Olive Growing Farming System and Damage by Cicadas

Abstract

Although cicadas have traditionally been considered pests of little or no importance, in recent decades, an increase in damages is being recorded in olive groves of southern Spain. New agricultural practices that affect soil management are behind it. During 2024, intensive sampling has been carried out in an organic grove with herbaceous cover (VC2), and in a second one with mixed vegetation cover (VC1, in which the crushed remains of the annual pruning are added). In both ecological groves, inventories of the vegetation have been carried out, as well as intensive sampling in the olive canopy, with the densities of oviposition injuries being recorded and compared with respect to conventional management (CONV). The objectives of this study are to compare the three managements based on the density of oviposition injuries, to determine the priority areas for cicadas’ oviposition within the trees; and to develop a sampling method to assess damage over large areas. The results show significant increases in the density of injuries in organic groves, with maximum values recorded in the olive grove with mixed cover. Oviposition injuries show an altitudinal gradient distribution, with maximum values in the lower zone of the trees. The factors involved are discussed.

1. Introduction

Cicadas are mostly tropical or subtropical insects, but many species also inhabit temperate regions. Some are minor pests of various crops, such as sugarcane, rice, coffee, fruit trees, either affecting the vitality of the trees and their normal radial incremental growth [1] by nymphal feeding or damaging twig branches during oviposition. Crops are lost when the females snap at weakened points, which can break and fall under the load of the crop, or because of strong winds [2,3,4,5]. In the Mediterranean region, Cicada barbara (Stål) and C. orni L., are two closely species that are morphologically very similar, with the exception of a few differences affecting the wing spotting pattern [6,7] and the genitalia of males [8]. They also show calling songs that are distinct [5,6,7,8]; the temporal configuration of Cicada barbara song is characterized by an uninterrupted pulse, while Cicada orni song shows a clear discontinuous pattern [9]. Both species are found mainly in open woodlands [10]. Only C. barbara is found in both North Africa and the Iberian Peninsula, while C. orni is distributed throughout southwestern, central and eastern Europe, western Asia, and the Middle East [11,12]. According to Boulard (1982) [5], the populations of C. barbara in the Iberian Peninsula would correspond to C. barbara lusitanica Boulard, different from the type subspecies, only found in North Africa (C. barbara barbara Stål) which would explain a possible African origin of this species [5], an hypothesis that could not be excluded [13]). These species affect a wide range of hosts [10,13,14,15,16] and show a relatively high overlap range [6]. In the olive groves, cicadas are frequent in crops in France, northwest Africa [5,6], Italy [17], Portugal [6], Greece, Tunisia [18], and Spain [19], in any case, having been classified as pests of localized importance and punctual or intermittent appearance [20]. In Spain, the most closely related to the olive tree is C. barbara, which has been called the olive cicada [21]. Although cicadas have traditionally been considered pests of little or no importance in olive groves, since the end of the 2000–2010 decade, an increase in the populations of cycads is being recorded in the olive groves of Andalusia (southern Spain), as well as in the severity of the injuries they caused [22,23]. Both adults and nymphs feed on xylem sap, and until recently have been considered potential vectors of Quick Decline Syndrome disease, caused by Xylella fastidiosa; however, their role in the natural spread of this bacterium has been considered as null or insignificant [24]. Until now, studies on C. barbara in Spanish olive groves come from crops in conventional farming, in which the nymphs have only the roots of the olive trees to feed on. Indeed, there is little or no evidence that belowground feeding by cicadas on the roots of their host plants could have a negative effect on plant performance [25]. However, (Yang, 2004) [26] indicates that although, in general, the feeding of the younger nymphs is of little consideration, the nymphs in their final stage are much more voracious, and seriously affect the growth of the plants. Adults suck the olive sap from the main and secondary branches with smooth bark, although no assessment has been made of possible damages at this stage [22]. Despite the above, the real damage to woody plants comes from the wounds caused by female cicadas when they slice branches to insert eggs [27]. These symptoms have been increasing in the southern Spanish olive groves and are of particular concern in nurseries and young plantations [22,23]. Control of C. barbara is rather complex, mainly based on nocturnal application of pyrethroid insecticides during the oviposition period (July and August) which has been relatively effective in conventional farming [23]. From laying, the eggs remain dormant until the autumn rainy period, which usually occurs in October and November [22].

The increase in cicada populations may be closely related to the implementation of new agricultural practices in soil management, which would be triggering substantial changes or influence in the development of juvenile stages. The main objective of these practices was to prevent soil erosion by implementing an herbaceous ground cover that forms a low grass prairie—which grows spontaneously or by artificial planting [28,29,30] and is maintained by mower control. Among its advantages, the greater plant biodiversity contributes to keeping phytophagous insects under natural control [31]; however, among its detractors, many farmers highlight plant cover’s most controversial facets, such as how it competes with crops for water and nutrients, which is especially intense during water-scarce periods (from mid-spring to early autumn, depending on the bioclimatic belt—Thermomediterranean or Mesomediterranean. To mitigate this effect, in most cases the herbaceous cover is periodically mowed mechanically, and the resulting residue is added in situ, forming a layer that prevents excessive evapotranspiration during the summer and protects the soil from erosion. In line with the above, the effect provided by the herbaceous vegetation cover is enhanced by the addition of the remains from the olive grove pruning -previously crushed- into the adventitious vegetation (mixed vegetal cover). These remains are composed of fine branches (usually less than 5 cm in diameter) and leaves [32], which represent an important source of nutrients [33], increasing nitrogen mineralization [34] and positively influencing the soil’s biological, chemical, and physical properties [35], resulting in a highly beneficial agricultural practice [36,37,38,39,40]. Among other advantages, it provides a longer protective effect against erosion [32,33] compared to that provided by a single herbaceous cover [29], preventing the appearance in the crop area of ruderal plant species [36], and enhancing the production of adventitious flora. Cicada nymphs have soil habituates where they are exclusively xylem suckers [1,41,42,43,44], as they directly extract their food from the roots of the plants that develop in the crop area, and accordingly, Carpio et al. (2020) [43] point out that vegetation cover in olive groves determines the highest abundance of Cicadomorpha. Although these authors do not refer exclusively to the Cicadidae, it follows that there is a need to attain a broader knowledge of the role played by cover crops that incorporate lowland prairie, as well as those close to patches of natural vegetation, borders, hedges, or streams.

Intensive sampling of the olive tree canopy has been used in three types of crops: conventional farming, organic farming (a single herbaceous cover forming a low grass prairie) and organic farming, with a mixed cover, to address the objectives of this study. The objectives were the following: (1) to characterize and quantify the density of oviposition injuries under these different farming systems; (2) to determine priority areas for oviposition by cicadas within olive trees; (3) to provide a basis for developing an extensive sampling method, acceptable in terms of effort–yield and reliability that allows acceptable estimates in larger areas.

2. Materials and Methods

2.1. Description of the Study Area

This study was carried out in olive groves in the province of Jaén (Andalusia, southern Spain) during the spring of 2022 and 2023. The specific area belongs to the olive groves located in a farm in the municipality of Mancha Real (Jaén, Andalusia, Spain) (Figure 1). Most of the olive trees are between 80 and 100 years old and belong to the “picual” variety, cultivated under irrigation and planted in a frame of 10 m × 10 m. In this olive grove, there are two large areas (Figure 1) characterized by different types of agricultural farming.

2.1.1. Olive Groves with Ecological Farming

These olive groves have a surface area of 238 ha, with the coordinates 37°52′12.55″ N, 3°34′03.33″ W, and altitude of approximately 500 m a.s.l. These olive groves receive edaphic fertilization through the application, twice a year, of organic and mineral nutrients. In addition, annual foliar fertilization is applied using crystalline urea (nitrogen content 46%), potassium sulfate, and natural amino acids (arginine, glycine, threonine, and proline). The pruning of olives is carried out sector by sector at the end of winter, with all the olive trees being pruned over three or four years. In this olive grove, two relatively large sub-areas were differentiated (Figure 1) depending on the fate of the pruning residues: (i) VC1, with an extension of 163 ha, in which the finer pruning remains (terminal shoots and leaves) are incorporated into the soil and spread along the central band of the interlines; (ii) (VC2) this olive grove has a surface area of 75 ha.

In both ecological olive groves, the development of a spontaneous and homogeneous vegetable cover is promoted in a controlled way at the end of spring, and to avoid overaccumulation of plant debris and reduce the fire risk, a pass is carried out using a tractor equipped with a paddle brush cutter. Its function is to crush the dry remains of the plant cover into very small fragments of a few millimeters, which are scattered on the olive grove’s surface. This results in a protective vegetable layer composed of small elements, the compaction of which makes a considerable reduction in its thickness possible. Regarding pest and disease control, no synthetic chemical products are applied in the organic olive apart from pheromones in combination with specific devices (McPhail, delta, and chromotropic traps). The adventitious vegetation is mechanically controlled by clearing between March and April using a hammer tractor. The resulting plant remains are crushed and spread along the inter lines.

2.1.2. Olive Grove with Conventional Farming

This olive grove has a surface area of 150 ha (CONV, Figure 1), this crop completely lacks herbaceous cover as well as any other plant species other than Olea europea. The soil fertilization is performed by applying organic and mineral nutrients twice a year; additionally, foliar fertilization is carried out annually with crystalline urea (46% nitrogen content), potassium sulfate, and natural amino acids (arginine, glycine, threonine, and proline). For the control of weeds and seeds, intense tillage is carried out by plowing and using the herbicide glyphosate (Roundup UltraPlus© 500 mL, Monsanto, St. Louis, MO, USA). For pest control, the most widely used insecticide is Spinetoram-25% (Spintor^® 480SC, Dow AgroSciences, Indianapolis, IN, USA) for controlling the olive moth (Prays oleae) and the olive fly, Bactrocera oleae (Rossi, 1790) (Diptera: Tephritidae). To control the branch borer, Euzophera pinguis (Haworth, 1811) (Lepidoptera: Pyralidae), Chlorpyrifos© 48% (IRAC Group 1B) is applied. For pathogen control, a fungicide application containing Agrofit^® (Agroterra; Valencia, Spain) is created as a wettable powder formulation that is 50% copper for use against the olive peacock spot (Spilocaea oleagina = Cycloconium oleaginum).

2.2. Sampling on the Vegetation Cover (VC1; VC2)

Five sessions of sequential sampling at weekly intervals (April–May 2022) were carried out on the herbaceous communities of the central blocks of both ecological groves. In each sampling, an olive tree was chosen at random in each olive grove. Using a flexometer, a 5 m long transect was established, extending in an east–west direction at a distance approximately 3 m from the trunk of the selected trees. To facilitate the data collection, the transect was divided into 5 cm segments, with a total of 100 sampling points per transect. For each segment, the number of contacts of each plant taxa with the flexometer was recorded, and the total number of contact was also recorded. The samples were determined using specific keys to the Flora vascular de Andalucía Oriental [45], and the description of biotypes by Raunkier (1934) [46].

2.3. Sampling in Olive Tree Canopy (VC1; VC2; CONV)

To determine the density of oviposition injuries within trees, samplings were carried out at monthly intervals (March–May 2023). For this purpose, in each sampling date, an olive tree was randomly selected from each of the three blocks (a, b, c, Figure 1) of each olive farm (VC1, VC2, CONV). Prior to sampling, three altitudinal zones (low, medium and high) were considered in the trees, each corresponding to one-third of the total height of the crown. Similarly, at each altitudinal level, four sectors were established corresponding to the four cardinal orientations: north (N), east (E), south (S) and west (W). For data collection, at each of the altitudinal level and cardinal sector, 20 twig branches (10 terminal twig branches and 10 subterminal twig branches) were randomly selected. The total number of samples in each olive tree and sampling date was 240 (40 in each of the cardinal orientation; of which 20 were terminal and 20 were subterminal twig branches), which represents a total number of 720 samples per sampling date, and a total number of 2160 samples as a whole.

During the data collection, a segment of 30 cm length was established in every terminal/subterminal branch, where the whole number of injuries due to the oviposition by cicadas was counted, noting its length (cm), as well as its position in the axis of the shoot. Therefore, it was specified if the injury affected the upper, lower or lateral sides, in which case a distinction was made between right or left, taking into account the acropetal direction. Since different injuries frequently coalesce, in these the total length of the injury was noted. Damage often involved branch breakage, a symptom also attributable to the olive bark beetle, Phloeotribus scarabaeoides [47,48]. Due to the impossibility of accurately attributing them to cicada injury, twigs with these symptoms have been discarded in this study, meaning that cicada damage has been slightly underestimated. When old oviposition injuries by cicadas have not involved branch fracture, the lesions may heal completely, with the scar remaining still clearly visible in subterminal twig branches up until 4–5 years from its origin.

2.4. Statistical Analysis

For the statistical analysis, the IBM SPSS Statistics 27 program was used. Initially, the normality of the data distributions was determined, for which the Shapiro–Wilk and Kolmogorov–Smirnov contrast test was used with the correction by Liliefors. To determine the homogeneity of the variables, Levene’s test was applied. In order to obtain parametric distributions, the Arctangent transformation has been applied. Once the normal distribution of the data was assumed, analysis of variance (ANOVA) has been applied to determine the existence of statistically significant differences, and in cases in which differences have been verified, the contrast test has been applied by applying the minimum significant differences test (LSD). To compare abundance values of the different plant species present in both ecological olive groves, the Student’s t test was applied.

To determine the minimum sample size, for each of the three altitudinal zones, the percentage error of an increasing number of samples in each altitudinal zone has been determined. Simple linear regression analysis has been applied to relate the accumulated number of damages in the different altitudinal zones and the increase in sampling size.

3. Results

3.1. Study of Herbaceous Cover (ECO-VC1 & ECO-VC2)

Vegetation sampling showed 20 herbaceous species in the organic olive groves (

Table 1. List of plant species inventoried in VC1 and VC2 olive groves, indicating biotypes, life form, no. of specimens collected (N), and abundance (%). By dark green (VC1) and light green (VC2), and the vegetative growth of plant development (months) for each species. The p values indicate statistically significant differences in abundance (t-Student test).

	(Biotype) 1					Months
Sp	[Life Form] 2	N	%VC1	%VC2	p	I	II	III	IV	V	VI	VII	VIII	IX	X	XI	XII
Filago	(Th.) [e.]	606	15.2	84.8	<0.001
pyramidata L.
Malva	(H./Th.) [fasc.]	410	65.8	34.2	<0.05
parviflora L.
Bromus	(Th.) [caesp.]	300	75.3	24.7	>0.05
rubens L.
Astragalus	(Th.) [e. fasc.]	149	95.3	4.7	<0.01
hamosus L.
Trisetaria	(Th.) [caesp.]	104	50	50	>0.05
panicea (Lam.)
Filago	(Th.) [e.]	103	89.3	10.7	<0.001
fuscescens Pomel
Herniaria	(Th.) [creep.]	91	80.2	19.8	>0.05
cinerea D. C.
Crucianella	(Th.) [e.]	47	0	100	>0.05
patula L.
Diplotaxis	(Th.) [e.]	35	0	100	<0.01
virgata (Cav.) DC.
Hordeum murinum	(Th.) [e.]	34	85.3	14.7	>0.05
leporinum Arcang.
Trigonella	(Th.) [e.]	26	23.1	76.9	<0.01
monspeliaca L.
Phalaris	(Th.) [caesp.]	23	47.8	52.2	>0.05
minor Retz.
Heliotropium	(H.) [ros.]	23	55.4	44.6	>0.05
europaeum L.
Plantago	(H./Th.) [ros.]	22	100	0	>0.05
lagopus L.
Erodium	(Th.) [creep.]	20	0	100	>0.05
malacoides (L.) L’Hér.
Ononis	(Th.) [e.]	19	15.0	85.0	>0.05
biflora Desf.
Melilotus	(Th.) [e.]	11	18.2	81.8	>0.05
elegans Salzm. ex Ser.
Leontodon longirostris	(H.) [ros.]	10	0	100	>0.05
(F. & P. D. Sell) Talav.
Stellaria	(Th.) [e.]	1	100	0	>0.05
pallida (Dumort.) Piré
Anagallis	(Th.) [e.]	1	100	0	>0.05
foemina Mill.

¹ Biotypes: Terophyte (Th.); Hemicryptophyte [H]. ² Life forms: caespitose [caesp.]; erect [e]; fasciculate [fasc.]; rosulate [ros.]; creeping [creep.].

), among which 13 species were common to both, while 4 and 3 species were found exclusively in olive groves VC1 and VC2, respectively. Among the common species, seven of them stood out from the rest due to their greater abundance (Table 1), in particular terophytes such as Filago pyramidata, Bromus rubens, Astragalus hamosus, Trisetaria panicea, Filago fuscescens, Herniaria cinerea, and the hemicryptophyte Malva parviflora. Most of these start their vegetative growth of plant development during the winter and were significantly abundant in olive grove VC1 (Table 1). With the exception of Filago fuscescens, which has a short vegetative growth of plant development, most of the taxa end in June–July (14 spp.), four species still remain in August, and four spp. have a second vegetative growth in autumn [39].

3.2. Description of Oviposition Injuries by Cicadas

Oviposition injuries consist of incisions that cicadas carry out with their ovipositor apparatus, which causes a deep cortical crack that affects the bark and mainly the phloem, where the eggs are deposited in paired cells. The subsequent detachment and drying of the affected tissue with respect to the xylem causes a marked retraction of the margins on both sides of the incision. These injuries cause the tips of many terminal branches to wither and die, as well as that the fruits present on them. Dead and dying terminals droop, resulting in a type of tree injury called “flagging”. Some of these break off and fall to the ground, and when they do not break off they may eventually heal and scar, so the noticeable symptoms in the wound sites of the subterminal branches correspond to an irregular and knotty swelling [27]. The average mean values of the oviposition injuries in terminal twig branches were of 6.21 cm (SD = 3.38); 5.84 cm (SD = 4.12 and 6.8 cm (SD = 3.54) for the olive trees in each of the three blocks of the VC1 olive grove (Figure 2). The diameters of the terminal twig branches affected by oviposition injuries, ranged from 1.5 mm to 5.5 mm, although the greatest proportion of lesions ranged were noted in twig branches from 2 to 4 mm (Figure 2), with average values of 3.32 mm, 2.87 mm and 3.12 mm, respectively, for the olive trees in the blocks of olive grove VC1. (Figure 2). The injuries most frequently (48.4% to 56.6%) (Figure 3) affected the facing downwards side, and the lowest frequency (7.8% to 10.2%) corresponded to the upper side of the branch, oriented upwards.

Regarding the subterminal twig branches, no recent injuries were recorded, as these were older than 3 years (at the time of sampling they frequently showed an advanced degree of healing).

3.3. Influence of the Olive Farming System on the Density of Oviposition Injuries

The comparison of the density of injuries between the three types of growing farming system. Significant differences were noted in both the subterminal (ANOVA; F = 29.319; 2 d.f.; p < 0.001) and terminal branches (ANOVA; F = 101.187; 2 d.f.; p < 0.001). In both, the highest values were recorded in olive grove with mixed vegetation cover (VC1) (p < 0.05; Figure 4), in which almost 50% of the 40 cm of terminal twig branches showed oviposition injuries. On the other hand, conventional olive grove showed average values significantly lower in both terminal and subterminal twig branches (p < 0.05, Figure 4), with average values ranging from 30% to 50% of those observed in VC2, and 25% of those observed in the VC1 olive grove. In the VC2 olive grove, trees showed intermediate values, and significantly different from VC1 and conventional olive groves.

In the olive tree canopy, significant differences are found in the density of injuries between the different altitudinal zones (Figure 5). For the terminal branches, significant differences between areas were observed regardless of the type of farming [VC1: ANOVA; F = 22.744, 2 d.f.; p < 0.001]; [VC2: ANOVA; F = 11.382; 2 d.f.; p < 0.001] and [CONV: ANOVA; F = 5.245; 2 d.f.; p < 0.005]. The values reached maximum records in the lower zone, and particularly in olive groves VC1 and VC2, where the proportion of affected branches was greater than 50%. The values between the middle and upper zones in the VC2 and CONV groves were not statistically significant, although they were in the VC1 olive grove (Figure 5; p < 0.05). As in the terminal branches, in the subterminal ones the highest values were recorded in the lower zone, although they were statistically significant only in the VC1 olive farm.

Regarding the distribution of injuries among the cardinal sectors of the trees, in none of the three types of olive farming system or types of branch (subterminal or terminal) did the values show statistically significant differences.

Considering the terminal branches, since these are where the lesions correspond to the most recent attacks (occurred in the last 2–3 years), which have not been healed, nor are they in the process of healing, there is a close relationship between the total number of injuries and the size of the sample, independently of the altitudinal floor in the olive tree (Figure 6). In the three altitudinal levels, by means of a simple linear regression analysis, regression lines with coefficients close to 99% are obtained.

3.4. Determination of an Extensive Sampling for Cataloging Olive Groves Based on Injuries Density

As shown in Figure 7, the relationship between the % Error committed and sample size is practically identical at the three altitudinal levels. Obviously, the preference of cicadas for the lower area of the olive tree implies that higher estimates of injuries density would be obtained here. From this, the possibility arises of considering only samples in the lower area of the crown, from which the maximum attack values will be obtained, or distributing the samples homogeneously at different heights, in order to obtain a more realistic average of the average attack density per tree (

Table 2. Variation of the % Error in the estimates of the mean number of the values of injuries/30 cm segment of terminal twig branch, with increasing sampling size, in the three altitudinal levels of the trees (lower, middle, and upper part (olive grove VC1).

N	Lower	Middle	Upper	N	Lower	Middle	Upper
1	-	-	-	21	7.86	7.33	7.33
2	28.00	33.33	33.33	22	7.64	8.16	8.16
3	27.50	25.00	20.00	23	7.52	8.03	8.44
4	20.00	20.00	19.25	24	7.37	7.90	8.28
5	16.67	16.67	17.50	25	7.21	7.77	8.12
6	14.29	14.29	15.81	26	7.06	7.51	7.97
7	12.50	12.50	14.14	27	6.91	7.40	7.82
8	13.09	13.09	12.60	28	6.80	7.59	7.59
9	12.03	12.50	11.29	29	6.67	7.36	7.36
10	11.11	11.75	11.11	30	6.55	7.15	7.15
11	10.32	11.07	10.83	31	6.45	7.05	6.94
12	10.44	10.66	10.05	32	6.34	6.95	6.75
13	9.88	10.14	9.35	33	6.23	6.77	6.56
14	9.37	9.61	8.73	34	6.13	6.69	6.50
15	8.91	9.09	8.18	35	6.03	6.52	6.33
16	8.94	8.61	8.20	36	5.96	6.45	6.17
17	8.58	8.49	8.16	37	5.87	6.30	6.01
18	8.25	8.08	7.75	38	5.78	6.23	5.86
19	8.22	7.71	7.37	39	5.69	6.10	5.72
20	8.09	7.36	7.36	40	5.64	6.21	5.58

).

However, since the injuries to the subterminal twig branches were at least three years old, and as said before, were in the process of healing at the time of sampling, it is recommended for assessment of damage by cicadas to focus exclusively on the terminal twig branches. On the other hand, although no differences between orientations exist, it is recommended to consider twig branches homogeneously from the entire periphery of the crown. As an example of extensive sampling for the estimation of the intensity of attack of C. barbara, the selection of at least four olive trees, considering four samples in each, one from each of the cardinal orientations, would allow estimates with a %Error within the tree lower than ±9% of the estimated average.

4. Discussion

The results show a clear preference of cicadas to lay eggs in the lower part of the canopy, as well as in the lower side of the terminal twig branches, protected from direct solar radiation, which is in line with what has been indicated in olive groves in southern Spain [22]. A tree canopy is a highly heterogeneous environment [49], so analyzing the preference of cicadas to place eggs in these microhabitats requires considering that during the oviposition period (July–August), the greatest risks to egg viability are determined by low environmental humidity (average values generally below 35%) and high temperatures, whose maximum records usually exceed 40 °C. Given the risk of dehydration as a determining factor, the selection of these microsites as the most favorable within the tree canopy represents an adaptation to minimize egg damaging by high temperatures [50]. Eggs are the most vulnerable stage, and are nearly isothermal with the microenvironments, so embryo temperature is determined by maternally chosen microhabitats, which are defined by interactions between ambient environmental characteristics (e.g., air temperature, solar radiation, wind speed) [51]. According to these authors, the energy budget of one microsite habitat differs from another depending on its position within the canopy, due to variations between them in radiation interception and wind attenuation due to the density of the foliage. Among the most remarkable feature of the eggs of temperate cicadas is the extremely long duration of the egg stage [52], which allows the eggs to face a sequence of environmental stresses over the course of the unfavorable seasons and hatch when more favorable conditions occur, such as the onset of the autumn rains [22]. Cicada nymphs are soil dwellers that feed exclusively on plant sap from root xylem vessels of their host plants stage [25,41,42], a food that is nutritionally diluted and difficult to obtain. Cicadas exhibit the longest development times and are among the largest insects [53,54,55], since this allows nymphs to store resources and produce more offspring [56]. During development, nymphs sometimes feed on a single root for their entire life span belowground [57]; however, no significant relationship has been found between cicada emergence for any species of cicada and percentage cover of individual plant species, suggesting that within a habitat type (grassland or forest), cicadas are generalist feeders [57]. The results of this study support this claim since no plant species other than the olive tree could provide food to the nymphs throughout their development [41]. However, the huge difference in damage density between the farming systems considered here highlights the role of low grass cover in the survival rate and production of cicadas. During the autumn rains [17], the neonate nymphs that colonize the soil of the olive groves must find host roots in which they form feeding cells, where the nutrient cells are established for a period not specified in the species studied [56]. It has been suggested that establishing new feeding sites is probably risky and costly for nymphs in terms of survival. To minimize these drawbacks, it has been postulated that nymphs can control the rate of feeding [1], and refrain from feeding at a rate that kills their host root, a common event in plants when they lose too many nutrients or water through their roots. due to parasitism by nematodes, fungi, or insect nymphs such as cicadas. [53]. However, when circumstances require it, the change in location allows the nymphs to continue feeding, either at another point on the root of the same plant, or on roots of other nearest plants. This movement from the initial feeding root takes place through access tunnels to their preferred root tissues over a succession of nymphal growth instars [20]. Since the development times of cicadas are influenced by the quality of food, it penalizes nymphs that fail to relocate to new feeding sites [56]. Our study shows that the change in location must be an essential event to nymphs, since the phenology of any potential host species in the olive grove would allow them to complete the development from a single specimen, not even a plant species other than the olive tree. Furthermore, the disappearance of herbaceous specimens from the crop area throughout the year, depending on their phenology, determines the need for the nymphs to change location. Among the crucial steps for nymphs’ survival is the summer drought period, when the residual herbaceous plants of the vegetation cover can exclusively survive in the under the canopy of the olive trees, where the soil is kept moist by the drip irrigation devices. This means that species, such as Heliotropium europaeum, Leontodon longirostris, Plantago lagopus, are available when most of the herbaceous plants have completed their vegetative development. These specimens represent a potential food source for 1 & 2 year old nymphs, and that still requires feeding for a period of at least one year more. This would explain the differences in the density of injuries between conventional olive groves, and organic olive groves, where the maximum values are recorded. Another crucial event for survival is during host searching by newly hatched larvae, which has been shown to occur mainly in October and November [19]. Then, after hatching, the larvae colonize the soil to find the suitable host roots. At this time, they have herbaceous species such as Trisetaria panicea, Bromus rubens, Heliotropum europaeum, Leontodon longirrostris, Anagallis foemina, which are relatively abundant in the peripheral area of the trees, where they can establish the first feeding cells. Later during the winter, the greatest diversity of herbaceous plants represents a greater availability of hosts to establish new feeding cells. Since the probability of reaching full development depends on the success in maintaining a feeding quality by cicada nymphs, this penalizes nymphs that fail to relocate to new feeding sites [56], which directly impacts the juvenile mortality rate; therefore, greater plant diversity and abundance ensures greater chances of survival, which is in line with the results, and explains the higher densities of injuries in olive trees of both organic groves.

Soil fertilization is an important factor, which has been highlighted as influencing the development rate of nymphs. In this regard, experiments have been carried out involving intraspecific comparisons in fertilized and unfertilized conditions. When Mogannia minuta grew on its native Miscanthus grass host, most individuals required 3 years to complete development, but when they grew on fertilized sugarcane, most individuals matured in 2 years [58]. The Japanese cicada, Cryptotympana facialis, presented a median development period of 8 years when raised on native plants in outdoor cages, but only 5 years when raised on fertilized potted aloe plants [56]. Therefore, the greater contribution of nutrients in olive groves receiving extra fertilization through the addition of crushed plant material provides favorable conditions, as manifested in this study in the largest herbaceous production (five of the seven most numerous inventoried plant species were statistically more abundant in the VC1 grove). This implies greater success in the reproduction of cicadas, and is directly related to the higher damages in the VC1 grove.

In short, although ecosystem services are provided to the farmer by the vegetation cover—whether simple or mixed [31,59,60,61,62,63,64,65,66], in a context of IPM approach, affected farmers should take necessary corrective measures, among which we point out some alternatives:

• Conventional chemical control, using products with a notable knockdown effect on adults during the reproductive period [67]. Obviously, this would not be a viable solution in organic crops, so for these, applications of kaolin-based formulation along with diatomaceous earth and essential oil have demonstrated acceptable control of oviposition injuries [68].
• Control of field infestations using exclusion nets, 1 cm mesh netting, which has proven to be the most effective strategy [67,69].
• Complementary cultural methods, based on the suppression during the summer of plant specimens that develop in the peripheral area of olive trees, close to irrigation drippers, which would have a very negative impact on the survival rate of nymphs.

5. Conclusions

As a result of this research, it has been possible to deepen the knowledge of the distribution, oviposition preference, and density of injuries in olive groves. Females lay eggs on the terminal twig branches, preferably on those with a diameter of between 2 and 4 mm, and more frequently in their lower zone. Likewise, regarding the distribution of oviposition injuries within the tree, these results show that females do not discriminate between different cardinal orientations, although they do show a clear preference for the lower zone of the tree, where density values are reached that are twice as high as in the upper zone.

Agronomic practices play a decisive role in the rate of oviposition injuries by C. barbara. These are highest in the olive grove where a mixed vegetation cover is promoted (herbaceous vegetation cover and the addition of crushed pruning remains) where the attack rate was 0.45 injuries/twig branch. Secondly, the maintenance of a simple vegetation cover (only spontaneous herbaceous plants) results in a lower average damage density, equivalent to 0.36 injuries/twig branch. Finally, the olive grove with conventional management (without herbaceous plants and without the addition of pruning remains) turns out to be the least affected, with an average rate of only 0.11 injuries/twig branch.

Regarding the setup of an extensive sampling method to obtain acceptable estimates of cicada damage in a given area, our results suggest to focus the sampling exclusively on the terminal twig branches, and in each tree select the twig branches homogeneously from the entire periphery of the crown. As an example, in each sampling point at least 4 olive trees would be selected, considering in each one 4 twig branches (1 from each cardinal orientation), which makes a minimum of 16 repetitions per sampling point, and allows estimates with a % Error within the tree lower than ±9% of the estimated average.