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Article

Epidemiology of Xylella fastidiosa in Ibiza and Formentera: A Comprehensive Study of Insect Vectors and Transmission Dynamics

by
Miquel Llompart
1,2,*,
Josep Cifre
2,
Diego Olmo
3,
Andreu Juan
4,
Francesc Castellà
5,
Sergio Jiménez
6 and
Jordi Sabaté
1
1
Institut de Recerca i Tecnologia Agroalimentàries, Ctra. Cabrils, km 2, 08348 Cabrils, Spain
2
Enginyeria Agronòmica i Sostenibilitat de Sistemes Agraris, Departament d’Enginyeria Industrial i Construcció, Universitat de les Illes Balears, Ctra. de Valldemossa, km 7.5, 07122 Palma, Spain
3
Institut de Recerca i Formació Agroalimentària i Pesquera de les Illes Balears, C/ d’Eusebi Estada, 145, 07009 Palma, Spain
4
Servei d’Agricultura, Conselleria d’Agricultura, Pesca i Medi Natural, C/ de la Reina Constança, 4, 07006 Palma, Spain
5
Consell Insular d’Eivissa, Av. d’Espanya, 49, 07800 Eivissa, Spain
6
Consell Insular de Formentera, Plaça de la Constitució, 1, 07860 Formentera, Spain
*
Author to whom correspondence should be addressed.
Agronomy 2025, 15(2), 329; https://doi.org/10.3390/agronomy15020329
Submission received: 19 November 2024 / Revised: 22 January 2025 / Accepted: 27 January 2025 / Published: 27 January 2025
(This article belongs to the Special Issue Recent Trends Towards Genetics-Based Methods for Pest Management in Agroecosystems—Second Edition)
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Abstract

:
Xylella fastidiosa (XF) is a Gram-negative bacterium responsible for severe plant diseases affecting a wide range of host plants, some of them important crops. Since 2017, only the pauca subspecies (ST80) have been identified in Ibiza. XF is naturally transmitted by xylem sap-feeding insects; among them, only Philaenus spumarius (PS) and Neophilaenus campestris Fallén (NC) have been reported as potential insect vectors for XF in Ibiza. This study aims to investigate the dissemination of XF and to propose effective control strategies. The crops and the surrounding vegetation were sampled for potential vectors. DNA from insects was extracted and amplified by three qPCR methods, allowing subspecies identification. The results confirmed the continuous presence of adults of PS and NC in Ibiza and Formentera from May to December with important populations. During the summer period, PS captures predominantly took place within the surrounding woody vegetation adjacent to the plots. The main host plant for PS was Pinus halepensis Miller in Ibiza and Juniperus phoenicea subsp. turbinata (Guss.) Nyman in Formentera. In Ibiza, off the total PS captures, 4.47% tested positive for XF. These results confirm that PS is the main vector of XF on these islands, both in terms of captures and the percentage of positive insects for XF. In Formentera, despite the presence of potential vectors and the proximity and contact with Ibiza, no XF-positive insects were found, confirming the absence of the bacterium on the island.

1. Introduction

Xylella fastidiosa (XF) is a Gram-negative, xylem-inhabiting, and vector-transmitted bacterium. XF is a pathogen of significant concern due to its broad host range and severe impact on agriculture, forests, landscapes, and gardens, together with the quarantine and eradication measures effects. The bacterium has emerged as a serious threat to European agriculture, causing severe diseases in key crops for Mediterranean agriculture such as Pierce’s disease of vines, almond leaf scorch, and olive quick decline syndrome [1,2,3]. In Europe, XF was first reported in Apulia, Southern Italy, on declining olive trees [4]. Since then, it has been detected in various regions of Mediterranean Europe in different outbreaks with diverse strains, including the Balearic Islands, where it has been found in Majorca, Minorca, and Ibiza. Until today, the presence of XF in Formentera Island has not been reported. In Ibiza, the presence of the XF subspecies pauca (ST80) was confirmed in 2017 [5,6], posing a substantial threat to local agriculture, endemic plant species, and landscape. In Ibiza, XF especially affects economically important crops, such as olives and almonds, while vineyards and citrus remain not affected by pauca subspecies [7,8].
XF is naturally transmitted by xylem-feeding insects belonging to the suborder Auchenorrhyncha [9], including spittlebugs (Aphrophoridae and Cercopidae), cicadas (Cicadidae), and sharpshooters (Cicadellidae, subfamily Cicadellinae), which are considered potential vectors of the bacterium. The confirmed insect vector species of XF in Europe are Philaenus spumarius (PS), Neophilaenus campestris Fallén (NC), and Philaenus italosignus Drosopoulos and Remane, all belonging to the Aphrophoridae family [10,11]. Among these, PS is considered the main vector across European outbreaks due to its polyphagous nature and its widespread distribution across various ecosystems and hosts. Despite being commonly found, PS was not initially seen as a major threat until its role as a vector of XF was established.
Ibiza’s agroecosystems are characterized by a mosaic of Mediterranean woody crops and farmhouses surrounded by forests with the prevalence of gymnosperm species: Pinus halepensis Miller, Juniperus phoenicea subsp. Turbinate (Guss.) Nyman, and Juniperus oxycedrus subsp. Oxycedrus. The undergrowth consists of Pistacia lentiscus, Cneorum tricoccon, Rosmarinus officinalis, and Erica multiflora. Formentera vegetation is very similar to a large part of the island covered by forests of P. halepensis and J. phoenicea subsp. turbinata and coastal maquis of P. lentiscus, R. officinalis, Olea europaea var. sylvestris, Thymus vulgaris, and Cistus albidus. The agricultural land area in Ibiza is approximately 7754 ha. Carob, almond, and olive trees occupy the largest areas, covering 544 ha, 308 ha, and 204 ha, respectively, followed by vineyards and citrus with 74 ha and 73 ha, respectively [12]. This represents most of the cultivated land on an island where agriculture is in decline. At this moment, carob trees, vineyards, and citrus are not affected by XF subspecies pauca (ST 80). The widespread expansion of XF is endangering agriculture, landscapes, endemic biodiversity, and local cultivars. Currently, there are 15 host species of XF in Ibiza [13]. The most affected species are Lavandula dentata, Olea europaea var. europaea, O. europaea var. sylvestris, Polygala myrtifolia, Prunus dulcis (Mill.) D. A. Webb, R. officinalis, and Nerium oleander [8].
The spread of XF in agricultural landscapes is influenced by several factors, including vector behavior, host plant availability, and environmental conditions. In Ibiza and Formentera, a unique combination of wild and cultivated plants, coupled with diverse agricultural practices, creates a complex local environment for XF transmission. This study aimed to improve our understanding of the roles of PS and NC in the transmission and spread of XF and its relationship with the local strain pauca (ST80). This study includes Formentera Island especially to understand the factors that did not allow the presence of the bacterium until today, focusing on the vector hosts and dynamics. Furthermore, understanding the epidemiology of XF, including vector population dynamics, host–plant interactions, and infection rates, could be crucial for developing effective control measures for the island and understanding some of the general patterns of spread.

2. Materials and Methods

2.1. Study Area and Sampling Design

This study was conducted on the islands of Ibiza and Formentera from 2019 to 2021 (Table 1). In Ibiza, fourteen sampling plots were selected across the island, focusing on the predominant crops: olives, almonds, vineyards, and fig trees, as well as the surrounding woody vegetation. Two additional urban sampling points were included due to the high incidence of XF on ornamental plants. In Formentera, twelve sampling points were selected to determine the presence of XF potential vectors. For both islands, the sampling points were chosen in collaboration with local agricultural services.

2.2. Insect Vector Sampling

Hemipteran Auchenorrhyncha insect species were surveyed to capture potential vectors of XF. Sampling was conducted bimonthly in Ibiza and biannually in Formentera within the Aphrophoridae adult flight period. Insects were captured using sweep netting, with a total of 40 m2 per plant host, plot, and date of sampling. For shrubs and trees, the sampling unit was 4 m2 of canopy at ten randomized sampling points per host plant and plot. For herbaceous ground vegetation, sweep netting was conducted linearly by walking approximately 20 linear meters (0.50 m × 20 m = 10 m2), with four repetitions per plot. For grapevines trained in the double cordon, sweep netting involved sampling ten vines (1 m height trellis × 10 m in a straight line = 10 m2) with four repetitions per plot, alternating between both sides of the cordon and avoiding the edge rows. Auchenorrhyncha insect species were classified following Ribaut [14], Della Giustina [15], and Holzinger et al. [16] and stored at −20 °C until analysis.

2.3. DNA Extraction from Insects

DNA from individual insects was extracted using the CTAB/Chloroform method, following the established EPPO [17] protocols. For xylem feeders (Aphrophoridae), only the heads were used for extraction, whereas entire phloem-feeding leafhoppers were fully crushed, both using Tissuelyser II (Qiagen®, Hilden, Germany). The extracted DNA was resuspended in 50 µL of HPLC-grade water and stored at −20 °C.

2.4. Detection of X. fastidiosa Subspecies

The XF detection in insect vectors was conducted using three different qPCR methods targeting different genomic regions of XF: Harper et al. [18] and Francis et al. [19] following EPPO recommendations [17]. Subspecies identification was performed using multiplex qPCR by Dupas et al. [20]. Primers and probes were synthesized by Metabion® (Planegg, Germany). Reactions were carried out in QuantStudio 3 (Applied Biosystems®, Waltham, MA, USA). The Harper qPCR detection method targets the Ribosome Maturation Factor RimM gene, and Francis targets the HL gene [21]. DNA from pure cultures of different XF subspecies from the Balearic Islands, provided by the official Plant Health Laboratory, and HPLC-grade water were used as positive controls and negative controls, respectively. To exclude nonspecific and weak amplifications, samples were considered positive with a Ct value below 35 cycles across all three general XF detection methods, with three technical replicates.

2.5. Statistical Analysis

Statistical analyses were performed using the IBM SPSS software package 23.0 [22]. Statistical significance for all data was accepted at a p-value < 0.05 (α-level). The chi-square test (χ2) was used to identify significant differences in the PS/NC ratio across sampling periods and years for both Ibiza and Formentera. It was also applied to detect significant differences in the frequency of XF-infected specimens captured in Ibiza across different sampling periods, years, and among the various host plants. When the data exhibited normal distribution and homogeneity of variance, a factorial ANOVA was conducted to assess significant differences in population density. The Duncan test was used to evaluate statistical differences between means (p < 0.05), as indicated by the ANOVA. A generalized linear model (GLM) with a negative binomial distribution was applied to analyze the number of captures per host plant and the number of positive insects per host plant. Fixed factors included in the model were plot, year, and host plant.

3. Results

3.1. Aphrophoridae Distribution, Host Plants, and Dynamics

Adults of PS and NC were captured on both Ibiza and Formentera, with their seasonal occurrence shown in Figure 1. No other xylem-feeding species were captured. In Ibiza, a total of 2491 Aphrophoridae were collected, comprising 85.35% PS and 14.65% NC. In Formentera, 553 Aphrophoridae were captured, with 87.70% identified as PS and 12.30% as NC. The highest number of aphrophorids was recorded in 2020 for both islands and both species. The PS/NC ratio differed significantly between sampling periods in Formentera (Ibiza: χ2 = 0.091, p = 0.955; Formentera: χ2 = 6.682, p = 0.010) and between years in Ibiza (Ibiza: χ2 = 83.288, p < 0.001; Formentera: χ2 = 1.041, p = 0.594).
It is important to note that the analysis indicated statistically significant differences between PS and NC, with the population density of PS being five times higher than that of NC on both islands (Ibiza: F = 5.907, d.f. = 1, p = 0.017; Formentera: F = 6.316, d.f. = 1, p = 0.017). The statistical analysis highlighted that these differences did not depend on the year. In the case of PS, Ibiza exhibited a higher PS population density compared to Formentera; however, these differences were not statistically significant (F = 0.759, d.f. = 1, p = 0.387). Similarly, the differences observed between years on both islands were also not statistically significant (Ibiza: F = 2.072, d.f. = 1, p = 0.157; Formentera: F = 1.971, d.f. = 1, p = 0.170).
In Ibiza, PS adults were captured from mid-May to early December. In late spring, the capture of PS adults shifted to wild woody vegetation, particularly on P. halepensis during the summer. In autumn, captures returned to herbaceous hosts, notably Dittrichia viscosa (L.) Greuter and Foeniculum vulgare Mill (Figure 2). In Ibiza, high numbers of PS adults were captured on more than seventeen different wild species, both woody and herbaceous, while in Formentera, they were captured on more than nine species (Figure 3). In 2020, when population density was at its highest, the number of host plant species was also the greatest on both islands. Most PS adults were collected from wild and cultivated woody plants. Specifically, in Ibiza, 329, 214, and 171 individuals were collected on P. halepensis, P. dulcis, and P. lentiscus, respectively. Finally, it cannot be overlooked that 68 captures were made on J. phoenicea subsp. turbinata, an important species in the dynamics, although its significance was lower compared to the results obtained on Formentera. Similarly, in Formentera, 114, 68, and 57 PS adults were collected on Vitis vinifera, J. phoenicea subsp. turbinata, and P. lentiscus, respectively. It is worth noting that in the June 2020 sampling, a total of 107 adult PS individuals were captured on a single V. vinifera plot (2.68 adults PS m−2).

3.2. Detection of X. fastidiosa in the Potential Insect Vectors

During the three-year survey conducted in Ibiza and Formentera, a total of 3063 Auchenorrhyncha specimens were collected, identified, and analyzed for XF. The total number of insects per island and per year, along with their taxa and the qPCR detection results for XF, are reported in Tables S3 and S4. In Ibiza, the collected insects belonged to three families, with the Cicadellidae family being the most species diverse. In contrast, in Formentera, the insects collected also belonged to only three families. XF was detected exclusively in Ibiza. The only species that tested positive for XF were PS and NC. Only the pauca strain was detected among the positive cases. PS was shown to be more infected by XF compared to NC (PS: 4.47%; NC: 1.64%; χ2 = 6.474, p = 0.011).
For PS, the occurrence of XF-positive individuals differed between years (χ2 = 9.322, p = 0.009). The first XF-positive individuals were detected in May. The results indicated that the sampling time was significantly different (χ2 = 9.688, p = 0.008). The rate reached its peak in late summer and early autumn, coinciding with the strongest qPCR titers (Ct value < 30) detected (Figure 4). After this peak, the incidence of positive PS decreased rapidly at the end of October. In 2019, of the PS adults captured in early December, only one specimen tested positive for XF. In 2020, the incidence of positive PS adults remained substantially constant from July to early October.
At least one insect tested positive for XF in 10 out of the 14 plots studied. There were significant differences in infection rates between insects captured on different plots (χ2 = 98.286, p < 0.001). The infection rate PS ranged from 0.00% (Plots 2, 8, 11, and 14) to 42.31% (Plot 13) (Table S4). In October 2019, a positivity peak of 64% was recorded in Plot 13.
The herbaceous species compartment had the highest number of PS captures and the highest number of positive insects (41+/1196). Among the woody species, P. halepensis was the main host plant for PS with infection rates of around 3%, a similar infection percentage to that of the specimens captured on the spontaneous cover crop (Table 2). These observed differences in the total number of positive insects per host plant were not statistically significant (χ2 = 7417.168, d.f. = 5, p = 0.191). However, the positivity levels for XF varied significantly, depending on the host plant where the capture was made (χ2 = 114.013, p < 0.001). This fact is explained by a positivity rate exceeding 60% in insects captured on ornamental species. The positivity rate of the insects captured on P. lentiscus was 8.19%, reaching 18.75% in October 2020. A similar positivity rate was recorded in the specimens captured on C. siliqua. Adult PS individuals captured on P. dulcis exhibited an infection rate of approximately 5%. No specimen of PS (n = 67) captured on J. phoenicea subsp. turbinata tested positive for XF.

4. Discussion

Understanding the vector species responsible for the spread of XF and its behavior is essential for elucidating its epidemiology and developing effective control measures to reduce the impact of the diseases caused by this vector-borne pathogen. In this context, the seasonal abundance and the infection rate of vectors play a pivotal role, as they directly affect transmission dynamics and the establishment of the disease in susceptible crops [23]. The results of this study underscore the importance of understanding vector ecology and host interactions for the effective management of XF.
Our results confirm the key role of spittlebugs in the transmission of XF in Mediterranean Europe [11]. However, before the emergence of XF in Europe, few studies had focused on the woody host plants of these vectors, primarily because PS was not considered a major cause of significant crop losses [24,25,26]. Surveys of potential vectors are a critical first step in understanding the epidemiology of XF infections and mitigating their harmful effects. This study aims to contribute to the growing body of knowledge on XF and its vectors in Europe, particularly on wild woody hosts, a key reservoir more difficult to manage than crops. This is particularly important in Ibiza, where agricultural plots are few and are melted in a mosaic of woods, abandoned agricultural fields, and private gardens in disperse villas. In addition to these particularities for the management of the disease on the island, it is necessary to take into account the presence of a specific strain, XF subspecies pauca (ST80), with particular characteristics in severity and host range compared to pauca (ST52) in Apulia and, evidently, with the pauca strains in central and south America.
In Ibiza, only two species of xylem sap feeders were captured, with 2126 PS and 365 NC individuals, confirming the low diversity of potential XF vector species in the Balearic Islands and the preeminence of PS [27,28]. The population densities were higher than those recorded by López [27].
The observed capture pattern of adult aphrophorids on the ground cover suggests two peaks of activity on these plant hosts, with some individuals remaining active until late December. This seasonal behavior indicates that adult aphrophorids use the herbaceous hosts as a habitat before moving to woody crops from late spring to early autumn, when they mate and lay eggs on them. The initial movement from the canopy to the crop, followed by dispersal to P. halepensis, J. phoenicea subsp. turbinata, and P. lentiscus in early summer, highlights a potential shift in habitat preference that could influence XF acquisition and vector–pathogen dynamics. These findings underscore the importance of considering seasonal and habitat-specific behaviors when assessing vector management strategies. During summer months, the spittlebugs dispersed into woody vegetation surrounding the agroecosystems. This observation is supported by other authors [29,30,31,32]. Additionally, an aggregation phenomenon of PS adults was probably observed on specimens of P. halepensis. This phenomenon is attributed to the fact that insects feeding on xylem sap are highly sensitive to plant turgor and xylem nutritional composition [33,34]. In this case, this phenomenon could be related to the aridity of the islands and the limited arboreal vegetation, especially in Formentera, where the aggregation phenomena were also likely observed in a vineyard. In Ibiza, the presence of P. halepensis in most of the agroecosystems on the island explains why the spittlebugs resist the summer months maintaining an important population. Lopes et al. [35] and Morente et al. [36] reported that in central Spain, NC adults were abundant in P. halepensis, a non-host plant for XF, during the summer. Therefore, the presence of P. halepensis in the vicinity of the crop may favor the establishment and proliferation of NC in a specific area throughout the year [37].
However, despite not colonizing almonds, vines, and olive trees, in late spring and early summer, when they disperse and before returning to cover, NC can briefly probe the canopy of trees in different crops, potentially acquiring and transmitting XF from one tree to another. Similar results have been obtained in the Iberian Peninsula and Italy [36,38,39,40].
In Ibiza, 4.71% (92+/2126) of PS and 1.64% (6+/65) of NC specimens tested positive for XF. However, similar infectivity percentages were identified in the Valencian Community (Spain) [41]. In general, the low percentage of XF-positive insects could be explained by the fact that most of the crops were surrounded by specimens of P. halepensis and J. phoenicea subsp. turbinata, which are non-host species for XF [42]. As demonstrated by our results, most of these insects seek refuge during the drier months in specimens of these species. Therefore, the potential vector may have left the crop without visiting any plants positive for XF. Additionally, in vineyard agroecosystems, V. vinifera is not a host of the pauca subspecies (ST80) [8]. Finally, in olive agroecosystems, the advanced stage of OQDS could partly explain the few captures in the canopy of O. europaea specimens.
Most insects carrying the XF bacterium were captured during October. These results align with those obtained by Saponari et al. [11], who recorded the highest prevalence rate of XF in insects captured during the first week of November. Overall, the highest infection rate in Ibiza, 60%, was recorded on individuals captured on ornamental species in urban areas, where there are no gymnosperm communities to aestivate. Apart from ornamental species, it is noteworthy that the highest XF prevalence rates in insects were obtained in PS adults captured on C. siliqua and P. lentiscus, with an XF prevalence of 10.26% and 8.19. To date, both plant species are not considered hosts of XF [42]; however, a species of the same genus, specifically Pistacia vera, is a host of the XF bacterium [43]. Ben Moussa et al. [44] obtained a similar XF prevalence at a site located 500 m from the central outbreak, where 9% of adults were found positive. Probably, the infected vectors captured on C. siliqua and P. lentiscus acquired the bacterium during previous feeding on infected hosts, as PS retains XF throughout its adult life, and it is unlikely that the last plant visited is responsible for the infection. However, this finding demonstrates the high mobility of the insect.
Our samplings confirmed the presence of PS and NC in Formentera, where their presence had not been reported before the year 2019. The number of captures was surprisingly high for an island with severe drought conditions, poor vegetation growth, and where the presence of aphrophorids had not previously been documented. Notably, a significant number of PS individuals were captured during a single sampling event in a vineyard canopy, with nearly 100 insects captured within a sampling area of 40 m2 (2.68 individuals/m2) in La Mola. La Mola is a broad plateau elevated above the eastern end of the island, where vineyards are surrounded by Mediterranean pastures. This high density likely resulted from an aggregation phenomenon caused by the absence of arboreal vegetation at the vineyard borders. Initially, PS adults could concentrate on the vine canopies before migrating to surrounding wild woody vegetation, in this case, P. halepensis and J. phoenicea specimens more than one kilometer away from the vineyards.
XF was not detected in the spittlebugs collected from Formentera. These results were consistent with the results of analyzed plants, supporting the disease surveys on the island [8,45,46,47]. However, while the EFSA suggests that plant monitoring may be more effective for XF detection, the sentinel insects could be a valuable complement in situations where there are captures of vectors in woody hosts and there are no symptomatic plants. In our case, however, the number of captures on the island of Formentera was high. Therefore, the use of these sentinel insects could still contribute to the early detection of a focus of infection.
Active surveillance of the area is crucial for the early detection of outbreaks [48], and the use of sentinel insects could contribute to this effort. The effectiveness of sentinel insects in monitoring the bacterium has been demonstrated in France, Spain, and Italy [44,48,49,50,51]. Monitoring plant movements alone may not be sufficient to prevent the introduction of XF to Formentera. The passive movement of vectors by wind and the ‘hitchhiking’ of infected insects on vehicles can facilitate their long-distance dispersal [39,52,53]. Therefore, the high spittlebug population in Ibiza, combined with significant vehicle movement between the islands, poses a considerable risk of an infected insect being introduced to Formentera and subsequently transmitting XF to a host plant. Moreover, when a vector-borne pathogen is introduced into an environment with suitable climatic conditions and the presence of vectors, the probability of its establishment and spread increases [54,55,56]. As a result, the establishment of XF on the island of Formentera is a significant risk that must be addressed proactively.
In conclusion, our findings confirm PS as the primary vector species in Ibiza, with NC playing a secondary role in disease transmission. Given that the eradication of XF in Ibiza is currently unfeasible, these results provide a basis for the development of effective, environmentally sustainable control strategies aimed at managing spittlebugs and their capacity to acquire and transmit XF. The goal is to mitigate the spread of the pathogen while maintaining agricultural productivity. These control strategies should be tailored to each specific pathosystem, taking into account the complex interactions among vectors, host plants, and crops. A multifaceted approach should be implemented to disrupt several interactions, including reducing both inoculum sources and vector populations.
Additionally, this study offers valuable insights into the spread of the XF pathogen in the Mediterranean region. Further research is necessary to deepen our understanding of the ecology and epidemiology of XF and its vectors, which is critical for designing effective management strategies to allow the coexistence with the bacterium as it continues to spread across Mediterranean Europe.

Supplementary Materials

The following supporting information can be downloaded at https://www.mdpi.com/article/10.3390/agronomy15020329/s1. Table S1: Host plant species of N. campestris per island and year (2019–2021); Table S2: Potential insect vector species collected during the 2019–2021 period in Ibiza and the identification of species that are carriers of X. fastidiosa; positives have a Ct value of qPCR < 35; Table S3: Potential insect vector species collected during the 2019–2021 period in Formentera and the identification of species that are carriers of X. fastidiosa; positives have a Ct value of qPCR < 35; Table S4: Number and percentage of P. spumarius captured in Ibiza carriers of the X. fastidiosa per plot (2019–2021); positives have a Ct value of qPCR < 35; Table S5: Number and percentage of P. spumarius captured in Formentera carriers of X. fastidiosa per host plant and year (2019–2021); positives have a Ct value of qPCR < 35; Table S6: Number and percentage of N. campestris captured in Formentera carriers of X. fastidiosa per host plant and year (2019–2021); positives have a Ct value of qPCR < 35.

Author Contributions

In this manuscript, the individual contributions of the authors are as follows: conceptualization, J.S.; methodology J.S.; formal analysis, M.L.; data curation, M.L., J.C., D.O., A.J., F.C., S.J. and J.S.; writing—original draft preparation, M.L.; writing—review and editing, M.L., J.C., D.O., A.J., F.C., S.J. and J.S.; supervision, J.S. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by grants 4384/2018 from the Government of the Balearic Islands and E-RTA 2017-00004-C06-05 from INIA-AEI, Spain.

Data Availability Statement

The original contributions presented in the study are included in the article/Supplementary Material; further inquiries can be directed to the corresponding author.

Acknowledgments

The authors are grateful to J.A. Domínguez, J. Torres, E. Peñalvo, J. Argente, J.M. Marín, and Grupo Tragsa for their field support.

Conflicts of Interest

The authors declare no conflicts of interest.

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Figure 1. Number of P. spumarius individuals captured per year (2019–2021): (a) Ibiza; (b) Formentera.
Figure 1. Number of P. spumarius individuals captured per year (2019–2021): (a) Ibiza; (b) Formentera.
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Figure 2. The average number of P. spumarius individuals captured per unit area in the crop canopy, vegetation cover, and wild vegetation from 2019 to 2021 in Ibiza.
Figure 2. The average number of P. spumarius individuals captured per unit area in the crop canopy, vegetation cover, and wild vegetation from 2019 to 2021 in Ibiza.
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Figure 3. Host plant species of P. spumarius per year (2019–2021): (a) Ibiza; (b) Formentera.
Figure 3. Host plant species of P. spumarius per year (2019–2021): (a) Ibiza; (b) Formentera.
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Figure 4. Percentage of P. spumarius carriers of ‘X. fatidiosa’. The results are presented per month of sampling and year in Ibiza. qPCR analysis by Harper et al. (2010, erratum 2013) [18] and Francis et al. (2006) [19]. Strong positives (Ct value of qPCR < 30); weak positives (Ct value of qPCR 30–35).
Figure 4. Percentage of P. spumarius carriers of ‘X. fatidiosa’. The results are presented per month of sampling and year in Ibiza. qPCR analysis by Harper et al. (2010, erratum 2013) [18] and Francis et al. (2006) [19]. Strong positives (Ct value of qPCR < 30); weak positives (Ct value of qPCR 30–35).
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Table 1. Plot location and their characteristics and vegetation of the surroundings.
Table 1. Plot location and their characteristics and vegetation of the surroundings.
ID/IslandNameLocationCropVegetation of the Surroundings
Plot 1 1Bodega Ibizkus38°52′ N 01°15′ EV. viniferaC. siliqua, C. albidus, E. arborea, J. phoenicea, J. oxycedrus, P. halepensis, P. lentiscus, P. dulcis, and R. officinalis
Plot 2 1Can Benet38°55′ N 01°18′ EO. europaea and V. viniferaC. siliqua, C. albidus, E. arborea, J. phoenicea, O. europaea, P. vulgare, P. halepensis, P. lentiscus, and R. officinalis
Plot 3 1Bodega Can Rich38°59′ N 01°20′ EO. europaea and V. viniferaA. donax, C. siliqua, D. kaki, O. europaea, P. vulgare, and P. dulcis
Plot 4 1Can Secorrat39°00′ N 01°21′ EC. siliqua, O. europaea, and V. viniferaC. albidus, E. arborea, J. phoenicea, J. oxycedrus, P. halepensis, P. lentiscus, and Q. ilex
Plot 5 1Pla de Corona39°02′ N 01°20′ EP. dulcisC. siliqua, J. phoenicea, O. europaea, P. halepensis, and P. lentiscus
Plot 6 1Pla d’Albarca39°02′ N 01°22′ EV. vinifera-
Plot 7 1Camí de Cas Vidals39°04′ N 01°28′ EC. siliquaC. albidus, D. viscosa, J. phoenicea., O. europaea, P. lentiscus, and R. officinalis
Plot 8 1Can Tixedó39°04′ N 01°29′ ENon-crop areasC. albidus, J. phoenicea, P. vulgare, P. lentiscus, and R. officinalis
Plot 9 1Crtra. de Sant Joan39°00′ N 01°29′ ENon-crop areasD. viscosa, J. phoenicea, P. lentiscus L., and P. vulgare
Plot 10 1Can Miquel Guasch38°59′ N 01°28′ EO. europaeaC. siliqua L., D. viscosa, J. oxycedrus, O. europaea, P. vulgare, P. halepensis, P. lentiscus, P. dulcis, and R. officinalis
Plot 11 1Can Marquet39°01′ N 01°29′ ECitrus sp. and O. europaeaC. siliqua, C. albidus, D. viscosa, J. regia, J. phoenicea, J. oxycedrus, L. nobilis, N. oleander, P. halepensis, P. lentiscus, Q. ilex, and R. officinalis
Plot 12 1Necrópolis des Puig des Molins38°54′ N 01°25′ EUrbanD. viscosa and P. vulgare
Plot 13 1Es viver38°54′ N 01°25′ EUrbanC. australis, C. siliqua, L. dentata, O. europaea, P. halepensis, P. myrtifolia, and R.officinalis
Plot 14 1Agrotourism Can Planells39°02′ N 01°25′ ECitrus sp. and P. americanaC. siliqua, C. albidus, E. arborea, J. phoenicea, J. oxycedrus, P. halepensis, O. europaea, P. lentiscus, Q. ilex, and R. officinalis
Plot 15 2Bodega Terramoll38°40′ N 01°32′ EV. viniferaP. lentiscus
Plot 16 2Vénda des Pi des Català38°41′ N 01°26′ ENon-crop areasJ. phoenicea and P. lentiscus
Plot 17 2El Pilar de la Mola38°40′ N 01°34′ EV. viniferaD. viscosa, J. phoenicea, P. halepensis, P. lentiscus, R. officinalis
Plot 18 2Pol. 2 Parc. 15738°41′ N 01°23′ EO. europaeaJ. phoenicea, and P. lentiscus
Plot 19 2Bodega Cap de Barberia38°39′ N 01°24′ EV. viniferaC. albidus, J. phoenicea, O. europaea, and R. officinalis
Plot 20 2Pol. 1 Parc. 29738°40′ N 01°24′ EO. europaeaJ. phoenicea and P. lentiscus
Plot 21 2Pol. 1 Parc. 14438°40′ N 01°25′ EO. europaeaJ. phoenicea and R. officinalis
Plot 22 2Pol. 2 Parc. 19738°41′ N 01°25′ EO. europaeaP. vulgare
Plot 23 2Pol. 14 Parc. 17838°39′ N 01°34′ EO. europaeaD. viscosa and P. vulgare
Plot 24 2Sa Figuera (Pol. 2 Parc. 95)38°41′ N 01°25′ EF. caricaP. lentiscus
Plot 25 2Figueres Can Toni Mestre38°41′ N 01°29′ EF. caricaP. lentiscus
Plot 26 2Bellotera de Can Vicent d’es Torrent38°42′ N 01°26′ ENon-crop areasQ. ilex and D. viscosa
1 Ibiza; 2 Formentera.
Table 2. Number and percentage of P. spumarius captured in Ibiza carriers of X. fastidiosa per host plant and year (2019–2021). Positives (Ct value of qPCR < 35).
Table 2. Number and percentage of P. spumarius captured in Ibiza carriers of X. fastidiosa per host plant and year (2019–2021). Positives (Ct value of qPCR < 35).
Host Plant Species of Adult P. spumarius CapturedqPCR Detection 1
201920202021Total
P. myrtifolia0+/02+/4 (50.00)0+/02+/4 (50.00)
C. siliqua0+/03+/32 (9.38%)1+/7 (14.29%)4+/39 (10.26%)
D. kaki0+/00+/28 (0.00%)0+/00+/28 (0.00%)
D. viscosa2+/13 (15.38%)0+/00+/1 (0.00%)2+/14 (14.29%)
F. carica0+/0 1+/19 (5.26%)0+/01+/19 (5.26%)
J. phoenicea subsp. turbinata0+/00+/62 (0.00%)0+/5 (0.00)0+/67 (0.00%)
D. viscosa2+/13 (15.38%)0+/00+/1 (0.00%)2+/14 (14.29%)
O. europaea var europaea0+/00+/5 (0.00%)0+/00+/5 (0.00%)
O. europaea var sylvestris0+/00+/00+/1 (0.00%)0+/1 (0.00%)
Other herbaceous species23+/705 (3.26%)9+/446 (2.02%)9+/45 (20.00%)41+/1196 (3.43%)
Other ornamentals species9+/14 (64.29%)0+/00+/09+/14 (64.29%)
Other woody species0+/00+/6 (0.00%)0+/00+/6 (0.00%)
P. halepensis0+/09+/278 (3.24%)2+/51 (3.92%)11+/329 (3.34%)
P. lentiscus0+/4 (0.00%)13+/158 (8.23%)1+/9 (11.11%)14+/171 (8.19%)
P. dulcis0+/010+/196 (5.10%)1+/18 (5.55%)11+/214 (5.14%)
Q. ilex0+/00+/1 (0.00%)0+/00+/1 (0.00%)
V. vinifera0+/00+/180+/00+/18 (0.00%)
GLM: total capturesAIC1353.750
p (host plant species)0.000
p (plot)0.000
p (year)0.000
GLM: number of positives (+)AIC231.244
p (host plant species)0.191
p (plot)0.008
p (year)0.486
Pearson correlation: total captures and number of positives (+)r0.639 **
p<0.001
Chi-square test: percentage of positives for XFr114.013
p<0.001
1 qPCR analysis by Harper et al. (2010, erratum 2013) [18] and Francis et al. (2006) [19]. The results are the number of positives (+)/totals analyzed. ** Correlation is significant at the 0.01 level.
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Llompart, M.; Cifre, J.; Olmo, D.; Juan, A.; Castellà, F.; Jiménez, S.; Sabaté, J. Epidemiology of Xylella fastidiosa in Ibiza and Formentera: A Comprehensive Study of Insect Vectors and Transmission Dynamics. Agronomy 2025, 15, 329. https://doi.org/10.3390/agronomy15020329

AMA Style

Llompart M, Cifre J, Olmo D, Juan A, Castellà F, Jiménez S, Sabaté J. Epidemiology of Xylella fastidiosa in Ibiza and Formentera: A Comprehensive Study of Insect Vectors and Transmission Dynamics. Agronomy. 2025; 15(2):329. https://doi.org/10.3390/agronomy15020329

Chicago/Turabian Style

Llompart, Miquel, Josep Cifre, Diego Olmo, Andreu Juan, Francesc Castellà, Sergio Jiménez, and Jordi Sabaté. 2025. "Epidemiology of Xylella fastidiosa in Ibiza and Formentera: A Comprehensive Study of Insect Vectors and Transmission Dynamics" Agronomy 15, no. 2: 329. https://doi.org/10.3390/agronomy15020329

APA Style

Llompart, M., Cifre, J., Olmo, D., Juan, A., Castellà, F., Jiménez, S., & Sabaté, J. (2025). Epidemiology of Xylella fastidiosa in Ibiza and Formentera: A Comprehensive Study of Insect Vectors and Transmission Dynamics. Agronomy, 15(2), 329. https://doi.org/10.3390/agronomy15020329

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