern
serpentinapoints
in thein Colombia
coastal centreand Venezuela,
in Bocas del
northern
Toro, theand southern
north of Colon,Brazil,
andmuch of Guyana,
San Blas; with theand southern of
combination Suriname.
A. grandis,The
A. combination
serpentina
A. grandis,
ofand A. striataA.inobliqua and A. striata
the northwest part ofoccurred
Chiriquíinand central Mexico
southwest and del
Bocas Guatemala,
Toro; andnorthern
with
Peru, eastern Brazil, southern Bolivia and a large part of central
the combination of A. obliqua, A. serpentina and A. striata in central-west Bocas western Argentina.
del Toro,The
combination A. grandis,
south-centralofChiriquí, the A. serpentina
central zone inand A. striataHerrera,
Veraguas, occurred inSantos,
Los northwest
and Guatemala,
coasts of
southern
Coclé and Peru,
Panamamuch of Uruguay,
Oeste. Very highand eastern Argentina,
establishment risk levelsand thefound
were combination of A. obli-
with all combi-
qua, A. serpentina
nations of species andin A.
thestriata occurred
provinces in much
of Darién, of Mexico,
Panamá, Colon, northern
PanamáGuatemala,
Oeste, northBelize,
of
Honduras,
Coclé, north central Salvador
and south and Nicaragua,
of Veraguas, south of Los central Costa
Santos, andRica,
muchwestern
of Bocascentral
del ToroPanama,
and
northern
Chiriquíand central
(Figure 4A).Colombia and Venezuela, western Ecuador, the eastern centre of Brazil
and eastern
In the Argentina. A very high
El Neutro episode, risk of
the level level
lowofrisk
establishment in thewas
of establishment Neotropics
presented was
forfound
A.
serpentina
with in the southwest
the combination of the of
fourBocas del Toro,
species and a medium
in southern risk level
Mexico, central was presented
Guatemala by
and Belize,
a the
largecombination of A. grandis
part of Honduras and A. striata
and Nicaragua, in theCosta
central northRica
centre
andofPanama,
Los Santos, south
a large of of
part
Herrera and the central coast in Panama. A high level of establishment
central and south of Colombia and Venezuela, central Guyana, Suriname, French Guiana, risk was presented
by the combination
north-central of A. grandis,
and southern A. obliqua
Brazil, and A.Peru,
east-central serpentina in east-central
north-central Bocas
Bolivia, del Toro,
southeastern
north and south-central Veraguas, southwest and northeast
Paraguay, north-central Argentina and northwest Uruguay (Figure 3B). Colon, north-central Panama
andIn San Blas, and some points of north and south Darién and by the
the La Niña event, a high risk of establishment was presented by the combination combination of A.
of A. grandis, A. obliqua and A. striata in south-central Mexico, central Guatemala, and
obliqua, A. serpentina and A. striata in southwest and east Bocas del Toro, north-central south-
south
west Chiriquí, northeast
Colombia, central Veraguas, northwest
and coastal areas Coclé,
of Peru south
and Los Santos,
Chile, the coastal
southwest centre
Brazil, muchin of
Panama, and northwest Darién. A very high risk of establishment in all species occurred
in a large part of the territory of Chiriquí, Bocas del Toro, Veraguas, Coclé, Herrera, Los
Santos, Western Panama, southeastern Panama and north-central Darién (Figure 4B).
In the La Niña episode, a low risk of establishment was presented by A. serpentina in
the southwest of Bocas del Toro, and a level of medium risk was presented by the
Insects 2024, 15, 331 8 of 16

Argentina, and west-central Uruguay; by the combination of A. grandis, A. serpentina and

A. striata in central Chile, east-central Argentina, southern Uruguay and Brazil; and by
the combination of A. obliqua, A. serpentina and A. striata in coastal and central areas of
Mexico, coastal areas of Guatemala, Salvador, northern Nicaragua, central and northwest
Costa Rica, central Panama, central-northern Colombia and Venezuela, southwest Ecuador,
central-west and east Brazil, southern Bolivia, much of Paraguay, and northern Argentina.
Combinations of a very high risk of establishment with all species were found in central
and southern areas of Mexico; a large part of Guatemala, Belize, Honduras, Nicaragua,
Costa Rica and Panama; northern and southern Colombia and Venezuela; a large part of
Guyana, Suriname, and French Guiana; much of north-central and southern Brazil; Peru;
Bolivia; southern Paraguay and east-central Brazil (Figure 3C).
By analysing the cut for Panama, it was found that medium risk levels of establishment
were presented in the El Niño episode with the combination of A. grandis and A. serpentina
in western Panama (Bocas del Toro). A high irrigation level was observed with the combi-
nation of A. grandis, A. obliqua and A. serpentina in the coastal centre in Bocas del Toro, the
north of Colon, and San Blas; with the combination of A. grandis, A. serpentina and A. striata
in the northwest part of Chiriquí and southwest Bocas del Toro; and with the combina-
tion of A. obliqua, A. serpentina and A. striata in central-west Bocas del Toro, south-central
Chiriquí, the central zone in Veraguas, Herrera, Los Santos, and coasts of Coclé and Panama
Oeste. Very high establishment risk levels were found with all combinations of species in
the provinces of Darién, Panamá, Colon, Panamá Oeste, north of Coclé, north and south of
Veraguas, south of Los Santos, and much of Bocas del Toro and Chiriquí (Figure 4A).
In the El Neutro episode, the level of low risk of establishment was presented for
A. serpentina in the southwest of Bocas del Toro, and a medium risk level was presented
by the combination of A. grandis and A. striata in the north centre of Los Santos, south of
Herrera and the central coast in Panama. A high level of establishment risk was presented
by the combination of A. grandis, A. obliqua and A. serpentina in east-central Bocas del
Toro, north and south-central Veraguas, southwest and northeast Colon, north-central
Panama and San Blas, and some points of north and south Darién and by the combination
of A. obliqua, A. serpentina and A. striata in southwest and east Bocas del Toro, north-central
and south Chiriquí, central Veraguas, northwest Coclé, south Los Santos, the coastal centre
in Panama, and northwest Darién. A very high risk of establishment in all species occurred
in a large part of the territory of Chiriquí, Bocas del Toro, Veraguas, Coclé, Herrera, Los
Santos, Western Panama, southeastern Panama and north-central Darién (Figure 4B).
In the La Niña episode, a low risk of establishment was presented by A. serpentina
in the southwest of Bocas del Toro, and a level of medium risk was presented by the
combination of A. grandis and A. striata in the centre of Coclé. A high irrigation level was
presented by the combination of A. grandis, A. obliqua and A. serpentina in northeast and
west Colon, central San Blas, points in central, east, and west Panama, and north-central
Darién. A very high risk of establishment for all species occurred in a large part of Bocas
del Toro, Chiriquí, north and south Veraguas, south Los Santos and Herrera, a large part of
Coclé, Panama Oeste, Panama and Darién (Figure 4C).
 presented by the combination of A. grandis, A. obliqua and A. serpentina in northeast and
west Colon, central San Blas, points in central, east, and west Panama, and north-central
Darién. A very high risk of establishment for all species occurred in a large part of Bocas
del Toro, Chiriquí, north and south Veraguas, south Los Santos and Herrera, a large part
Insects 2024, 15, 331 of Coclé, Panama Oeste, Panama and Darién (Figure 4C). 9 of 16

Combinedmaps
Figure4.4.Combined
Figure mapsofofrisk
riskof
ofestablishment
establishment for Anastrepha species in
for Anastrepha in Panama
Panama ininepisodes
episodesofofEl
ElNiño
Niño(A),
(A),ElElNeutro
Neutro(B)(B)
andand
LaLa Niña
Niña (C).(C).
TheThe legend
legend specifies
specifies the following:
the following: white
white quadrant—
quadrant—border
border of provinces,
of provinces, pink quadrant—Colombia,
pink quadrant—Colombia, creamcream quadrant—Costa
quadrant—Costa Rica, colours—Anastrepha
Rica, colours—Anastrepha species,
species, numbers—establishment risk level, joined letters—the different species. Synthesis:
numbers—establishment risk level, joined letters—the different species. Synthesis: grey
grey colour—No
Data; black colour—0; SP—No Presence; letters: GR—A. grandis, OB—A. obliqua, SE—A. serpentina,
ST—A. striata. Numbers with different colours represent the level of establishment risk for the species:
1, green—low establishment risk; 2, low to high shades of blue—medium establishment risk; 3, low
to high shades of orange—high establishment risk; 4, red—very high establishment risk.
Insects 2024, 15, 331 10 of 16

4. Discussion
Changes in the distribution and niche of species in relation to climatic variability and
anthropogenic effects are occurring in leaps and bounds; therefore, studies on this research
topic are becoming increasingly important [74–77]. We characterised the changes in the ex-
isting fundamental niches for four species of the genus Anastrepha with occurrences during
El Niño, El Neutro and La Niña episodes and found that these species have the potential
to occupy different ecological spaces depending on the climatic ENSO scenario [37,78–80].
It is possible that aspects inherent to the biology of different Anastrepha species, such as
the interaction with biotic variables, such as host plants, competing organisms, parasitoids,
and predators, and local abiotic elements of the area accessible for the establishment of the
insect, influence the niche breadth in response to the climatic variations of a locality [22,76].
There is an information gap associated with the host of the native species of Anastrepha in
Central America since these native species have been little studied and their parasitoids are
unknown [81]. There are a limited number of investigations that evaluate biotic and abiotic
interactions; in Panama they do not exist, and in other regions of the Neotropics they are
few (Mexico and Colombia) [82]. Our results for the four species showed changes in the con-
figuration of the ellipsoids, as these species can adapt to survive. With these environmental
variations regulating their physiological functions, depending on the ecological zone and
according to the climatic episode, they could compete for resources in certain locations
that they were not previously established [22]. The results demonstrated that the niches
of the species evaluated share certain similarities in the shape and size of the occupied
environmental space represented by the ellipsoids. These overlaps increase in El Neutro
vs. La Niña events, in which these species manage to improve their fitness mainly via
reproduction (longevity, better oviposition and fertile eggs) [77,83,84] and by being located
in geographical areas in the Neotropics with stable temperature and environmental humid-
ity conditions and with great biodiversity of specific and temporary host plants [85–87].
El Neutro vs. El Niño events presented similarities in the niche volume, which changed,
decreasing the overlap. These ellipsoids represented only a portion of the fundamental
niche due to the increase in temperatures and dry and arid conditions (such as desert areas,
steppes or the Andes Mountain range), with scarce rainfall that restricts the expansion of
species by affecting their reproductive biology at various stages (death of adults) and a
decrease in the range of specific host plants [77,88,89]. On a practical level, these changes
presented in the different climatic events will guide and strengthen decision making in
IPM plans in the case of various species of fruit flies of the genus Anastrepha, which are
of interest to various institutions associated with pest management at the international
level [90]. Some fruit fly species, such as A. striata, can present a certain plasticity to changes
in climatic conditions, maintaining or expanding their environmental space in different
episodes and becoming a more competitive species for resources [22,91].
The overlap between the studied fruit fly species during the different ENSO episodes
presented niches within an environmental space defined according to their ellipsoids. Some
presented greater or lesser overlap, indicating that a certain number of species are affected
during the El Niño and El Neutro episodes by competing for the same trophic resources
if they maintain the same specific or alternative host plants and if they are influenced by
the same climatic conditions (temperatures between 20 and 30 ◦ C, average humidity of
75%) [22,91]. Under these abiotic and biotic precepts, A. obliqua and A. striata maintain
their greater overlapping capacities in different geographical areas based on Hutchinson’s
theory of duality, according to the ellipsoid corresponding to the species [89,92]. In the
La Niña episode, species such as A. serpentina presented changes in the overlap, which
could be due to high temperatures (35 ◦ C), greater humidity and excessive precipitation
at an ecological level [92,93]. All the information generated and compiled allows contin-
gency plans to be organised for the control of insect pests, thereby optimising regional
economic resources [94]. Furthermore, previous studies demonstrate that these species
have a high degree of environmental suitability in the neotropics, thus corroborating the
present study [37].
Insects 2024, 15, 331 11 of 16

Databases of insect species at the international level need to establish projects that
maintain updated research on this topic to strengthen the preventive control of these
Anastrepha species [95–98]. The maps that present a very high risk of the establishment
of all fruit fly species in the El Niño episode agree with the low levels of precipitation
and average temperatures in tropical and subtropical zones. This could be due to the cli-
matic variability that causes high levels of climatic, social and economic uncertainty in the
American geography, and the availability of fruit hosts at the time that would increase the
establishment risk [98–100]. As these climatic variables are among the most important at a
biological level for Anastrepha species, they tend to influence their expansion or contraction
on an ecological level, which will affect fruit plots and commercial export crops at harvest
and postharvest, which are the dates of the greatest commercialisation [21,77]. The high
degree of climate uncertainty in recent years with the El Niño and La Niña phenomena
projects various in-depth analyses regarding the ENSO episodes that justify the study of
models in short periods due to the constant changes in the temperatures of the Pacific
Ocean [21,99]. Apparently, these changes in climatic patterns (precipitation and stable, av-
erage temperatures) increase the level of establishment risk for Anastrepha species, enabling
them to find suitable areas for their reproduction [21–102]. The establishment risk maps
presented will allow institutions, researchers and producers to be guided in specific areas
of the Neotropics to design control plans to prevent the potential establishment of their
populations according to a greater or lesser level of intensity of the environmental variable
on site [100,102,103].
The fly species evaluated here have a high risk of establishing themselves throughout
Panama due to a more stable climate throughout the different episodes of the El Niño
phenomenon and its limited territorial geography with a fairly homogeneous flora that
facilitates the expansion of these species, except in very dry and warm places in certain
months of the year when the species A. grandis would not thrive [37,104,105]. These results
indicate that the fruit fly species of the genus Anastrepha do not have geographical barriers
in this region of the world, but their dispersion is limited by small changes in the availability
of environmental space caused by the environmental variability of the ENSO cycle. This can
be analysed with niche studies on small scales, which could help make better prevention
decisions that alert the institutions responsible for phytosanitary safety and food safety
policies of a country and thus optimise time and money [106].

5. Conclusions
The results of this research make it possible to guide and manage preventive phy-
tosanitary plans in the IPM of species of fruit flies of the genus Anastrepha throughout the
Neotropics in the face of climatic variability of the ENSO cycle. In addition, this research
guides future basic and applied research work on other insect pests that attack fruit trees of
interest to the international scientific community whose studies are limited to niche topics.
In recent years, climate variability has changed the perspective in the field of research, and
this methodological approach helps to materialise pest control plans throughout the world.

Author Contributions: Conceptualization, A.B.D., R.A.V., A.B.A., J.Á.J. and M.A.-S.; methodology,
A.B.D., R.A.V., A.B.A., J.Á.J. and M.A.-S.; validation, A.B.D., R.A.V., A.B.A., J.Á.J. and M.A.-S.; formal
analysis, A.B.D., R.A.V., A.B.A., J.Á.J. and M.A.-S.; investigation, A.B.D., R.A.V., A.B.A., J.Á.J. and
M.A.-S.; data review, A.B.D., R.A.V., A.B.A., J.Á.J. and M.A.-S.; writing—original draft preparation,
A.B.D.; writing—proofreading and editing, A.B.D., R.A.V., A.B.A., J.Á.J. and M.A.-S.; supervision,
R.A.V., A.B.A., J.Á.J. and M.A.-S.; activity management, A.B.D., R.A.V., A.B.A. and M.A.-S.; funding
acquisition, A.B.D. All authors have read and agreed to the published version of the manuscript.
Funding: This research was financed by SENACYT-IFARHU-Panama as part of the doctoral schol-
arships project for public officials in the agricultural sector, contract number 270-2021-117, and by
the National Research System (SNI) (Anovel Barba and Randy Atencio). In addition, this research
was made possible through collaboration with the technical staff of the CIAPCP-AIP-Panama, as a
member of the group.
Insects 2024, 15, 331 12 of 16

Data Availability Statement: All data are contained in the article.

Acknowledgments: Thanks are given, first of all, to God, and also to all the collaborators of this
research work.
Conflicts of Interest: The authors declare no conflicts of interest.

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