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Article

Population Dynamics of Potential Insect Vectors of Xylella fastidiosa (Xanthomanadales: Xanthomonadaceae) and Other Auchenorrhyncha in Olive and Citrus Groves of Crete, Greece

by
Ioannis E. Koufakis
1,2,*,
Argyro P. Kalaitzaki
2,
Maria L. Pappas
1,
Antonios E. Tsagkarakis
3,
Despina K. Tzobanoglou
4 and
George D. Broufas
1
1
Department of Agricultural Development, Democritus University of Thrace, Pantazidou 193, 68200 Orestiada, Greece
2
Institute of Olive Tree, Subtropical Plants and Viticulture, Hellenic Agricultural Organization ‘DEMETER’, Leoforos Karamanli 167, 73100 Chania, Greece
3
Department of Crop Science, Agricultural University of Athens, Iera Odos 75, 11855 Athens, Greece
4
Department of Rural Development of Chania, Hellenic Ministry of Rural Development and Food, Agrokipio, 73100 Chania, Greece
*
Author to whom correspondence should be addressed.
Agronomy 2024, 14(10), 2243; https://doi.org/10.3390/agronomy14102243
Submission received: 7 August 2024 / Revised: 20 September 2024 / Accepted: 27 September 2024 / Published: 28 September 2024
(This article belongs to the Special Issue Viral Diseases and the Threats of Their Arthropod Vectors to Crop Health: Surveillance, Detection, and Early-Warning Systems)
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Abstract

:
This study investigated the phenology and population dynamics of potential insect vectors of Xylella fastidiosa Wells et al. and other Auchenorrhyncha species in olive and citrus groves of Chania province, Crete, Greece. Although X. fastidiosa has not been reported in Greece, its introduction could cause serious diseases in many crops, including olives and citrus. Olive groves of Olea europaea L. ‘Koroneiki’ were sampled systematically using sweep net and Malaise traps over 24 months. One citrus grove was sampled for one year using a Malaise trap. Sweep net samples were taken from the herbaceous cover, tree canopy, and field borders of olive groves. Auchenorrhyncha were more abundant on the herbaceous cover compared to the canopy and field margins. Aphrophoridae species were mostly found on the herbaceous cover and in low numbers during fall (October–December) and spring (April–May). Cicadellidae species, such as Euscelis spp., were frequently found on the herbaceous cover of both olive and citrus groves. One Aphrophoridae and several Cicadellidae species were recorded in the citrus grove. Altitude was found to influence the population abundance of some Auchenorrhyncha species in olive groves. These results provide information for effective integrated management of insect vectors and their vector-borne pathogens.

1. Introduction

Hemipteran insects are devastating pests of crops due to their wide host range, rapid reproduction, and their ability to vector plant diseases. They are, by far, the most important insect vectors of plant-infecting pathogens [1,2]. In recent decades, vector-borne diseases have caused some of the most devastating plant diseases in perennial and annual crops in Europe due to global trade of propagation material and ornamental plants as well as the high movement of people across Europe and the world [3]. In Greece, several vector-borne pathogens have been recorded during the last decades such as the Citrus Tristetsa virus [4] transmitted by aphids, the Tomato chlorosis virus transmitted by the whitefly Bemisia tabaci (Gennadius) (Hemiptera: Aleyrodidae) causing the tomato yellows disease [5], as well as the Candidatus Liberibacter solanacearum (Rhizobiales: Rhizobiaceae) spread by psyllid insect vectors [6].
Moreover, a serious potential threat, not yet recorded in Greece, is the vector-dependent plant pathogenic bacterium Xylella fastidiosa Wells et al. (Xanthomanadales: Xanthomonadaceae) [7], which is listed in the A2 Quarantine list of EPPO [8] due to the high potential risk in the EPPO region [9]. Additionally, the pathogen is regulated in the EU as a quarantine pest under Regulation (EU) 2016/2031 (‘Plant Health Law’) on protective measures against plant pests and listed in the ANNEX II of quarantine pests. Xylella fastidiosa is an endophyte native to the Americas [10] and has been found to cause several important diseases to economically important crops such as the Pierce’s disease of grapevine (Vitis vinifera L.) and variegated chlorosis in citrus in the Americas [11]. This bacterium is restricted to the xylem of plants; it is transmitted through Hemiptera (=homopteran) xylem-feeding insect vectors in nature [12] and has a wide spectrum of host plant species (664 host plants species) within 88 botanical families [13]. These insect vectors belong to the Cicadomorpha infraorder, the suborder of Auchenorrhyncha, and to the families Cicadellidae (sharpshooter leafhoppers of the subfamily Cicadellinae), Aphrophoridae (spittlebugs), Cercopidae (froghoppers), and Membracidae (treehoppers) [14,15,16]. Cicadidae and Tibicinidae species are also considered as potential insect vectors although their role in X. fastidiosa transmission is likely negligible [17,18]. However, most sharpshooter species, which are considered important vectors of X. fastidiosa in the Americas, are absent in Europe [11].
In Europe, X. fastidiosa (ssp. pauca) was initially detected in 2013 on symptomatic olive trees in the province of Lecce Region in Apulia, Italy, causing the so-called “Olive Quick Decline Syndrome” (OQDS), affecting about 10,000 ha of olive trees [19,20,21], while recent study estimated that in the Salento area, about 6.5 million trees have been infected [22,23]. Since the Apulian outbreak, several subspecies and strains of the pathogen have been found in other European countries such as France (Corsica and Provence-Alpes-Côte d’Azur region), Spain (Balearic Islands, Valencia, Madrid), central Italy (Tuscany), Portugal (Porto), and Germany (isolated finding in Saxony) [8,24,25,26].
In total, 78 candidate vector species are present across the countries of Europe where X. fastidiosa has been detected [27]. However, the most important X. fastidiosa vector in all the associated epidemics in Italy, France (Corsica), and Spain is the meadow spittlebug Philaenus spumarius L. (Hemiptera: Aphrophoridae) [21,28,29,30,31]. The Philaenus genus, and especially P. spumarius, a very common species in Europe, has been studied extensively by geneticists for over 40 years for its color polymorphism [32,33,34]. In the Mediterranean, there are eight recorded species belonging to the Philaenus genus, but only three species in Greece (P. spumarius, P. signatus Melichar, and P. loukasi Drosopoulos & Asche) [35,36,37]. A recent study confirmed that two more xylem-sap feeding spittlebug species, namely Neophilaenus campestris Fallen and Philaenus italosignus Drosopoulos & Remane, can be vectors of X. fastidiosa since they acquired and transmitted the pathogen successfully [38].
A rich Auchenorrhyncha diversity (437 species) has been recorded in Greece in various habitats [37,39,40]. A recent study showed that most European potential insect vectors of X. fastidiosa were found in relatively low numbers in the olive orchards [41]. According to the study by Antonatos et al. [42], 48 species of the families Cicadellidae, Aphrophoridae, and Cercopidae, of which 23% were spittlebugs, were recorded. More in-depth surveys are needed to enrich our understanding of the diversity, biology, and ecology of potential insect vectors of X. fastidiosa and other Auchenorrhyncha within Cretan agroecosystems.
Therefore, in this study a 2-year investigation was performed to: (1) identify the potential insect vectors in the suborder Auchenorrhyncha with special reference to those associated with X. fastidiosa in different olive groves covering most of the altitude range of olive cultivation in Crete by using two sampling methods, (2) identify the potential Auchenorrhyncha insect vectors in a citrus agroecosystem, (3) study the seasonal fluctuation of Auchenorrhyncha populations in olive orchards, and (4) compare the effectiveness of the two sampling methods used.

2. Materials and Methods

2.1. Study Site

Samplings were conducted in five organic olive groves from November 2017 to November 2019, covering a wide range of altitudes in the Chania prefecture of Crete, a representative olive production region of Southern Greece (Table 1, Figure 1). All the olive groves consist of olive trees of the ‘Koroneiki’ cultivar, which is the most commonly cultivated cultivar in Greece used for olive oil production. All groves comply with organic standards according to EU legislation (Council Regulation (EC) 834/2007). During the study period, standard cultivating techniques (mechanical weeding, pruning, irrigation) were performed. Insecticide sprayings were applied only against Bactrocera oleae (Rossi) using plant protection products that are permitted in organic farming. The most common weeds found on the herbaceous cover of these olive orchards were Avena sterilis L., Hordeum vulgare L., Daucus carota L., Oxalis pes-caprae L., Sonchus oleraceus L., Cynodon dactylon (L.), Crepis vesicaria L., and Glebionis segetum L. In one olive grove (site 2), there were perennial bushes such as Lavandula sp., Rosmarinus officinalis L., and Cistus spp. Weed species identification was based on dichotomous keys [43,44,45].
Additionally, one organic citrus grove located in Chania prefecture near the city was sampled from July 2017 to February 2019 (Table 1, Figure 1). During the study period, standard cultivating techniques were performed (weeding, pruning, irrigation), and insecticides were not applied. The lower vegetation consisted mainly of grasses such as Avena sativa L.

2.2. Sampling of Insects

Auchenorrhyncha were collected by using two sampling methods, the Malaise trap and the entomological sweep net.

2.2.1. Malaise Trap

In all study areas, a white color Malaise trap was installed. This is a non-attractant trap that provides continuous sampling, and its success is based on the behavior of most flying insects when hitting an obstacle to fly and/or crawl upwards, where they are captured within a plastic bottle [46]. The dimensions of the Malaise trap were 176 cm in height at the top end, 110 cm in height at the lower end, 165 cm in length, and 115 cm in width, with a 165- by 110-cm interception area [41,47]. On the upper part of the traps, a plastic bottle (600 mL) filled with approximately 200–300 mL of 70% ethyl alcohol was placed to preserve the collected specimens. The samples from the plastic bottle were collected fortnightly during the first year and monthly during the second year.

2.2.2. Sweep Net

In all olive groves, adults of Auchenorrhyncha were collected fortnightly the first year and monthly in the second year using an entomological sweep net. This is the most widely used method for sampling spittlebugs and other Auchenorrhyncha [21,30,36,48]. Following the EFSA protocol [49], for every olive grove, on each sampling date 120 sweeps were performed at the herbaceous cover, 10 sweeps at the periphery of the olive tree canopy of 20 randomly selected trees, and 10 sweeps to bushes and/or trees at the field margins. Auchenorrhyncha captured by the sweep net were collected using an entomological aspirator and preserved in labelled plastic tubes with ethyl alcohol 95%. In total, 39 samplings were carried out during the 2-yr survey period.

2.3. Auchenorrhyncha Identification

All captured insects, collected using both methods, were placed in plastic tubes containing 95% ethyl alcohol and immediately transferred to the Laboratory of Entomology of the Institute of Olive trees, Subtropical plants and Viticulture at Chania in Crete, Greece, for identification. All collected adults of Auchenorrhyncha were identified to the family and subfamily levels. Spittlebug species, along with some abundant and significant leafhoppers, were identified to the genus or species level. The taxonomic classification of the captured Auchenorrhyncha was based on the dichotomous keys of Nickel [50], Ribaut [51,52], Ossiannilsson [53,54,55], Biederman and Niedringhaus [56], Gnezdilov et al. [57], Holzinger et al. [58], Le Quesne and Payne [59], and Anufriev et al. [60]. For identification to species level, male genitalia were dissected and kept in KOH (10%) for 24 h, except for Typhlocybinae, which were kept for 2 h. Then, each was mounted on glass slides with a cavity, in glycerol, and observed under a stereoscopical microscope (KONUS CRYSTAL-45, Konus Optical and Sport Systems, Settimo di Pescantina, Verona, Italy). Some specimens were also examined under a phase contrast microscope (Leica DRMB, Leica Microsystems GmbH, Wetzlar, Hesse, Germany) for validation purposes.

2.4. Data Analysis

The Auchenorrhyncha specimens were categorized using the criteria of dominance [41,61,62,63]. ‘Dominance’ is calculated as the percentage of individuals of a given taxon compared with the total number of individuals of all taxa found. Hence, a given taxon is classified as ‘dominant’, ‘influent’, or ‘recedent’ if it constitutes >10, 5–10, or <5% of the total number of individuals, respectively.
The relative importance (RI) of a species was calculated for each sampling method and cultivation type. RI considers not only the species abundance but also its occurrence or frequency. Thus, species that are poorly represented in terms of individual numbers but frequently recovered over a long period can be balanced with abundant species with sporadic occurrence [64,65]. The RI of each species was determined using the formula:
RI = (ni/nt) × (mi/mt) × 100,
where ni = number of individuals of species “i”, nt = number of individuals of all species, mi = number of samples containing species “i”, and mt = total number of samples. A “very frequent” species is defined as having a RI equal to or higher than 1%, the RI of “frequent” species lies between 0.02% and 0.99%, and “rare or occasional” species have a RI equal to or lower than 0.019% [64,66].
Data on the collected insects from different field plots and olive grove habitats were analyzed using Student T-test to identify significant differences in the abundance of different insect families and species between the two sampling methods used between lowland and highland olive groves. To compare the effect of sampling site (i.e., herbaceous cover floor, olive tree canopy, and field margins), a one-way analysis of variance (ANOVA) was used, and means were compared using Tukey–Kramer HSD at a significance level of 0.05. Data from counts of the collected insects were compared between sampling site (i.e., herbaceous cover floor, olive tree canopy, and field margins) and insect family using a two-way ANOVA. Prior to analysis, log(x + 1) data transformation was used, and normality (Q-Q plot) and heteroscedasticity (Levene’s test) were tested for meeting the criteria for parametric analysis. Analyses were conducted using the Statistical Analysis System JMP 7.0 [67].

3. Results

3.1. Identification and Abundance of Insects

During the sampling period, 7215 insects belonging to eight families (Aphrophoridae, Cicadellidae, Cicadidae, Cixiidae, Delphacidae, Dictyopharidae, Issidae, and Tettigometridae) of Auchenorrhyncha were collected from all groves (olive and citrus). Cicadellidae and Issidae were the most abundant families (Table S1).
A total of 2817 Auchenorrhyncha adults, belonging to 8 families, were collected using a sweep net from the olive tree canopy, herbaceous cover, and field margins of all olive groves. Within the Cicadellidae family, eight subfamilies were identified: Agalliinae, Aphrodinae, Deltocephalinae, Dorycephalinae, Idiocerinae, Macropsinae, Megophthalminae, and Typhlocybinae. Among these, Deltocephalinae (1626) was the most abundant followed by Typhlocybinae (259) (Table S1). A total of 3895 Auchenorrhyncha adults, belonging to 7 families, were collected with Malaise traps from all olive groves. Within the Cicadellidae family, 8 subfamilies were collected with Typhlocybinae (1545) being the most abundant followed by Deltocephalinae (1487) (Table S1). The Aphrophoridae P. spumarius, N. campestris, and N. lineatus and Cicadidae species were the only xylem sap-feeding species collected from the olive groves with sweep net and Malaise trap during the 2-yr survey (Table S1).
A total of 503 Auchenorrhyncha adults, belonging to 5 families, were collected using a Malaise trap from a citrus grove. Cicadellidae was the most abundant family followed by Delphacidae. Within the Cicadellidae, five subfamilies (Agalliinae, Aphrodinae, Deltocephalinae, Idiocerinae, and Typhlocybinae) were identified, with Typhlocybinae being the most abundant followed by Deltocephalinae. The only xylem sap-feeding Auchenorrhyncha species collected from the citrus grove during the sampling period was N. lineatus.
Dominance ranking in olive groves sampled with sweep nets showed two dominant (B. incisa, E. lineolatus) and one influent (P. spumarius) species (Table S1). Species displaying less than 5% of dominance were classified as recedent. Concerning relative importance (RI), Deltocephalinae species B. incisa was revealed as being very frequent, B. rosea, E. lineolatus, and S. lauri were classed as frequent, while E. variegatus and E. ohausi were classed as infrequent. Concerning the Aphrophoridae family, P. spumarius was revealed as being frequent while N. campestis and N. lineatus were revealed as infrequent. When sampling with Malaise traps, all species of the family Aphrophoridae, as well as the Deltocephalinae species B. incisa, S. lauri, E. variegatus, and E. lineolatus were recorded as recedent, whereas E. ohausi and B. rosea were revealed as dominant and influent, respectively. As regards RI, all species of the subfamily Deltocephalinae, except E. variegatus, which was infrequent, as well as the Aphrophoridae P. spumarius were recorded as frequent, while N. campestris and N. lineatus were regarded as infrequent. In the citrus orchard, dominance ranking revealed only one species (E. ohausi) as influent while the remaining species of the subfamily Deltocephalinae, as well as the only captured Aphrophoridae (N. lineatus), were classified as recedent. As regards RI, all collected Aphrophoridae species, as well as the Deltocephalinae species E. variegatus and S. lauri, were found to be infrequent while B. incisa, B. rosea, E. lineolatus, and E. ohausi were regarded as frequent.

3.2. Sampling Methods

Figure 2 shows the abundance of each Auchenorrhyncha family sampled with the two different methods (sweep net and Malaise trap). Cicadellidae was the most abundant family, followed by Issidae and Aphrophoridae, in both sampling methods. Aphrophoridae abundance was significantly higher in sweep net (78%) compared to Malaise trap (22%) (t = 3.39, d.f. = 76; p = 0.001), while no differences occurred in other families (Figure 2a). Moreover, within the Aphrophoridae family, the abundance of P. spumarius adults was significantly higher in sweep net than in Malaise trap (t = −2.75; d.f. = 76; p = 0.007) while no difference occurred for N. campestris and N. lineatus (Figure 2b). Regarding Deltocephalinae species, significantly higher abundance was recorded in sweep net than in Malaise trap for the species B. incisa (t = 2.75; d.f. = 76; p = 0.007) and E. lineolatus (t = 1.82; d.f. = 76; p = 0.035). In contrast, the abundance of E. ohausi was significantly higher in Malaise trap (t = −3.85; d.f. = 76; p = 0.0002) (Figure 2c).

3.3. Auchenorrhyncha Abundance and Altitude

Figure 3 shows the mean number of collected adults per family sampled with sweep net during a two-year survey in lowland and highland olive groves. Over the survey period, the number of Cicadellidae adults collected was significantly higher in low-altitude (lowland) than in high-altitude (highland) olive groves (t = 2.44; d.f. = 76; p = 0.016). However, the number of collected Aphrophoridae (t = −3.24; d.f. = 72; p = 0.001) and Issidae (t = −2.11; d.f. = 76; p = 0.037) adults was significantly higher in highland olive groves (Figure 3a). Likewise, the number of P. spumarius adults was significantly higher in highland olive groves (t = 3.17; d.f. = 76; p = 0.002) (Figure 3b).
The number of Aphrophoridae adults was higher in highland than in lowland olive groves in both sampling years (year1: t = −2.15; d.f. = 50; p = 0.036, year2: t = −2.61; d.f. = 24; p = 0.015), while Issidae adults were significantly higher in highland olive groves only during the first year (t = −1.89; d.f. = 50; p = 0.063). In contrast, the number of Cicadellidae adults was significantly higher in lowland olive groves, only during the first year of sampling (t = 2.54; d.f. = 50; p = 0.014) (Figure 3c,d).

3.4. Habitat Preference

The number of collected Auchenorrhyncha was significantly influenced by the different habitats of the olive grove (herbaceous cover, field margins, olive tree canopy) (F = 12.25; d.f. = 2, 14; p = 0.0013) (Figure 4), but not from the different olive groves (F = 0.59; d.f. = 4, 14; p = 0.67). Significant differences were recorded among the different families (F = 39.12; d.f. = 7; p < 0.0001). The interaction between habitats and families was also significant, showing that the different habitats differently influenced the abundance of the different families sampled (F = 12.63; d.f. = 14; p < 0.0001). The number of collected Auchenorrhyncha from five olive groves during a one-year period was significantly higher in herbaceous cover than in the field margins and the olive tree canopy (Figure 4).
In the olive tree canopy, we recorded five families, with Issidae and Cicadellidae having significantly higher numbers of adults compare to Cicadidae, Aphrophoridae, and Delphacidae (F = 51.87; d.f. = 7, 39; p < 0.0001) (Figure 5). Synophropsis lauri (36%) and Issidae species (56%) were the dominant species on the olive tree canopy, while Aphrophoridae species such as P. spumarius (0.9%) and N. campestris (0.45%) were collected in low numbers. P. spumarius adults were mostly found on the herbaceous cover throughout the sampling period and only a few individuals (2) were recorded on the olive tree canopy. On the herbaceous cover, we recorded six families and the number of collected adults differed among families (F = 25.39; d.f. = 7, 39; p < 0.0001). Cicadellidae was the most abundant family followed by Aphrophoridae, Issidae, Delphacidae, Cixiidae, and Tettigometridae. On the field margins, we recorded five families and the number of collected adults differed among families (F = 51.87; d.f. = 7, 39; p < 0.0001). Cicadellidae was the most abundant family, followed by Issidae, Aphrophoridae, Delphacidae, and Cixiidae.

3.5. Seasonal Fluctuation

Figure 6 shows the seasonal abundance and fluctuation of adult Auchenorrhyncha in the five olive groves. Auchenorrhyncha were present throughout the two-year sampling period. The highest number was sampled in November 2017 (N = 442) with Malaise traps and in October 2018 with sweep net (N = 534) while the lowest was sampled in March 2019 with both Malaise (N = 6) and sweep net (N = 5). In both sampling methods, higher numbers of Auchenorrhyncha were recorded during Spring (April–June) and Autumn (September–November). A higher abundance of Auchenorrhyncha was recorded in 2018 compared to the corresponding months in 2019, primarily due to unusually high levels of rainfall in January and February of 2019 (Figure 7).
Regarding the Aphrophoridae family, individuals were present during two periods each year, one from April to May and another from October to December, as recorded by both sampling methods (Figure 8). Likewise, the adults of P. spumarius were collected mainly in April-May 2018 and lower populations were recorded during October-December in both years. The presence of its population was more evident with sweep net. During summer months from June to September, P. spumarius disappeared from the olive groves (Figure 8) apart from July, when only one (1) individual was collected.
Additionally, from January to March, the number of individuals collected was very low. Neophilaenus campestris adults appeared in April-May and October-December in very low numbers, whereas N. lineatus appeared only in November-December in very low numbers (Figure 8).
Euscelis lineolatus was recorded in high populations in all experimental groves covering a wide range of altitudes (10 to 300 m). Its presence was recorded during the cool period of the year (mid-November to early April) with a population peak in December and January, while it was absent from May to September (Table S2). In contrast, Euscelis ohausi and E. variegatus were found mainly during early summer (May–June) and autumn (September–October), with their populations decreasing during July and August. Moreover, Balclutha spp. were frequently found in olive and citrus groves especially during fall (October–November) on the ground vegetation and especially in lowland areas. Furthermore, several Issidae species were collected throughout the experimental period. Their presence was recorded almost all year round, with one population peak in May and June and another in October and November.

4. Discussion

The results of our two-year systematic study revealed a rich diversity of Auchenorrhyncha (eight families) captured with two different sampling methods, sweep net and Malaise traps. The most abundant family was Cicadellidae, consisting of eight subfamilies. However, no sharpshooters of the subfamily Cicadellinae were found in our samplings, similar to other relevant studies in Greece [41,42,68] and in other Mediterranean regions [69,70]. In all groves, the Deltocephalinae and Typhlocybinae subfamilies of the Cicadellidae family were the most abundant.
Among the potential insect vectors of X. fastidiosa [11], only three species of the Aphrophoridae family were recorded throughout the 2-yr systematic survey in all groves, but at very low numbers (4.45%); these were P. spumarius, N. campestris, and N. lineatus. Although cicadas are abundant in Crete as in other parts of the Mediterranean [71], in our survey, they were recorded in low numbers because the sampling methods used were not suitable. Morente et al. [70] also reported the ineffectiveness of sweep netting to capture a representative number of cicadas. However, the role of cicadas in the epidemiology of X. fastidiosa in Europe is likely negligible [18]. Within the Aphrophoridae family, P. spumarius was recorded to be the most abundant species in olive groves, as previously found by Tsagkarakis et al. [41] and Antonatos et al. [42,72]. However, N. lineatus was not detected in previous studies in Chania [41,42,68,72]. According to predicting models, the climatic conditions of Western Greece are favorable for P. spumarius [73] and the pathogen [24]. However, over the 2-yr study, the population of spittlebugs was low and P. spumarius accounted for 7.8% and 1.5% of the total Auchenorrhyncha captured by sweep netting and Malaise traps, respectively. This is in contrast with findings from the outbreak region (Apulia) of Southern Italy, where P. spumarius was the most abundant species in olive orchards (39.8% of the total Auchenorrhyncha captured) [69]. The optimal temperature for development and reproduction of P. spumarius is 15.6 °C [74]; taken together, it seems that the northern and cooler Mediterranean regions are more suitable for its development. This may represent a geographic limitation potentially attributed to climatic conditions, similar to the case of Trioza erytreae Del Guercio (Hemiptera: Triozidae), an insect-vector of Huanglongbing, the most serious citrus disease worldwide [75]. In our study, the highest populations of P. spumarius were observed in periods with ambient mean temperatures between 15 and 20 °C. During the 2-yr study, P. spumarius nymphs were observed with visual inspection of host-plant species, exhibiting the characteristic foam they produce. In the study area, nymphs appeared once every year from the end of February until early May when they molted to the adult stage. However, we did not capture any nymphs with the sampling methods used. Similar to the Apulian olive groves [76], the preference of nymphs for Asteraceae plants such as Crepis sp. and Sonchus sp. is also evident in olive and citrus groves in Crete. Furthermore, P. spumarius was the most abundant xylem feeder found in Corsica (France) on Cistus monspeliensis [31] and in Alicante (Spain), where it plays a key role in the spread of X. fastidiosa in almond orchards [70]. Likewise, P. spumarius was found in much higher frequency and numbers than Neophilaenus campestris and N. lineatus in olive groves of Chania, which is in accordance with earlier studies in Greece [41,68] and Italy [69,76]. Conversely, N. campestris was found to be widespread in Spain and northeastern Portugal and could possibly be involved in the transmission of X. fastidiosa to hosts other than olive, as well as in the maintenance of inoculum sources in herbaceous hosts [70]. Concerning the citrus grove, the only potential insect vector captured was the Aphrophorid species N. lineatus (two adults in November 2017); however, further research needs to be conducted to clearly understand the species composition in citrus groves. Thanou et al. [77] also found a low number of xylem-feeders in citrus groves. No individuals from the Cercopidae family were found in either olive or citrus groves over the 2-yr study. Moreover, it seems that there is a geographical variation in the composition of xylem-sap feeding species in olive orchards in Greece. Important xylem-feeders such as P. signatus, Lepyronia coleoptera, and Cercopis sanguinolepta previously recorded in Central Greece [42] were not found in our study, complementing the findings of Tsagkarakis et al. [41]. Hence, the situation in Crete appears different from what has been observed elsewhere in Greece or in the other areas of Europe (Italy), and this low population density of spittlebugs in olive and citrus environment may not allow the fast spread of X. fastidiosa in case the pathogen is introduced in Crete.
Two sampling methods, sweep net and Malaise trap, were assessed for capturing Auchenorrhyncha, including potential insect vectors of X. fastidiosa, in five olive groves in two consecutive years. In this study, a wide range of Auchenorrhyncha and especially highly mobile insects such as Cicadellidae species (Deltocephalinae and Typhlocybinae) were successfully collected with Malaise traps. However, the use of Malaise traps seems to be of limited value for estimating the spittlebugs’ population densities since these insects are less active and thus their abundance can be underestimated. Moreover, Malaise traps cannot be used to estimate the abundance of insects on different habitats such as the tree canopy and field margins in the olive and citrus environment. On the other hand, sweep netting is a widely used sampling method for many insects, including Auchenorrhyncha. The sampling of Aphrophoridae species resulted in 3.6-fold more individuals captured by sweep netting compared to Malaise traps. However, it is not a continuous sampling system and requires frequent visits to the experimental field as well as intense manual work. Both methods seem appropriate for sampling leafhoppers (Cicadellidae) as many individuals were collected in both sampling methods. The abundance of some Auchenorrhyncha species was found to be dependent on the sampling method and this suggests that both systems should be used simultaneously to have a better understanding of the population dynamics of Auchenorrhyncha species. This is in accordance with Purcell et al. [78], who proposed that a combination of sampling methods would provide more accurate estimations of abundance and movement of insects, which is important for understanding the role of potential insect vectors in disease spread.
Our results demonstrate altitudinal variations in important Auchenorrhyncha species in Crete. The numbers of Aphrophoridae species, such as P. spumarius, were significantly higher in highland (180–300 m alt.) compared to lowland (10–30 m alt.) olive groves, confirming existing literature on its dispersal ability [79,80]. Specifically, Santoiemma et al. [80] found an increase in occurrence probability of P. spumarius in high elevation sites and suggest that high elevation landscapes dominated by olive groves are more likely to host populations of P. spumarius and are therefore higher risk for emergence of X. fastidiosa epidemics. Thus, while P. spumarius can tolerate a wide variety of climatic conditions [27], olive groves at higher elevations may provide a more favorable environment for population growth due to cooler temperatures [74]. Conversely, Cicadellidae species exhibited population decline from lower to higher altitudes, aligning with Le Cesne et al. [81], who reported a decrease in the number of individuals captured by Malaise traps with increasing altitude.
Systematic sweep net samplings revealed a higher number of Auchenorrhyncha in the herbaceous cover compared to the field margins and the tree canopy of olive groves. This is probably due to the feeding and oviposition preference of Auchenorrhyncha to host plants on the herbaceous cover. On the olive tree canopy, Issidae and Deltocephalinae species, especially S. lauri, were the most abundant. However, they have been documented as minor pests of olive in Greece [82].
Aphrophoridae species, especially P. spumarius, were found mainly on the herbaceous cover, feeding from Poaceae, Asteraceae, and Fabaceae plants. In Corsica, P. spumarius is almost exclusively collected from Cistus monspeliensis (Malvales: Cistaceae), with only a few specimens collected in grasses and clover [31]. In contrast, in our study, its presence on the Cistus creticum was not confirmed. Aphrophoridae species were also captured in the olive tree canopy and the field margins but in low numbers. However, in other countries such as Italy and Spain, P. spumarius was found in high numbers on both herbaceous cover and in the olive tree canopy [69,70]. Perhaps the high-water stress of olives and the desiccation of the herbaceous cover due to drought could explain the extremely low collection of spittlebug adults during late spring and their total absence during summer in the olive orchards in Chania [83]. The low presence of P. spumarius on the olive tree canopy could indicate a lower probability of pathogen dispersal in case of accidental introduction in the study area.
Regarding seasonal fluctuation, Auchenorrhyncha showed population increases in fall (November and December) and spring (April and May) in both years with both sampling methods, possibly due to the favorable weather conditions for their development and the presence of several host plants on the herbaceous cover. Overall populations were lower in 2019 than in 2018, probably due to the unusually high rainfall in the study area in January and February of 2019, a rare phenomenon that could occur more often in the future due to the climate change. Similarly, Aphrophoridae and particularly P. spumarius populations were recorded twice a year, once in spring (April and May) when the newly emerged adults appear and once in fall (November and December) when females oviposit eggs on several plants of the herbaceous cover. It seems that the peak of P. spumarius adults in Crete occurs one month earlier than in Apulia, where they appear in May [38,83], probably due to the different climatic conditions. During summer months and especially from mid-June to September, P. spumarius adults were absent from the olive orchards. This is in accordance with other studies from Greece [41] and in contrast with Ben Moussa et al. [69], who found high populations of P. spumarius during summer months in Apulian olive groves. This is an indication that P. spumarius migrate during summer from olive groves to oversummering hosts and reappear in October until the end of December, as happens in Spain, Corsica, and Portugal [70].
The leafhopper Euscelis lineolatus was the most abundant species during winter in Apulian olive groves, which was detected positive to X. fastidiosa [69]. In our study, E. lineolatus was also recorded in high populations in all experimental groves during the cool period of the year (mid-November to early April) and in a wide range of altitudes (10 to 300 m). Other frequent Deltocephalinae species were Euscelis ohausi and E. variegatus, found mainly during early summer (May–June) and autumn (September–October) with their populations decreasing during July and August, probably due to high temperatures. Moreover, Balclutha spp. were most present during fall (October–November) on the ground vegetation and especially in lowland areas.

5. Conclusions

The results of the two-year systematic survey indicate a rich diversity of Auchenorrhyncha in western Crete, including potential insect vectors of X. fastidiosa. The presence of three (3) potential insect vectors of X. fastidiosa (P. spumarius, N. campestris, N. lineatus) was confirmed, while Cercopidae and Cicadellinae species (sharpshooters) were absent in the study areas during the extended duration of our research. The low presence of P. spumarius on the olive tree canopy as well as the herbaceous cover could indicate a lower probability of pathogen dispersal in the case of an accidental introduction in the area. Moreover, our results suggest that although Malaise trapping constitutes a useful tool for monitoring insects of the Cicadellidae family, ideally this method should be combined with sweep nets to obtain a holistic approach and more representative samples from Aphrophoridae species as well. This is the first extensive and systematic study to investigate the insect species composition, abundance, habitat preference, and seasonal fluctuation of Auchenorrhyncha in Cretan agroecosystems, providing valuable insights for designing effective integrated pest management strategies.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/agronomy14102243/s1; Table S1: Total number, dominance and frequency of adult Auchenorrhyncha collected by sweep net and malaise trap from five olive groves during a 24-mo survey (November 2017–November 2019) and by malaise trap from a citrus grove during a 19-mo survey (July 2017 to February 2019). N, number of individuals captured; D, dominance (r, recedent; i, influent; d, dominant); RI, relative importance (if, infrequent; fr, frequent; vf, very frequent); Table S2: Mean number of Auchenorrhyncha adults per species per sampling in five olive groves during a 2-yr survey with sweep net.

Author Contributions

Conceptualization, I.E.K., A.P.K., M.L.P. and G.D.B.; methodology, I.E.K., A.P.K., M.L.P. and G.D.B.; validation, I.E.K., A.P.K.; A.E.T., M.L.P. and G.D.B.; formal analysis, I.E.K. and G.D.B.; investigation, I.E.K.; resources, I.E.K., A.P.K. and D.K.T.; data curation, I.E.K. and G.D.B.; writing—original draft preparation, I.E.K. and G.D.B.; writing—review and editing, I.E.K., A.P.K., D.K.T., A.E.T., M.L.P. and G.D.B.; visualization, I.E.K. and G.D.B.; supervision, A.P.K., M.L.P. and G.D.B.; project administration, I.E.K., A.P.K. and G.D.B.; funding acquisition, I.E.K., M.L.P. and G.D.B. All authors have read and agreed to the published version of the manuscript.

Funding

The research work was supported by the Hellenic Foundation for Research and Innovation (HFRI) and the General Secretariat for Research and Technology (GSRT), under the HFRI PhD Fellowship grant (GA. no. 770).

Data Availability Statement

The raw data supporting the conclusions of this article will be made available by the authors on request.

Acknowledgments

We would like to express our sincere gratitude and appreciation to the Institute of Olive tree, Subtropical plants and Viticulture of the Hellenic Agricultural Organization (ELGO-DIMITRA) and the local farmers for granting us the opportunity to conduct our experimental research within their laboratories and orchards, respectively. We are sincerely grateful for their generosity and cooperation throughout the duration of this study.

Conflicts of Interest

The authors declare no conflicts of interest.

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Figure 1. Geographical locations of olive and citrus groves surveyed for the presence of Auchenorrhyncha during the 2017–2019 period in the Chania region in Greece. The five olive groves sampled with sweep net and Malaise trap are marked as follows: square (site1), triangle (site 2), circle (site 3), cross (site 4), and X (site 5). The citrus grove sampled with just a Malaise trap is marked with an asterisk (site 6).
Figure 1. Geographical locations of olive and citrus groves surveyed for the presence of Auchenorrhyncha during the 2017–2019 period in the Chania region in Greece. The five olive groves sampled with sweep net and Malaise trap are marked as follows: square (site1), triangle (site 2), circle (site 3), cross (site 4), and X (site 5). The citrus grove sampled with just a Malaise trap is marked with an asterisk (site 6).
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Figure 2. Average relative abundance (±SE) of adults (a) per family, (b) Aphrophoridae species, and (c) Deltocephalinae species sampled by each of the two methods (sweep net and Malaise trap) in five olive orchards over a period of 2 years. * Significant differences in average relative abundance between sampling methods (a) per family, (b) Aphrophoridae species, and (c) Deltocephalinae species (Student’s t-test: p < 0.05).
Figure 2. Average relative abundance (±SE) of adults (a) per family, (b) Aphrophoridae species, and (c) Deltocephalinae species sampled by each of the two methods (sweep net and Malaise trap) in five olive orchards over a period of 2 years. * Significant differences in average relative abundance between sampling methods (a) per family, (b) Aphrophoridae species, and (c) Deltocephalinae species (Student’s t-test: p < 0.05).
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Figure 3. Mean (±SE) number of adults (a,c,d) per family and (b) Aphrophoridae species captured with sweep net in two lowland (10–30 m alt.) and two highland (180–300 m alt.) olive groves. * Significant differences in the total number of adults per family or species between lowland and highland olive groves (Student’s t-test: p < 0.05). (Values are the total number of adults captured in two lowland and two highland olive groves per sampling).
Figure 3. Mean (±SE) number of adults (a,c,d) per family and (b) Aphrophoridae species captured with sweep net in two lowland (10–30 m alt.) and two highland (180–300 m alt.) olive groves. * Significant differences in the total number of adults per family or species between lowland and highland olive groves (Student’s t-test: p < 0.05). (Values are the total number of adults captured in two lowland and two highland olive groves per sampling).
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Figure 4. Mean (±SE) number of adult insects collected from the herbaceous cover, field margins, and the olive tree canopy of five olive groves with sweep net over a period of 1 year. Different letters indicate significant differences according to Tukey–Kramer HSD (ANOVA: p < 0.05). (Values are the total number of adults captured in the three habitats of the five olive groves).
Figure 4. Mean (±SE) number of adult insects collected from the herbaceous cover, field margins, and the olive tree canopy of five olive groves with sweep net over a period of 1 year. Different letters indicate significant differences according to Tukey–Kramer HSD (ANOVA: p < 0.05). (Values are the total number of adults captured in the three habitats of the five olive groves).
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Figure 5. Mean (±SE) number of adult insects collected from (a) the herbaceous cover, (b) field margins, and (c) the olive tree canopy of five olive groves with sweep net over a period of 1 year. Different letters above the bar within the same habitat indicate significant differences according to Tukey–Kramer HSD (ANOVA: p < 0.05). (Values are the total number of adults captured in the three habitats of the five olive groves).
Figure 5. Mean (±SE) number of adult insects collected from (a) the herbaceous cover, (b) field margins, and (c) the olive tree canopy of five olive groves with sweep net over a period of 1 year. Different letters above the bar within the same habitat indicate significant differences according to Tukey–Kramer HSD (ANOVA: p < 0.05). (Values are the total number of adults captured in the three habitats of the five olive groves).
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Figure 6. Seasonal fluctuation (from November 2017 to November 2019) of all Auchenorrhyncha adults in five olive groves. Y-axes: mean (±SE) number of collected Auchenorrhyncha per month.
Figure 6. Seasonal fluctuation (from November 2017 to November 2019) of all Auchenorrhyncha adults in five olive groves. Y-axes: mean (±SE) number of collected Auchenorrhyncha per month.
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Figure 7. Climatic data of the study area from November 2017 to November 2019, retrieved from the weather station of Kolympari.
Figure 7. Climatic data of the study area from November 2017 to November 2019, retrieved from the weather station of Kolympari.
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Figure 8. Seasonal fluctuations (from November 2017 to November 2019) of spittlebug adults in five olive groves. Y-axes: mean (±SE) number of collected spittlebugs per month.
Figure 8. Seasonal fluctuations (from November 2017 to November 2019) of spittlebug adults in five olive groves. Y-axes: mean (±SE) number of collected spittlebugs per month.
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Table 1. Location and characteristics of olive and citrus groves sampled with Malaise trap (MT) and sweep net (SN) in the Chania prefecture of Crete, Greece.
Table 1. Location and characteristics of olive and citrus groves sampled with Malaise trap (MT) and sweep net (SN) in the Chania prefecture of Crete, Greece.
AreaLocationCoordinatesAlt. *CropSampling MethodField Margins Vegetation
Site 1Chania35°29′12.8″ N 24°01′28.0″ E10Olea europea ‘Koroneiki’MT, SN Citrus, Avocado, Grasses
Site 2Zounaki35°28′54.3″ N 23°49′48.4″ E100Olea europea ‘Koroneiki’MT, SNPistacia lentiscus, Erica sp., Cistus spp., Ilex sp.
Site 3Zymbragou35°26′27.1″ N 23°45′25.0″ E300Olea europea ‘Koroneiki’MT, SNArbutus sp., olive trees, Juglans sp.
Site 4Kasteli35°29′31.7″ N 23°38′42.0″ E30Olea europea ‘Koroneiki’MT, SNVitex sp., Olive trees
Site 5Lousakies35°28′34.3″ N 23°38′02.7″ E180Olea europea ‘Koroneiki’MT, SNPistacia lentiscus, grasses, herbal plants
Site 6Chania35°29′31.9″ N 24°03′00.1″ E10Citrus spp.MTGrasses, Anthemis spp.
* Alt.: Altitude in meters (m).
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Koufakis, I.E.; Kalaitzaki, A.P.; Pappas, M.L.; Tsagkarakis, A.E.; Tzobanoglou, D.K.; Broufas, G.D. Population Dynamics of Potential Insect Vectors of Xylella fastidiosa (Xanthomanadales: Xanthomonadaceae) and Other Auchenorrhyncha in Olive and Citrus Groves of Crete, Greece. Agronomy 2024, 14, 2243. https://doi.org/10.3390/agronomy14102243

AMA Style

Koufakis IE, Kalaitzaki AP, Pappas ML, Tsagkarakis AE, Tzobanoglou DK, Broufas GD. Population Dynamics of Potential Insect Vectors of Xylella fastidiosa (Xanthomanadales: Xanthomonadaceae) and Other Auchenorrhyncha in Olive and Citrus Groves of Crete, Greece. Agronomy. 2024; 14(10):2243. https://doi.org/10.3390/agronomy14102243

Chicago/Turabian Style

Koufakis, Ioannis E., Argyro P. Kalaitzaki, Maria L. Pappas, Antonios E. Tsagkarakis, Despina K. Tzobanoglou, and George D. Broufas. 2024. "Population Dynamics of Potential Insect Vectors of Xylella fastidiosa (Xanthomanadales: Xanthomonadaceae) and Other Auchenorrhyncha in Olive and Citrus Groves of Crete, Greece" Agronomy 14, no. 10: 2243. https://doi.org/10.3390/agronomy14102243

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