Startseite Lebenswissenschaften Illustrating the current geographic distribution of Diaphorina citri (Hemiptera: Psyllidae) in Campeche, Mexico: a maximum entropy modeling approach
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Illustrating the current geographic distribution of Diaphorina citri (Hemiptera: Psyllidae) in Campeche, Mexico: a maximum entropy modeling approach

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Veröffentlicht/Copyright: 3. Juli 2024
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Florida Entomologist
Aus der Zeitschrift Florida Entomologist Band 107 Heft 1

Abstract

Diaphorina citri Kuwayama (Asian citrus psyllid) is a quarantine pest found in at least 60 countries, causing indirect damage as a primary vector of pathogens associated with Huanglongbing in citrus trees. Huanglongbing-infected trees die within 3–8 years, accompanied by economic losses in citriculture. D. citri has spread in Mexico to several states and is a high risk to Mexican citriculture due to its ability to cause damage and the lack of a disease cure. The primary objective of this research was to enhance our understanding of the current status of D. citri in southeastern Mexico. This study analyzed the distribution of D. citri in Campeche, Mexico from 2013 to 2020. The study generated 572,619 D. citri records from 40,620 yellow sticky traps deployed in 10 of the 12 municipalities of the state. We employed advanced MaxEnt and DivaGIS software to accomplish this study. Results showed population fluctuations with a peak during June and July from 2013 to 2019 and July and September in 2020. The study found a higher presence of D. citri in Campeche, Tenabo, Carmen, Champotón, and Escárcega and a higher incidence in Citrus latifolia Tanaka ex Q. Jiménez and Citrus sinensis (L.) Osbeck crops. The variance in the number of D. citri adults captured per year and the dispersion index (a parameter measuring the ability of insects to leave one ecosystem and move to another in search of suitable conditions for their survival and reproduction) was greater than the annual mean, demonstrating a spatially distributed, right-skewed aggregate. The elliptical polygon or standard deviation ellipse indicated the tendency for a less elongated ellipse in 2013–2014. From 2015 to 2018 D. citri expanded north towards Hecelchakán and south towards Champotón, Escárcega, and Carmen. In 2019, D. citri expanded north towards Champotón, Campeche, Tenabo, Hecelchakán, and Calkiní. The months with the most activity between 2013 and 2020 were May, June, July, and August, with June having the highest numbers collected. The results of the enveloped tests (parameter measuring how environmental conditions influence the spatial patterns of insect populations) showed the adaptability of D. citri to different conditions. D. citri prefers temperatures of 24.6–27.9 °C and 1,050–1,500 mm of rainfall. Areas with high-risk for D. citri are coastal and northern parts of the study area. Central Campeche is suitable, and southern parts have low to medium risk. Our research shows the relationship between climatic factors and the distribution of D. citri in the state of Campeche, Mexico. Moreover, our findings will be crucial for implementing effective surveillance measures in areas where the probability model indicates the potential presence of D. citri. This is especially significant due to the remarkable adaptability of D. citri to diverse environmental conditions.

Resumen

Diaphorina citri Kuwayama (psílido asiático de los cítricos) es una plaga de cuarentena presente en al menos 60 países, que causa daños indirectos como vector primario de patógenos asociados al Huanglongbing en los cítricos. Los árboles infectados por el Huanglongbing mueren en un plazo de 3 a 8 años, lo que conlleva pérdidas económicas en la citricultura. D. citri se ha diseminado en México a varios estados y representa un alto riesgo para la citricultura mexicana debido a su capacidad para causar daños y a la falta de una cura para la enfermedad. El objetivo principal de esta investigación fue mejorar nuestra comprensión de la situación actual de D. citri en el sureste de México. Este estudio analizó la distribución de D. citri en Campeche, México de 2013 a 2020. El estudio generó 572,619 registros de D. citri a partir de 40,620 trampas pegajosas amarillas desplegadas en 10 de los 12 municipios del estado. Empleamos software avanzado MaxEnt y DivaGIS para llevar a cabo este estudio. Los resultados mostraron fluctuaciones poblacionales con un pico durante junio y julio de 2013–2019 y julio y septiembre de 2020. El estudio encontró una mayor presencia de D. citri en Campeche, Tenabo, Carmen, Champotón y Escárcega y una mayor incidencia en los cultivos de Citrus latifolia Tanaka ex Q. Jiménez y C. sinensis (L.) Osbeck. La varianza en el número de adultos de D. citri capturados por año y el índice de dispersión (parámetro que mide la capacidad de los insectos para abandonar un ecosistema y desplazarse a otro en busca de condiciones adecuadas para su supervivencia y reproducción) fue mayor que la media anual, lo que demuestra un agregado espacialmente distribuido y sesgado a la derecha. El polígono elíptico o elipse de desviación estándar indicaba la tendencia a una elipse menos alargada en 2013–2014. De 2015–2018 D. citri se expandió al norte hacia Hecelchakán y al sur hacia Champotón, Escárcega y Carmen. En 2019, D. citri se expandió al norte hacia Champotón, Campeche, Tenabo, Hecelchakán y Calkiní. Los meses con mayor actividad entre 2013–2020 fueron mayo, junio, julio y agosto, siendo junio el de mayor número de colectas. Los resultados de las pruebas envolventes (parámetro que mide cómo las condiciones ambientales influyen en los patrones espaciales de las poblaciones de insectos) mostraron la adaptabilidad de D. citri a diferentes condiciones. D. citri prefiere temperaturas de 24,6–27,9 °C y precipitaciones de 1,050–1,500 mm. Las zonas de alto riesgo para D. citri son la costa y el norte del área de estudio. El centro de Campeche es adecuado, y las partes meridionales tienen un riesgo de bajo a medio. Nuestra investigación muestra la relación entre los factores climáticos y la distribución de D. citri en el estado de Campeche, México. Además, nuestros hallazgos serán cruciales para implementar medidas de vigilancia efectivas en áreas donde el modelo de probabilidad indica la presencia potencial de D. citri. Esto es especialmente significativo debido a la notable adaptabilidad de D. citri a diversas condiciones ambientales.

Keywords: Asian citrus psyllid; Campeche; Mexico; Diva-GIS; modeling; Maxent
Palabras Clave: psílido asiático de los cítricos; Campeche; México; Diva-GIS; modelización; Maxent

1 Introduction

Worldwide production of citrus averages 98 million tons per year, making it a major global agricultural commodity (USDA 2021). Oranges are among the most significant species, accounting for two-thirds of the total production (Maya-Ambía 2017). Plants of all citrus species are vulnerable to various diseases during their growth cycle. One of the most common is Huanglongbing, also known as citrus greening. Huanglongbing is associated with three Gram-negative bacteria, all Candidatus Liberibacter spp. (alpha-proteobacteria, order Rhizobiales), which are obligatory parasites of both plants and insects (Haapalainen 2014; Widyawan et al. 2023). Candidatus Liberibacter asiaticus (CLas) is transmitted by Diaphorina citri Kuwayama (Hemiptera: Psyllidae, Asian citrus psyllid) (Bové 2006) and sometimes by other citrus psyllid species.

Mexico has solidified its position as the fifth largest producer of citrus globally, with 594,369 ha cultivated (FAO 2017; SIAP 2020). Twelve percent of total Mexican citrus production is exported and the remaining 88 % is consumed domestically. Persian limes and oranges are the largest crops by acreage, totaling 226,486.67 ha with a total production of 3.4 million tons and a value of MXN 18.4 billion (SIAP 2021). Mexico first reported Huanglongbing in 2009 in Tizimin, a municipality in the southeast region of Yucatan. Despite being contained initially, it spread quickly throughout the country, and by 2016 it had reached the states of Baja California Sur, Campeche, Chiapas, Colima, Hidalgo, Jalisco, Nayarit, Nuevo Leon, Quintana Roo, Sinaloa, and Tabasco (López-Collado 2015; Santivañez et al. 2013; SENASICA 2016).

The Asian citrus psyllid is the most significant citrus pest worldwide (Aidoo et al. 2022; CABI 2019; Santivañez et al. 2014) mainly because it vectors pathogens associated with Huanglongbing, which has resulted in substantial losses for major citrus-producing countries globally. Currently, the most effective way to control Huanglongbing is through vector management. Common strategies in infected areas include planting healthy trees, identifying and removing infected trees to prevent spread, or using intense treatments with broad-spectrum pesticides such as neonicotinoids, pyrethroids, and organophosphates (Bassanezi et al. 2020; Chen et al. 2021; Graham et al. 2020; Levy et al. 2023; Li et al. 2020; Tiwari et al. 2012; Vanaclocha et al. 2019). However, the inappropriate and excessive use of synthetic chemical insecticides has led to insecticide resistance (Chen et al. 2023). In some places removal of symptomatic trees has not slowed disease spread enough to be an economically viable practice (Bassanezi et al. 2013; Dewdney et al. 2022; Lee et al. 2015).

Recently, the development of geographic information systems (GIS) has boosted studies related to the analysis of spatial distribution applied to insect ecology (Rano et al. 2022), and mathematical modeling software has been created to predict the effects of climate change on insect species. Among these, the Maximum Entropy (Maxent) model stands out as one of the most successful where available occurrence data are present (Wiltshire and Tanner 2020). Its remarkable predictive capabilities make it a valuable tool for predicting the impact of climate change on insects (Asase and Peterson 2016; Zurell et al. 2020). The advancement in GIS technology and computer statistical methods has made it possible to predict the geographical distribution of species by examining climatic suitability worldwide (Bale et al. 2002; Lee et al. 2023).

Knowledge of intraspecific competition, mutual attraction, and population dispersal help in characterizing and tracking insect distribution (Ellsbury et al. 1998; Grabarczyk et al. 2023; Park and Obrycki 2004). Ongoing research on the geographic distribution and population changes of insects is necessary to establish effective monitoring strategies and improve current surveillance plans (Santiago-Rosario et al. 2023; Wang et al. 2016).

This study aimed to analyze spatial data and forecast trends in the geographic spread of the Asian citrus psyllid in Campeche, Mexico from 2013 to 2020. It focuses on unique aspects of the geographic data, employing a GIS technique for describing and visualizing spatial distributions, detecting outlier locations, uncovering spatial associations, identifying hot spots, and presenting visual representations of the insect’s presence through spatial regimes or other forms of spatial variability.

2 Materials and methods

2.1 Characteristics of the study area

Campeche is located in the southeastern region of Mexico and is part of the United Mexican States, along with Mexico City. It is comprised of 12 municipalities and is situated in the Yucatán Peninsula. It is bordered by Yucatán to the north and northeast, Quintana Roo to the east, Guatemala and Belize to the south, the Gulf of Mexico to the west, and Tabasco to the southwest. Campeche has a warm climate, with temperatures consistently above 20 °C. The warmest month reaches a maximum temperature of 36 °C, and the coldest month sees a minimum temperature of 18.5 °C, with an average temperature of 26 °C. The state experiences significant precipitation from June to January, with a total of 2,080 mm. However, from February to May, the region experiences a dry period, with the heaviest precipitation taking place in the southern part of the state (Corvo et al. 2008; Hernández-Rivera et al. 2015; Sampayo-Maldonado et al. 2023).

2.2 Data collection

The data used in this study were collected by the D. citri Monitoring System (SIMDIA), a part of the Campaign Against Regulated Citrus Pests in municipalities in Campeche, Mexico, between 2013 and 2020. The information was provided by the State Plant Health Committee of Campeche (CESAVECAM), a subsidiary of the National Service of Health, Safety, and Agrifood Quality (SENASICA) and the Secretary of Agriculture and Rural Development (SADER) of Mexico. A total of 40,620 yellow sticky traps were placed in commercial citrus orchards, each trap measuring 14.5 × 20.5 cm and reflecting light at around 550–600 nm wavelength (Allan et al. 2020; Pan et al. 2021). The traps were placed alternately on the plants at a height of 1.5–2.0 m. Twenty traps were installed at each monitoring site. Sites were selected within the Regional Control Areas (ARCOs). ARCOs in Mexico are established to control regional infestations and should have a minimum area of 1,000 ha. Each trap was identified with a unique number, and the location, grower’s name, orchard area, and citrus cultivar were recorded. The number of psyllids captured per trap was recorded weekly, and a new trap was installed in its place (García-Ávila et al. 2021; Robles-García 2019).

2.3 Database sorting

The collected data were used to create a database of Asian citrus psyllid in citrus-growing areas in Campeche. Inconsistent or incorrect data were excluded from the database, such as those with missing geographic coordinates, erroneous locations, and data outside the state of Campeche, among others. The following variables were analyzed: geographic coordinates, municipality, location, citrus cultivar, months, weeks, and the number of Asian citrus psyllid adults captured per installed trap in each citrus tree. These data were used to determine the aggregation indexes and distribution patterns of the pest (Jokar 2023; Soemargono et al. 2008).

2.4 Population fluctuation and aggregation indices

The monthly accumulated values of the psyllid count per trap were compiled into databases in CSV format and imported into the open-source software QGIS version 3.16 (QGIS 2023). These databases were used to generate distribution maps by year, municipality monitored, and type of crop affected. The means and variances of the monthly adult captures were calculated to determine the type of dispersion in Campeche, Mexico. The Dispersion Index (DI, variance/mean ratio) and Green’s Coefficient (Cx, variance/sample mean ratio) were calculated to confirm the dispersion pattern, using the variance/mean ratio as a method for analyzing aggregation patterns. The Greig-Smith (1957) approach was adopted, whereby a value less than 1 indicates a regular distribution, and a value greater than 1 indicates an aggregated distribution.

The study calculated the variance-mean ratio (Id = S 2/x) and Green’s coefficient (Cx = (S 2/x) − 1/(∑x − 1)) to determine the spatial distribution patterns of the Asian citrus psyllid in Campeche, Mexico. The variance-mean ratio, where S 2 is the variance and x is the sample mean, indicates a random spatial arrangement if the value is equal to 1, a regular or uniform arrangement if less than 1, and an aggregated arrangement if significantly greater than 1. Green’s coefficient, based on the variance/sample mean ratio, shows a uniform pattern with negative values, an aggregation pattern with positive values, and a random distribution with values equal to zero (Green 1966; Pielou 1960; Taylor 1961, 1984).

2.5 Spatial distribution analysis

Heat maps were created to represent the density of insect occurrences visually, based on a weighting factor. The heat maps were created using a two-dimensional visualization of a latitude and longitude data matrix, which represented Asian citrus psyllid presence as a grid of colored pixels. The colors in the heat map show the changes and magnitude of the variable over time. Given the size of the study area (52,000 km2), the search radius was set to 5,000 m and the pixel size to 100 m. Interpolation was performed for all months with observations, and the color scale was adjusted to the maximum annual value or absolute value to represent the values obtained. To analyze the distribution of the data, an algorithm was used that measures the trend of the observation points. This algorithm calculates the standard distance in the X and Y directions, defining the axes of an ellipse that encompasses the distribution of the observation points. This ellipse, known as a standard deviation ellipse, allows us to determine if the distribution of the points measuring psyllid presence is elongated and has a particular orientation, i.e., a trend of occurrence. The Directional Distribution/Measuring Geographical Distributions tool from ArcMap 10.3 Toolbox (Environmental Systems Research Insititue Inc., Redlands, CA, USA) was used to calculate the ellipse. This tool created a new elliptical polygon layer centered at the center of all observation points. The attribute values of the ellipse include two standard distances (long and short axes) and the orientation, or azimuth, which shows the direction in which the measured values are trending, in this case, Asian citrus psyllid occurrence (Zhao et al. 2022).

An interpolation algorithm was used to generate the heat maps, which calculate density based on the distribution and number of points in the study area. A higher concentration of points results in higher interpolation values, making it easier to identify the areas where Asian citrus psyllid was most prevalent, referred to as hot spots (Zumwald et al. 2021).

In our study, the relationship between the climatic variables that the predictive model indicated had the greatest impact and the probability of occurrence of Asia citrus psyllid was analyzed and a response curve was obtained.

Data were normalized according to the methodologies outlined by Karimzadeh et al. (2014) and El Den Nasser et al. (2023). Data collection standards were implemented to ensure that all data collected adhered to a consistent set of criteria, encompassing file formats, units of measurement, and collection methods. Data cleaning was conducted to identify and correct potential errors, inconsistencies, or outliers by eliminating duplicate data, interpolating missing data, and rectifying input errors. In ArcGIS 10.3 software, data values were adjusted to a specific distribution. The Reclassify tool in the Spatial Analyst Tools menu was used to reassign the data values to a scale from 0 to 1, preserving the relative relationship between the values and setting minimum and maximum ranges for the new values. The Zonal Statistics and Cell Statistics tools were used to calculate the mean and standard deviation of the data. Additionally, the Raster Calculator tool was employed to apply the z-score formula to the data by subtracting the mean and dividing by the standard deviation.

2.6 Environmental variables

To model the distribution of Asian citrus psyllid, bioclimatic variables were obtained from WorldClim v2.1 with a spatial resolution of approximately 1 km2 (www.worldclim.org). This is a database of high-resolution global weather and climate data that is used for mapping and spatial modeling (Fick and Hijmans 2017). The data were converted into ASCII format using QGIS v3.28 (Abou-Shaara et al. 2021). The bioclimatic variables used in the modeling process were elevation, annual precipitation, precipitation in the driest month, temperature annual range, annual mean temperature, and mean diurnal range (Hosni et al. 2022a).

2.7 Modeling process evaluation

To model Asian citrus psyllid distribution, Maxent software was utilized, which employs artificial intelligence and maximum entropy principles (Elith et al. 2006; Phillips et al. 2023). Maxent version 3.4.4 was used in this study. The model was trained using 75 % of the occurrence data, and the remaining 25 % was set aside for testing (Hosni et al. 2022b). The maximum number of background points and iterations was set to 10,000 and 500, respectively. To enhance the model’s performance, cross-validation was carried out with 10 replicates (Kessler et al. 2019; Zhang et al. 2023). The quality of the model was evaluated based on the Area Under the Curve (AUC) of the Receiver Operating Characteristic (ROC) results, which ranges from 0 to 1, with 0 being random discrimination and 1 representing perfect discrimination (Hosni et al. 2020). Models with AUC values below 0.5 were considered poorly fitting, and those with values above 0.75 were considered well-fitting (Mulieri and Patitucci 2019).

The Maxent model describes the relative contributions of various environmental variables. The first estimate was calculated by adding the increase in regularized gain at each iteration of the training algorithm to the corresponding variable contribution, or subtracting it when the value of lambda was negative. The second estimate was derived by randomly rearranging the values of each environmental variable while considering the training data. The model was re-evaluated using the rearranged data, and the reduction in the training AUC was normalized as a percentage.

2.8 Two-dimension niche analysis and prediction areas

The DIVA-GIS software version 7.5 (http://www.diva-gis.org/) was utilized to average the predictions produced by different atmospheric circulation models from the same period. These predictions were reclassified to measure the species’ geographical area and divided into six categories of suitability for Asian citrus psyllid. The categories are unsuitable region, low-suitability region (0.0–2.5), medium-suitability region (2.5–5.0), high-suitability region (5.0–10.0), very high-suitability region (10.0–20.0), and excellent-suitability region (20.0–27.0) (Liu et al. 2005; Mao et al. 2022). To generate the two-dimensional niche of the Asian citrus psyllid, the enveloped test was applied to the annual mean temperature and annual precipitation data (Govindasamy et al. 2003; Hosni et al. 2022a).

3 Results

3.1 Population fluctuation and aggregation indices

During the period from 2013 to 2020, Asian citrus psyllid was widespread in the citrus-growing regions of Campeche state. A total of 40,620 traps recorded the presence of adult psyllids, resulting in 572,619 records from 10 of the 12 municipalities in the state. The annual variance in the number of adult psyllids captured was up to three times greater than the mean, indicating a skewed distribution towards higher population densities. The variance-to-mean ratio for each year in the period of 2013–2020 was above 1, indicating an aggregated spatial distribution of D. citri, confirmed by the results of the Greig-Smith aggregation test (Table 1).

Table 1:

Data analysis and aggregation indices of the number of Diaphorina citri adults captured per week during the 2013–2020 monitoring program in the state of Campeche, Mexico.

Year No. traps No. weeks No. records No. total adultsa X̅ ± 95 % CI s 2 DI Cx AT_GS
2013 19,748 52 70,047 13,783 1.743 ± 0.03 5.500 3.155 0.0002 **
2014 2,465 28 47,006 5,999 2.132 ± 0.06 9.640 4.522 0.0006 **
2015 4,443 53 158,012 2,664 1.445 ± 0.03 2.094 1.449 0.0002 **
2016 3,974 52 152,256 5,592 2.366 ± 0.09 22.518 9.517 0.0015 **
2017 3,729 51 44,167 3,835 1.727 ± 0.02 2.420 1.401 0.0001 **
2018 1,795 51 40,223 2,235 1.954 ± 0.15 25.099 12.845 0.0053 **
2019 2,481 50 32,265 6,676 2.542 ± 0.13 44.772 17.613 0.0025 **
2020 1,985 50 28,643 32,260 4.650 ± 0.10 77.891 16.751 0.0005 **
Total 40,620 387 572,619 73,044 – – – – –

  1. aTotal number of D. citri adults captured in traps during 2013–2020. x = Mean number of D. citri adults captured in traps during 2013–2020. 95 % CI = 95 % confidence interval of the sample mean ( X̅). s 2 = Variance of the number of D. citri adults captured per trap. DI = Dispersion index (variance/mean ratio), Cx = Green’s coefficient (variance/sample mean ratio). AT_GS = Aggregation test according to Greig-Smith’s (1957) methodology; significant for aggregation (**).

The Asian citrus psyllid population showed a downward trend from January to April but began to increase from the end of April to May, reaching a peak in June and July from 2013 to 2019. In 2020, however, two population peaks were recorded, one in July and the other in September, with a decrease in October (Figure 1).

Figure 1: Population fluctuation of the number of Diaphorina citri adults captured per month during the 2013–2020 monitoring seasons in the state of Campeche, Mexico.
Figure 1:

Population fluctuation of the number of Diaphorina citri adults captured per month during the 2013–2020 monitoring seasons in the state of Campeche, Mexico.

In the period from 2013 to 2016, Asian citrus psyllid was found more frequently in the municipalities of Campeche and Tenabo. In 2017, the municipality of Carmen had an increase in presence that decreased in the following year. From 2019 to 2020, a significant increase was observed in the municipalities of Campeche, Champotón, Escárcega, and Tenabo (Figure 2). Asian citrus psyllid was found most commonly on Citrus latifolia Tanaka ex Q. Jiménez and Citrus sinensis (L.), but it also was present in Citrus aurantium L. and Citrus reticulata Blanco crops (Table 2).

Figure 2: Distribution of the geographical proliferation of the number of Diaphorina citri adults captured in each municipality during the 2013–2020 monitoring program in the state of Campeche, Mexico. Each graph represents the distribution at a two-year period.
Figure 2:

Distribution of the geographical proliferation of the number of Diaphorina citri adults captured in each municipality during the 2013–2020 monitoring program in the state of Campeche, Mexico. Each graph represents the distribution at a two-year period.

Table 2:

Geographic distribution of Diaphorina citri adults collected per week and per crop species during the 2013–2020 survey program in the state of Campeche, Mexico.

Municipality/crop variety Total number of adults
2013 2014 2015 2016 2017 2018 2019 2020
Calakmul – – 162 105 20 8 559 1,053
Citrus latifolia – – 105 65 20 8 559 1,053
Citrus sinensis – – 57 40 – – – –
Calkiní 516 227 54 368 181 20 58 2,166
Citrus latifolia 444 223 49 363 181 20 58 2,166
Citrus sinensis 72 4 5 5 – – – –
Campeche 7,453 3,530 1,095 2,682 711 608 815 9,586
Citrus latifolia 6,429 2,979 809 1,928 655 568 733 8,608
Citrus reticulata 153 45 64 91 25 24 73 978
Citrus aurantium 12 16 22 277 1 – – –
Citrus sinensis 859 490 200 386 30 16 9 –
Carmen – – 92 260 839 215 512 575
Citrus latifolia – – 53 130 423 99 211 368
Citrus reticulata – – 25 25 167 59 190 143
Citrus aurantium – – 2 46 48 18 47 64
Citrus sinensis – – 12 59 201 39 64 –
Champotón – – 216 1,268 348 221 1,129 3,725
Citrus latifolia – – 137 964 332 199 777 2,369
Citrus reticulata – – 42 213 – 11 213 839
Citrus sinensis – – 37 91 16 11 139 517
Escárcega – – 321 97 572 428 3,021 6,046
Citrus latifolia – – 277 79 498 403 2,918 5,708
Citrus aurantium – – 1 – – – – –
Citrus sinensis – – 43 18 74 25 103 338
Hecelchakán 84 313 81 104 157 – 24 2,170
Citrus latifolia 62 306 76 78 157 – 24 2,170
Citrus sinensis 22 7 5 26 – – – –
Hopelchén 977 139 40 163 110 77 98 1,185
Citrus latifolia 546 26 8 82 – – – –
Citrus aurantium – – – – 110 77 98 1,185
Citrus sinensis 431 113 32 81 – – – –
Seybaplaya – – 39 30 11 15 11 115
Citrus latifolia – – 36 24 7 3 9 115
Citrus sinensis – – 3 6 4 12 2 –
Tenabo 4,753 1,790 564 515 886 643 449 5,639
Citrus latifolia 3,164 1,403 464 425 846 518 418 3,204
Citrus reticulata 23 10 5 8 – – – –
Citrus aurantium 364 253 1 3 – – – –
Citrus sinensis 1,202 124 94 79 40 125 31 2,435
Total 13,783 5,999 2,664 5,592 3,835 2,235 6,676 32,260

  1. The number in bold next to each municipality visited represents the total number of adults in that municipality and is the sum of the individuals in each crop (citrus tree).

3.2 Spatial distribution analysis

Distribution maps for 2013–2020 show changes in population over time and space (Figure 3). The graph displays a concave curve with its highest values in 2013 and 2020. The localities of Tikinmul and San Antonio Cayal in the municipality of Campeche had the highest incidence of Asian citrus psyllid, as seen in the maps. The months with the highest incidence per year from 2013 to 2020 were May, June, July, and August, with June consistently having the highest numbers, followed by August in 2018, July in 2015, and May in 2014.

Figure 3: Heat maps showing the annual incidence of Diaphorina citri adults in the state of Campeche, Mexico, 2013–2020. The coloring of the heat maps indicates the presence of insects at risk of spreading. Red: very high risk, Orange: high risk, Yellow: moderate risk, Green: low risk, Blue: very low risk.
Figure 3:

Heat maps showing the annual incidence of Diaphorina citri adults in the state of Campeche, Mexico, 2013–2020. The coloring of the heat maps indicates the presence of insects at risk of spreading. Red: very high risk, Orange: high risk, Yellow: moderate risk, Green: low risk, Blue: very low risk.

The incidence of Asian citrus psyllid was observed to be higher in the municipalities of Campeche and Tenabo during 2013 and 2014, resulting in a more compact ellipse shape. From 2015 to 2018, there was a slight expansion to the north in the municipality of Hecelchakán and the south in the municipalities of Champotón, Escárcega, and Carmen. From 2019 onwards, the expansion process continued northward, and by 2020, the municipalities of Champotón, Campeche, Tenabo, Hecelchakán, and Calkiní had been included. By visually drawing an ellipse on a map, one can get a general idea of the data orientation, but the standard deviation ellipse calculation confirms this trend.

However, the data collected each year are not consistent; this suggests that the data points or variables being measured vary from year to year. To enable a fair comparison between different years and make the comparisons more meaningful, the data were normalized based on the number of cases. Before normalization, it was evident that in terms of the raw data, the years 2020 and 2013 had the highest values. However, after the normalization process, only the year 2020 retained the highest value. This implies that 2020 had the highest incidence even when accounting for variations in the number of cases.

Following 2020, the years 2019, 2016, 2014, 2018, and finally 2013 had the next highest incidences, in that order, according to the normalized data. Surprisingly, despite initially having one of the highest raw values, 2013 dropped to sixth place after normalization. This suggests that its high value was influenced by the number of cases in that year.

3.3 Analysis of variable contributions

The AUC is a reliable evaluation parameter for maximum entropy modeling, and high AUC values usually indicate successful modeling outcomes. The AUC value, in this case, was 0.89, indicating that the model accurately represented the Asian citrus psyllid environment. The AUC values for the training data and test data of the initial model, based on the current geographical distribution of Asian citrus psyllid and climate variables, were 0.890 and 0.894 respectively, demonstrating the accuracy of the prediction model. There was only a 0.004 difference between the AUC values of the training set and the test set. The omission rate was calculated based on the training presence records and test records, and was close to the predicted omission, considering the cumulative threshold (Figure 4). This implies that the maximum AUC achievable is less than 1, with a maximum possible AUC for the test data of 0.863. The AUC for the test data, in this case, was 0.885, with a standard deviation of 0.006 (Table 3).

Figure 4: The receiver operating characteristic (ROC) curve and sensitivity/specificity of training and test data for Diaphorina citri distribution. ROC curve represents the true positive rate (sensitivity) versus the false positive rate (1 – specificity) for different classification thresholds. Area under the ROC Curve (AUC) quantifies the overall discriminative ability of the model. The sensitivity represents the proportion of true positives correctly identified by the model, while specificity represents the proportion of true negatives correctly identified.
Figure 4:

The receiver operating characteristic (ROC) curve and sensitivity/specificity of training and test data for Diaphorina citri distribution. ROC curve represents the true positive rate (sensitivity) versus the false positive rate (1 – specificity) for different classification thresholds. Area under the ROC Curve (AUC) quantifies the overall discriminative ability of the model. The sensitivity represents the proportion of true positives correctly identified by the model, while specificity represents the proportion of true negatives correctly identified.

Table 3:

Relative percentages of bioclimatic variables used in Maxent to model the current habitat suitability of the Asian citrus psyllid, Diaphorina citri in the state of Campeche, Mexico.

Variablea Percent contribution Permutation importance (%)
Elevation 27.6 8.6
Annual precipitation 21.0 26.9
Precipitation of driest month 17.2 10.3
Temperature annual range 16.6 30.3
Annual mean temperature 15.2 11.0
Mean diurnal range 2.5 12.9

  1. aBioclimatic variables from WorldClim version 2.1, www.worldclim.org.

3.4 Contribution of bioclimatic variables

The impact of each bioclimatic variable on the predictive distribution model is shown through the use of a jackknife test. The results indicated that temperature-related variables play a crucial role in Asian citrus psyllid modeling. Among the climatological parameters, annual precipitation had the largest impact on Asian citrus psyllid distribution. Annual mean temperature also was found to be a significant factor in Asian citrus psyllid distribution. The environmental variable with the highest gain, when used alone, was annual mean temperature, implying that it holds the most valuable information. On the other hand, the environmental variable that resulted in the biggest drop in gain when omitted was annual precipitation, suggesting that it contains information that is not present in the other variables. The values displayed are the average of multiple runs (Figure 5).

Figure 5: Jackknife test gain for Diaphorina citri. The plot assesses the relative importance of the predictor variables in constructing the model. Blue bars represent the information gain obtained by including the corresponding variable in the model. In general, the higher the information gain, the more important the variable is in predicting the model. Green bars represent the loss of information when a specific variable is excluded from the model. Red bars represent redundancy among variables.
Figure 5:

Jackknife test gain for Diaphorina citri. The plot assesses the relative importance of the predictor variables in constructing the model. Blue bars represent the information gain obtained by including the corresponding variable in the model. In general, the higher the information gain, the more important the variable is in predicting the model. Green bars represent the loss of information when a specific variable is excluded from the model. Red bars represent redundancy among variables.

3.5 Enveloped tests and predicted suitable areas

The results showed that Asian citrus psyllid can adapt to various environmental conditions. The response of key environmental factors revealed that the optimal annual mean temperature for Asian citrus psyllid was between 24.6 and 27.9 °C, and the annual rainfall amount was between 1,050 and 1,500 mm. This is consistent with the broad distribution of this insect and its capacity to thrive in both dry and rainy regions (Figure 6).

Figure 6: A two-dimensional niche of Diaphorina citri between annual temperature and annual precipitation. Red dots represent the geographic locations where occurrences of the species or group of species you are analyzing have been recorded. Green dots represent geographic locations where the species would be expected to occur based on ecological niche models, or in areas that have similar environmental characteristics to the locations where the species was recorded. The blue box is a graphical representation of the optimal range of climatic conditions for the species in terms of temperature and precipitation.
Figure 6:

A two-dimensional niche of Diaphorina citri between annual temperature and annual precipitation. Red dots represent the geographic locations where occurrences of the species or group of species you are analyzing have been recorded. Green dots represent geographic locations where the species would be expected to occur based on ecological niche models, or in areas that have similar environmental characteristics to the locations where the species was recorded. The blue box is a graphical representation of the optimal range of climatic conditions for the species in terms of temperature and precipitation.

The results showed that the municipalities with the highest risk of Asian citrus psyllid proliferation are located in coastal and northern regions of the state. This is due to favorable conditions for growth. The central part of Campeche has a high degree of suitability, and the southern part of the state has low to medium-risk conditions. This can be confirmed by the distribution patterns seen in the heat maps and ellipse maps (Figure 7).

Figure 7: Predicted maps for the distribution of Diaphorina citri using Maxent and DIVAGIS modeling software. A) Maxent’s probability of occurrence map of the potential distribution of Asian citrus psyllid across the landscape, generated using algorithms to model distribution using species occurrence data and environmental data. Darker colors indicate a higher probability of occurrence, while lighter colors indicate a lower probability. B) DIVAGIS Map predicting the current presence of Asian citrus psyllid in areas where it is estimated to be present at a given time, using ecological niche models and environmental data.
Figure 7:

Predicted maps for the distribution of Diaphorina citri using Maxent and DIVAGIS modeling software. A) Maxent’s probability of occurrence map of the potential distribution of Asian citrus psyllid across the landscape, generated using algorithms to model distribution using species occurrence data and environmental data. Darker colors indicate a higher probability of occurrence, while lighter colors indicate a lower probability. B) DIVAGIS Map predicting the current presence of Asian citrus psyllid in areas where it is estimated to be present at a given time, using ecological niche models and environmental data.

4 Discussion

Based on the findings of this study, it is suggested that heightened surveillance efforts should be directed toward the northern citrus-growing regions of the state of Campeche. This is due to the potential of the psyllid populations in these areas to serve as focal points for the spread of bacteria that cause Huanglongbing. Asian citrus psyllid can travel distances of up to 2 km (Boina et al. 2009; Lewis-Rosenblum et al. 2015). Failure to control spread of the Asian citrus psyllid in high-risk areas could result in substantial economic losses (Lu and Sun 2017).

Some notable cases of damage and economic loss have been documented in Brazil and Florida. In 2004, Huanglongbing was first reported in groves in the central state of São Paulo, while in 2005 the disease was identified in southern Florida, USA (Gottwald 2010; Teixeira et al. 2005). Since then, plantations in the two most important citrus producing states in the world, São Paulo and Florida, have been severely devastated by the disease. According to Belasque et al. (2010), plantations in various regions of the world can become economically unviable within 10 years of the first symptom being detected if appropriate control measures are not implemented. Another important report is that of Bové (2006), who describes a case in China where citrus trees were completely destroyed in only five years due to the lack of control measures. This devastation is attributed to the bacterium Candidatus Liberibacter asiaticus, which has also caused significant economic losses in the citrus industry in North and South America. This bacterium has been observed to have an extremely small genome of approximately 2,394 genes, suggesting that its aerobic respiration is limited. The bacterium is known to reside in the phloem of citrus and relies on a variety of amino acids from both the infested trees and the insect vector for energy (Coletta-Filho et al. 2004; Duan et al. 2009; Hijaz and Killiny 2014).

In studies analyzing the distribution and predictive behavior of insects, it is essential to consider aspects related to their ability to migrate and fly. This ability allows them to travel long distances in search of food, suitable habitat, and reproductive partners, directly influencing their geographic distribution and ability to colonize new areas. In addition, their ability to fly facilitates the transport of pathogens from one location to another, with significant implications for plant, animal, and human health. Detailed knowledge of insect flight capabilities is essential for the development of effective pest management strategies. Understanding the extent of these insects’ ability to travel helps to develop more accurate control measures and predict the potential spread of pest populations (Holland et al. 2006).

According to previous research, adult psyllids typically exhibit limited migratory behavior due to their restricted flight ability caused by underdeveloped wing muscles. Instead of sustained flight, these insects rely on jumping from leaf to leaf, resulting in a movement range of approximately 5 m (López et al. 2005). However, to disperse over larger distances, psyllids can exploit wind currents by ascending to heights of up to 7 m. Their wind-assisted travel can cover a distance of at least 4 km, contingent upon the speed of air currents (Aurambout et al. 2009). Under favorable wind conditions, they can move up to 50 km (Antolínez et al. 2022). Nonetheless, recent reports have documented instances of flight activity in Asian citrus psyllid, contradicting the notion of limited flight. For instance, Martini et al. (2018) observed prolonged flights lasting over 60 s when exposing these psyllids to temperatures ranging from 21 to 28 °C in laboratory settings. Their findings indicated that flight distance increased in proportion to temperature, suggesting that Asian citrus psyllid can adapt its flight behavior in response to abiotic factors (Antolínez et al. 2021).

In our study, the highest presence of Asian citrus psyllid was observed from June to August. This result differs from the findings of Ortega-Arenas et al. (2013), who conducted a study in three citrus plantations located in the region of Cazones, in the northern part of the state of Veracruz, Mexico. Although this area shares some topographic and climatic characteristics with the State of Campeche, such as an altitude of 10 m above sea level, an average temperature of 25 °C, and an average annual rainfall of 2,000 mm, researchers reported that the highest abundance of Asian citrus psyllid occurred in February and March. However, they noted that infestations for this psyllid could occur in any month of the year, depending on the biotic factors (phenological development, and associated microorganisms, as the endosymbionts Ca. Carsonella ruddii, Ca. Profftella armatura, Ca. Wolbachia spp.; López-San Juan et al. 2021) and abiotic factors (rainfall, temperature, terrain, and human influence) specific to each region. These findings underscore the need to understand the methods used by farmers to prevent infestations in their citrus crops (Hall et al. 2008; Tsai et al. 2002).

D. citri prefers Rutaceae, and its reproductive success is dependent on young leaves and buds (flush). However, the production of flush can be affected by factors such as climate, plant age, and cultivar (Meng et al. 2022; Ortega-Arenas et al. 2013). The use of yellow traps is a highly effective method for determining the insect’s seasonal abundance in rural areas, especially when placed in sites with un-sprouted trees. Leong et al. (2022) recommend using four traps per hectare, as this is enough to observe Asian citrus psyllid movement activity, subject to the specific edaphic and climatic conditions of each region.

Understanding the distribution patterns of Asian citrus psyllid in a specific region is crucial for the prevention, control, and, ideally, elimination of pathogen-carrying insects. López-Buenfil et al. (2017) carried out a study on the population dynamics of Ca. Liberibacter asiaticus in Mexico and concluded that not only is it important to manage the pathogen through insect vector control but also crop phenology management should be guided by an understanding of the interaction between the pathogen and the plant, considering their dynamics. In the case of sprout management in arid regions characterized by intermittent sprouting periods, it is possible to manipulate this process using irrigation and chemical plant growth regulators. This manipulation facilitates control of pathogen transmission, during the limited periods when plants produce vulnerable sprouts.

The impact of temperature on insect dispersal has been observed to be significant (Narouei-Khandan et al. 2016; Vimala et al. 2022). Nava et al. (2007) stated that temperatures above 32 °C are unfavorable for the development of D. citri, but in the state of Campeche, the temperatures are higher, where it can reach at least 42 °C at peak hours (noon), and D. citri populations have been recorded in all 12 months of the year. This suggests that Asian citrus psyllid has adapted to the high temperatures in the area. The previous statement is consistent with the findings reported by Razi et al. (2014), who discovered psyllids carrying positive bacterial loads at temperatures near 50 °C. According to Beattie and Barkley (2009), psyllid populations are adaptable to regions with high temperatures, but populations may decrease during months with cool temperatures such as November and December, as the activity of the insect slows down (Qureshi and Stansly 2009).

During the data processing phase, we noticed that elevation plays a significant role in the training of the system (Maxent software), contributing significantly to the model. However, following data permutation, its contribution diminishes substantially. Nevertheless, elevation exhibits a correlation with temperature and precipitation. Specifically, there exists an inverse relationship between elevation and temperature, meaning that as altitude increases, temperature tends to decrease. It is noteworthy to mention that in coastal regions like the state of Campeche, the relationship between precipitation and elevation can be influenced by multiple factors. Generally, there is an upward trend in precipitation as elevation increases in these areas. This phenomenon can be primarily attributed to the orographic effect, whereby moist oceanic winds interact with nearby mountain ranges along the coast, resulting in the ascent of air. As the air rises, it cools and leads to the condensation of water vapor, ultimately leading to cloud formation and heightened precipitation. Nonetheless, it is crucial to acknowledge that the association between precipitation and elevation in coastal areas may vary due to local factors such as geographic configuration, prevailing wind directions, and additional topographic characteristics within the region.

Heat maps are a useful tool for processing large data sets, such as the 572,619 records collected over eight years from 2013 to 2020. Heat maps can be used to observe patterns and changes over time (Pawar et al. 2022). The most important factor affecting the geographical distribution of Asian citrus psyllid was annual precipitation, and the response curve shows that the probability of occurrence gradually decreases as the annual temperature increases. Before devising a pest monitoring plan, the suitability of the habitat should be assessed. Evaluating the present habitat suitability for Asian citrus psyllid could furnish crucial data to formulate useful regional monitoring plans.

Our research examined the influence of climatic factors on the geographic distribution of Asian citrus psyllid in Campeche State, Mexico, using MaxEnt and DivaGIS software modeling. Our findings enhanced knowledge of the present distribution of Asian citrus psyllid in Campeche, Mexico, with potential implications for the national and regional distribution. The models corroborated a high to medium risk range for Asian citrus psyllid habitat suitability in Campeche. Under the current climate model, the most important variables that affected the suitable environment of Asian citrus psyllid were precipitation and mean temperature. Therefore, it is crucial to implement monitoring and control measures in areas where the insect is likely to be present, due to its ability to thrive in diverse environmental conditions.

Corresponding author: Carlos Granados-Echegoyen, CONAHCYT-Instituto Politécnico Nacional, CIIDIR Unidad Oaxaca, Santa Cruz Xoxocotlán, Oaxaca 71230, México, E-mail:

Acknowledgments

The first author extends their gratitude to the National Council for the Humanities, Sciences, and Technologies (CONAHCYT-Mexico) for the scholarship offered. Additionally, the author thanks the Interdisciplinary Research Center for Integral Regional Development Oaxaca Unit (CIIDIR Oaxaca) of the National Polytechnic Institute (IPN) of Mexico, the State Plant Health Committee of the State of Campeche (CESAVECAM), and the Autonomous University of Campeche (UACAM) for their invaluable information and support in this research.

  1. Research ethics: Not applicable.

  2. Author contributions: The authors has accepted responsibility for the entire content of this manuscript and approved its submission.

  3. Competing interests: The authors state no conflict of interest.

  4. Research funding: None declared.

  5. Data availability: Not applicable.

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Received: 2023-02-18
Accepted: 2023-10-19
Published Online: 2024-07-03

© 2024 the author(s), published by De Gruyter on behalf of the Florida Entomological Society

This work is licensed under the Creative Commons Attribution 4.0 International License.

Artikel in diesem Heft

  1. Frontmatter
  2. Research Articles
  3. Distribution and dispersal of adult spotted wing drosophila, Drosophila suzukii (Diptera: Drosophilidae), in organically grown strawberries in Florida
  4. A comparison of the capture of non-target arthropods between control methods and monitoring traps of Anastrepha ludens in citrus agroecosystems
  5. Development of microsatellite markers for colony delineation of the invasive Asian subterranean termite (Blattodea: Rhinotermitidae) in South Florida and Taiwan
  6. Biology and life table of Oligonychus punicae Hirst (Trombidiformes: Tetranychidae) on three host plants
  7. Relative captures and detection of male Ceratitis capitata using a natural oil lure or trimedlure plugs
  8. Evaluation of HOOK SWD attract-and-kill on captures, emergence, and survival of Drosophila suzukii in Florida
  9. Rearing Neoseiulus cucumeris and Amblyseius swirskii (Mesostigmata: Phytoseiidae) on non-target species reduces their predation efficacy on target species
  10. Response of male Bactrocera zonata (Diptera: Tephritidae) to methyl eugenol: can they be desensitized?
  11. Monitoring of coccinellid (Coleoptera) presence and syrphid (Diptera) species diversity and abundance in southern California citrus orchards: implications for conservation biological control of Asian citrus psyllid and other citrus pests
  12. Topical treatment of adult house flies, Musca domestica L. (Diptera: Muscidae), with Beauveria bassiana in combination with three entomopathogenic bacteria
  13. Laboratory evaluation of 15 entomopathogenic fungal spore formulations on the mortality of Drosophila suzukii (Diptera: Drosophilidae), related drosophilids, and honeybees
  14. Effect of diatomaceous earth on diamondback moth, Plutella xylostella (Lepidoptera: Plutellidae), larval feeding and survival on cabbage
  15. Bioactivity of seed extracts from different genotypes of Jatropha curcas (Euphorbiaceae) against Spodoptera frugiperda (Lepidoptera: Noctuidae)
  16. Assessment of sugarberry as a host tree of Halyomorpha halys (Hemiptera: Pentatomidae) in southeastern USA agroecosystems
  17. The importance of multigeneration host specificity testing: rejection of a potential biocontrol agent of Nymphaea mexicana (Nymphaeaceae) in South Africa
  18. Endophytic potential of entomopathogenic fungi associated with Urochloa ruziziensis (Poaceae) for spittlebug (Hemiptera: Cercopidae) control
  19. The first complete mitogenome sequence of a biological control agent, Pseudophilothrips ichini (Hood) (Thysanoptera: Phlaeothripidae)
  20. Exploring the potential of Delphastus davidsoni (Coleoptera: Coccinellidae) in the biological control of Bemisia tabaci MEAM 1 (Hemiptera: Aleyrodidae)
  21. Behavioral responses of Ixodiphagus hookeri (Hymenoptera; Encyrtidae) to Rhipicephalus sanguineus nymphs (Ixodida: Ixodidae) and dog hair volatiles
  22. Illustrating the current geographic distribution of Diaphorina citri (Hemiptera: Psyllidae) in Campeche, Mexico: a maximum entropy modeling approach
  23. New records of Clusiidae (Diptera: Schizophora), including three species new to North America
  24. Photuris mcavoyi (Coleoptera: Lampyridae): a new firefly from Delaware interdunal wetlands
  25. Bees (Hymenoptera: Apoidea) diversity and synanthropy in a protected natural area and its influence zone in western Mexico
  26. Temperature-dependent development and life tables of Palpita unionalis (Lepidoptera: Pyralidae)
  27. Orchid bee collects herbicide that mimics the fragrance of its orchid mutualists
  28. Importance of wildflowers in Orius insidiosus (Heteroptera: Anthocoridae) diet
  29. Bee diversity and abundance in perennial irrigated crops and adjacent habitats in central Washington state
  30. Comparison of home-made and commercial baits for trapping Drosophila suzukii (Diptera: Drosophilidae) in blueberry crops
  31. Miscellaneous
  32. Dr. Charles W. O’Brien: True Pioneer in Weevil Taxonomy and Publisher
  33. Scientific Notes
  34. Nests and resin sources (including propolis) of the naturalized orchid bee Euglossa dilemma (Hymenoptera: Apidae) in Florida
  35. Impact of laurel wilt on the avocado germplasm collection at the United States Department of Agriculture, Agricultural Research Service, Subtropical Horticulture Research Station
  36. Monitoring adult Delia platura (Diptera: Anthomyiidae) in New York State corn fields using blue and yellow sticky cards
  37. New distribution records and host plants of two species of Hypothenemus (Coleoptera: Curculionidae: Scolytinae) in mangrove ecosystems of Tamaulipas, Mexico
  38. First record of Trichogramma pretiosum parasitizing Iridopsis panopla eggs in eucalyptus in Brazil
  39. Spodoptera cosmioides (Lepidoptera: Noctuidae) as an alternative host for mass rearing the parasitoid Palmistichus elaeisis (Hymenoptera: Eulophidae)
  40. Effects of biochar on ambrosia beetle attacks on redbud and pecan container trees
  41. First report of Diatraea impersonatella (Lepidoptera: Crambidae) on sugarcane (Saccharum officinarum L.) in Honduras
  42. Book Reviews
  43. Kratzer, C. A.: The Cicadas of North America
https://doi.org/10.1515/flaent-2024-0032
Schlagwörter für diesen Artikel
Asian citrus psyllid; Campeche; Mexico; Diva-GIS; modeling; Maxent
Creative Commons
BY 4.0

Artikel in diesem Heft

  1. Frontmatter
  2. Research Articles
  3. Distribution and dispersal of adult spotted wing drosophila, Drosophila suzukii (Diptera: Drosophilidae), in organically grown strawberries in Florida
  4. A comparison of the capture of non-target arthropods between control methods and monitoring traps of Anastrepha ludens in citrus agroecosystems
  5. Development of microsatellite markers for colony delineation of the invasive Asian subterranean termite (Blattodea: Rhinotermitidae) in South Florida and Taiwan
  6. Biology and life table of Oligonychus punicae Hirst (Trombidiformes: Tetranychidae) on three host plants
  7. Relative captures and detection of male Ceratitis capitata using a natural oil lure or trimedlure plugs
  8. Evaluation of HOOK SWD attract-and-kill on captures, emergence, and survival of Drosophila suzukii in Florida
  9. Rearing Neoseiulus cucumeris and Amblyseius swirskii (Mesostigmata: Phytoseiidae) on non-target species reduces their predation efficacy on target species
  10. Response of male Bactrocera zonata (Diptera: Tephritidae) to methyl eugenol: can they be desensitized?
  11. Monitoring of coccinellid (Coleoptera) presence and syrphid (Diptera) species diversity and abundance in southern California citrus orchards: implications for conservation biological control of Asian citrus psyllid and other citrus pests
  12. Topical treatment of adult house flies, Musca domestica L. (Diptera: Muscidae), with Beauveria bassiana in combination with three entomopathogenic bacteria
  13. Laboratory evaluation of 15 entomopathogenic fungal spore formulations on the mortality of Drosophila suzukii (Diptera: Drosophilidae), related drosophilids, and honeybees
  14. Effect of diatomaceous earth on diamondback moth, Plutella xylostella (Lepidoptera: Plutellidae), larval feeding and survival on cabbage
  15. Bioactivity of seed extracts from different genotypes of Jatropha curcas (Euphorbiaceae) against Spodoptera frugiperda (Lepidoptera: Noctuidae)
  16. Assessment of sugarberry as a host tree of Halyomorpha halys (Hemiptera: Pentatomidae) in southeastern USA agroecosystems
  17. The importance of multigeneration host specificity testing: rejection of a potential biocontrol agent of Nymphaea mexicana (Nymphaeaceae) in South Africa
  18. Endophytic potential of entomopathogenic fungi associated with Urochloa ruziziensis (Poaceae) for spittlebug (Hemiptera: Cercopidae) control
  19. The first complete mitogenome sequence of a biological control agent, Pseudophilothrips ichini (Hood) (Thysanoptera: Phlaeothripidae)
  20. Exploring the potential of Delphastus davidsoni (Coleoptera: Coccinellidae) in the biological control of Bemisia tabaci MEAM 1 (Hemiptera: Aleyrodidae)
  21. Behavioral responses of Ixodiphagus hookeri (Hymenoptera; Encyrtidae) to Rhipicephalus sanguineus nymphs (Ixodida: Ixodidae) and dog hair volatiles
  22. Illustrating the current geographic distribution of Diaphorina citri (Hemiptera: Psyllidae) in Campeche, Mexico: a maximum entropy modeling approach
  23. New records of Clusiidae (Diptera: Schizophora), including three species new to North America
  24. Photuris mcavoyi (Coleoptera: Lampyridae): a new firefly from Delaware interdunal wetlands
  25. Bees (Hymenoptera: Apoidea) diversity and synanthropy in a protected natural area and its influence zone in western Mexico
  26. Temperature-dependent development and life tables of Palpita unionalis (Lepidoptera: Pyralidae)
  27. Orchid bee collects herbicide that mimics the fragrance of its orchid mutualists
  28. Importance of wildflowers in Orius insidiosus (Heteroptera: Anthocoridae) diet
  29. Bee diversity and abundance in perennial irrigated crops and adjacent habitats in central Washington state
  30. Comparison of home-made and commercial baits for trapping Drosophila suzukii (Diptera: Drosophilidae) in blueberry crops
  31. Miscellaneous
  32. Dr. Charles W. O’Brien: True Pioneer in Weevil Taxonomy and Publisher
  33. Scientific Notes
  34. Nests and resin sources (including propolis) of the naturalized orchid bee Euglossa dilemma (Hymenoptera: Apidae) in Florida
  35. Impact of laurel wilt on the avocado germplasm collection at the United States Department of Agriculture, Agricultural Research Service, Subtropical Horticulture Research Station
  36. Monitoring adult Delia platura (Diptera: Anthomyiidae) in New York State corn fields using blue and yellow sticky cards
  37. New distribution records and host plants of two species of Hypothenemus (Coleoptera: Curculionidae: Scolytinae) in mangrove ecosystems of Tamaulipas, Mexico
  38. First record of Trichogramma pretiosum parasitizing Iridopsis panopla eggs in eucalyptus in Brazil
  39. Spodoptera cosmioides (Lepidoptera: Noctuidae) as an alternative host for mass rearing the parasitoid Palmistichus elaeisis (Hymenoptera: Eulophidae)
  40. Effects of biochar on ambrosia beetle attacks on redbud and pecan container trees
  41. First report of Diatraea impersonatella (Lepidoptera: Crambidae) on sugarcane (Saccharum officinarum L.) in Honduras
  42. Book Reviews
  43. Kratzer, C. A.: The Cicadas of North America
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Heruntergeladen am 1.4.2026 von https://www.degruyterbrill.com/document/doi/10.1515/flaent-2024-0032/html
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