Pest Management Science Pest Manag Sci 64:720–724 (2008)

Crop losses due to olive mothmediated by ethylenePedro Ramos, Raquel Rosales, Ibrahim Sabouni, Dolores Garrido∗ andJose M RamosDepartment of Plant Physiology, University of Granada, Fuentenueva s/n, 18071 Granada, Spain

Abstract

BACKGROUND: Studies for nine years in southern Spain on the olive moth, Prays oleae Bern., have testedthe possibility of altering oviposition behaviour on newly formed olive fruits by means of a single ethyleneapplication.

RESULTS: A single spraying of ethylene on the olive trees at the beginning of fruiting significantly decreased theolive moth egg populations and consequent the olive fruit fall. At the same time, no negative effect was found inthe activity of natural oophagous predators of the olive moth.

CONCLUSIONS: The ethylene treatments against P. oleae yielded substantial economical benefits each year (amean of ¤526 ha−1), benefits that fluctuated depending on the olive crop and on the annual fruit fall caused by thismajor pest. 2008 Society of Chemical Industry

Keywords: natural compounds; ethylene; ethephon; olive moth; crop yield; Olea europaea; Prays oleae; fruit fall;oophagous predators

1 INTRODUCTIONThe olive moth (Prays oleae Bern.) is, economically,one of the most important pests of olive treesin the Mediterranean basin. The main damageusually appears during fruiting, when moth larvaepenetrating the fruits cause the fall of immatureolives, provoking serious economic losses, which inthe province of Granada (southern Spain) can reach¤77 million annually.1 During fruit set, Prays femaleslay a variable number of eggs on immature olivefruits, but the number of eggs can subsequently bereduced by predation by Chrysopides.2–4 Previouswork has demonstrated that female oviposition canbe influenced by spraying the trees with an ethylenereleaser5 without affecting oophagous predators. Theamount of eggs laid on a fruit is a parameterthat can be altered by several factors, one ofprime importance being the degree of synchronybetween adult emergence and the fruit ‘suitability’ foroviposition by egg-laying females.6,7 For the degree ofsynchrony, which can vary greatly from year to year,8

a very good indicator is the number of days betweenthe first adult emergence (measured as captures insex pheromone traps) and the starting of oviposition,i.e. the period of time without oviposition on fruits.9

In southern Spain, this period ranges from 1 to14 days, depending on the presence of adults andfruits simultaneously in the field. When this period islong (14 days), the infestation is found to be ‘light’

(less than 100 eggs per 100 fruits); when the periodlasts about 8–9 days, the attack will be ‘moderate’(100–300 eggs per 100 fruits); and finally, when1–2 days separates first emergence of adults and thefirst eggs, the attack will be ‘high’ (more than 300 eggsper 100 fruits).1 Preliminary results in southern Spainindicated that a treatment of the trees with the ethylenereleaser ethephon (2-chloroethylphosphonic acid) justbefore insect oviposition on fruits slightly increasedthe ethylene released naturally by the plant, and thisrelease was very effective in significantly reducing theegg population and crop losses.10,11 How ethyleneaffects the defence mechanism in olive trees is notentirely clear, although the authors have shown thatethylene does not affect either the Prays reproductivecycle or the tree phenology, but it can affect oviposition(female approach to the fruit for egg laying). Ethyleneis a natural plant-growth regulator clearly involvedin certain mechanisms of plant defence, and thehypothesis is that ethephon triggers a more complexdefence mechanism, involving ethylene and also someother hormones in the process.12 The present studycovers nine years of research in southern Spain on thepossibility of altering the oviposition behaviour of P.oleae females on recently formed olive fruits subjectedto a single ethephon application at physiological dosesat the beginning of fruiting.

∗ Correspondence to: Dolores Garrido, Department of Plant Physiology, University of Granada, Fuentenueva s/n, 18071 Granada, SpainE-mail: dgarrido@ugr.es(Received 28 May 2007; revised version received 3 September 2007; accepted 12 November 2007)Published online 18 February 2008; DOI: 10.1002/ps.1548

2008 Society of Chemical Industry. Pest Manag Sci 1526–498X/2008/$30.00

Ethylene reduces olive moth effects

2 METHODS AND MATERIALSField experiments were conducted for nine years(1986, 1987, 1988, 2001, 2002, 2003, 2004, 2005and 2006) in olive groves of the province of Granada(southern Spain). The olive trees (mainly of the varietyPicual) of about 50 years of age, measuring no morethan 3 m high and planted on 10 m centres, were grownunder rain-fed conditions without pesticide treatmentsfor at least 20 years. The climate of the zone is typicalMediterranean, with cold, wet winters and hot, drysummers (presenting mean annual values over thelast 35 years of 22 ◦C maximum and 9 ◦C minimum),with roughly 50% relative humidity and 460 mmof annual rainfall. For the treatments, ethephon480 g L−1 SL (Ethrel-48; Bayer CropScience) wasused at a concentration of 1.2 mL L−1 13 and appliedat an overall spray volume of 100 L ha−1 (57.6 gethephon ha−1) at the start of fruit formation. Ten olivetrees were sprayed each year, leaving ten other treesas controls. Each year, fruit sampling was conductedfrom the date of treatment (early June to the end ofJuly, i.e. 45–50 days, until 100% of the viable motheggs had hatched). Ten treated and control trees weresampled at random, collecting a minimum of 100fruits from different heights and orientations of eacholive tree. Over the nine-year study period, more than18 000 olive fruits were examined, and the overallnumber of moth eggs was approximately 28 000. Bybinocular microscopy, the three types of pest egg weredifferentiated:14 (1) live eggs, milky white in colour,translucent, taking on a yellowish tone afterwards;(2) hatched eggs, reddish-black in colour, with a holewhere the newborn larva burrowed into the fruit,visible under the chorion; (3) depredated (empty)eggs, of which only the chorion remains, stronglyattached to the fruit surface, taking the form of athin, transparent film with a characteristic reticulation.With this basic information, several parameters werecalculated, including: the egg population (POP),i.e. the total number of eggs laid per 100 fruits;the potential infestation (PI), i.e. the percentage offruits with eggs in any state; the predator activity(PrA), i.e. the percentage of empty eggs from thetotal number of eggs examined; the final infestationor fruit fall (FI), i.e. the percentage of fruits withhatched eggs. The theoretical yield (TY) (kg ha−1)of the olives was calculated from the real yield(RY) (kg ha−1) and from the final infestation asRY = TY − (TY × FI/100). The real yield was takenfrom data of the Annals of Agrarian Statistics of theSpanish Ministry of Agriculture, Fish and Food.15 Theeconomic costs were estimated according to marketprices for 2005/2006: ¤0.65 (kg olives); ¤0.91 (subsidykg−1); ¤60 (1 L Ethrel-48) and ¤200 (labour ha−1).

3 RESULTS AND DISCUSSIONOver the study period, P. oleae oviposition lasted anaverage of 40 days, normally starting in late May andending towards mid-July. The mean values of this

oviposition period for the nine years studied can bedivided into five phases: phase I, from egg layingto onset of hatching (7 days); phase II, from 1 to25% of eggs hatched (12 days); phase III, from 25to 50% of eggs hatched (5 days); phase IV, from50 to 75% of eggs hatched (5 days); and, finally,phase V, from 75 to 100% of eggs hatched (11 days).Egg population (POP) provided a good estimate ofthe relative density of moth eggs in the olive fruits.Figure 1 shows the evolution of egg population (meanvalues of the nine years studied) in ethephon-treatedand control olive trees. From the beginning of phaseIII (19 days after ethephon treatment), the mothegg population underwent a statistically significantdecrease in ethephon-treated trees by comparison withcontrol trees (41%), and this tendency was maintainedin the rest of the phases until the end of egg hatching(44%).

Figure 2 shows the mean annual values of thetreated and control egg populations when the numberof eggs stabilized (i.e. during phase V). In all thestudy years, the egg populations significantly decreasedwhen the trees were treated with ethylene, especiallyduring the years 2003 and 2006, with more than 60%reduction. The percentage of potential infestation (PI)is a parameter that usually correlates well with the eggpopulation, and some authors16,17 recommend theuse of one of these two parameters (POP or PI) whenestimating P. oleae activity on the fruit, even when bothparameters are calculated in a different way. In thiswork, the correlations between the two parametersover the nine years (r = 0.85; P = 0.05) confirmedprevious results.

Figure 3, presenting the evolution of the potentialattack from the beginning of oviposition, indicatesthat, along with POP, the potential infestation (PI)significantly declined in the treated trees compared

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Figure 1. Differences in evolution of Prays oleae egg population(POP) in olives treated with ethylene and in control trees. The resultsare the mean values for the nine years used in this study. Valueswithin each phase with different letters differ significantly at theP = 0.05 level using the least significant difference test.

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Figure 2. Mean values of egg population (POP) of Prays oleae inolives treated with ethylene at the fruit set and in controls for each ofthe nine years studied, and the total. Values within each year withdifferent letters differ significantly at the P = 0.05 level using the leastsignificant difference test.

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Figure 3. Evolution of the potential infestation (PI) of Prays oleae inolives treated with ethylene compared with control trees. The resultsare the mean values for the nine years used in this study. Valueswithin each phase with different letters differ significantly at theP = 0.05 level using the least significant difference test.

with the control, from the beginning of phase III tothe end of the oviposition.

Figure 4 represents the mean annual values whenPI stabilized; these values show statistical decreases inPI of treated olives in all the nine years studied.

In the literature, most biocontrol methods involvenatural predators of the genus Trichogramma. Thus,indigenous strains of Trichogramma sp. have beenproposed for the biological control of lepidopterouspests of olive trees.18 However, in southern Spain,chrysopides are the main natural enemies of P. oleae,and the predatory activity of these insects in someyears is high enough substantially to reduce the finalinfestation of the pest.3,4 In the present study, Fig. 5

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Figure 4. Mean values of potential infestation (PI) of Prays oleae inolives treated with ethylene at the fruit set and controls for each of thenine years studied, and the total. Values within each year withdifferent letters differ significantly at the P = 0.05 level using the leastsignificant difference test.

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Figure 5. Mean predatory activity (PA) evolution of Prays oleae inolives treated with ethylene in comparison with control trees of thenine years of study.

shows that the evolution curves for the predatoractivity (PrA) due to chrysopide larvae in treated andcontrol trees are almost identical. When the meanvalues for the nine years are compared (Fig. 6), nodetectable differences are discernible between controland treated trees; that is, the ethephon treatment didnot affect the activity of these oophagous predators ofP. oleae. Ethylene is a natural compound released byplants, and in the dosage used it is not toxic either toplants or to the olive entomofauna.19

Final infestation (FI) is a parameter that reliablymeasures the phytophagous attack on the olive fruits,and, in an indirect way, the damage caused to thefruits. From an economic standpoint, FI was the most

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Figure 6. Mean values of the predator activity (PA) on Prays oleae incontrol and ethylene-treated trees. The results are shown for eachyear individually and for the total.

important parameter studied, since it estimates thepercentage of olive fruit fall due to Prays attack.Different studies in the province of Granada haveshown that the final attack strongly correlates withother parameters: directly with the population, directlywith potential attack and inversely with oophagouspredation.16,17 With this information, a series ofmultiple regressions can be established to predict thedamage that the pest can cause to the olive fruits, andthereby assess the necessity of treatment with ethyleneor any other natural product that induces defence inplants. The evolution of the final attack is shown inFig. 7. Statistical differences were detected in treatedand control trees from the beginning of phase III tophase V, the greatest difference being observed inphase V (33%).

When each year was studied individually (Fig. 8), itwas estimated that, in the nine study years, ethephonprovoked significantly reduced fruit fall as comparedwith controls. In addition, the correlation study hasshown that the years with a higher fruit loss due to olivemoth were the years in which the ethephon treatmentshowed a higher effectiveness in reducing this fruit fall(rPi control−Pi ethephon = 0.91; P = 0.05).

Figure 9 shows the annual comparisons for realharvest (kg ha−1) in the control trees and the calculatedharvest (kg ha−1) for the ethylene-treated trees. In allyears the crops associated with the ethylene treatmentswere higher than the control crops, these differencesbeing statistically significant, except for 1986.

Figure 10 presents the economic yield (¤ ha−1) forthe treated olive trees. The only year with economicallosses was 1986, with ¤85 ha−1, while the other yearsregistered economic profits, especially during 2001and 2003, with a surplus of more than ¤1500 ha−1,and with a mean value for the nine years of ¤526 ha−1.

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Figure 7. Differences in the final infestation (FI), or fruit fall evolution,of Prays oleae in ethylene-treated olives and in controls. The resultsshow the mean values for the nine years studied. Values in eachphase with different letters differ significantly at the P = 0.05 levelusing the least significant difference test.

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Figure 8. Mean values of final infestation or fruit fall of Prays oleae inolives treated with ethylene at the fruit set and controls. The resultsare shown for each year individually and for the total. Values withineach year with different letters differ significantly at the P = 0.05 levelusing the least significant difference test.

The importance of these economic profits varied,depending on the yield and the decrease of fruitfall due to ethephon treatments, as reflected by themagnitude of the correlation coefficient, establishedwhen introducing these three variables in a multiplecorrelation (r = 0.98; P = 0.05). The results for allthe nine years indicate that a single treatment withethephon sprayed on olive trees at the beginningof fruit set can significantly decrease the moth eggpopulation and thus the fruit fall caused by Prays. At

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Figure 9. Crop yield (kg ha−1) in control and ethylene-treated olivetrees. The results are shown for each of the nine years analysed andfor the total. Values within each year with different letters differsignificantly at the P = 0.05 level using Student’s t-test.

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Figure 10. Economical yield (¤ ha−1) for olive trees treated withethylene at the fruit set through the nine years used in this study, andthe mean of the nine years (total).

the same time, no negative effect was observed in theactivity of natural oophagous predators of P. oleae. Inconclusion, the ethephon treatments against P. oleae atthe beginning of fruit formation resulted in importanteconomical profits each year (a mean of ¤526 ha−1),benefits that fluctuated depending on the olive cropand on the annual fruit fall caused by olive moth.

ACKNOWLEDGEMENTSThe authors thank CICYT for the Project AGL200-1552-CO2-01, and Ministerio de Educacion y Cienciay Plan Propio (University of Granada) for supportingthe research of RR. They also thank Consejerıa de

la Presidencia, Junta de Andalucıa, for the ProjectAM35/04.

REFERENCES1 Ramos P, Campos M and Ramos JM, Long-term study on the

evaluation of yield and economic losses caused by Prays oleaeBern. in the olive crop of Granada (southern Spain). Crop Prot17:645–647 (1988).

2 Alrouechdy K, Les Chrysopides en verger d’olivier. Bio-ecologiede Chrysoperla carnea Steph. (Neur. Chrysopidae), relationscomportementales et trophiques avec certaines especesphytophages. These Doct. Ing., Univ. Paris, 198 pp. (1980).

3 Ramos P and Ramos JM, Veinte anos de observaciones sobre ladepredacion oofaga en Prays oleae Bern. Granada (Espana),1970–1989. Bol San Veg Plagas 16:119–127 (1990).

4 Varela JL and Gonzalez R, Estudio sobre la entomofauna deun olivar de la provincia de Granada, durante el periodo devuelo de la generacion antofaga de Prays oleae Bern. (Lep.Yponomeutidae). Phytoma Espana 111:15–20 (1999).

5 Rosales R, Garrido D, Ramos P and Ramos JM, Ethylene canreduce Prays oleae attack in olive trees. Crop Prot 25:140–143(2006).

6 Niccoli A and Boni F, Osservazioni sulla distribuzione delleuova di Prays oleae Bern. sui frutti e sull’incidenza dei fattoridi mortalita. Redia 67:515–525 (1984).

7 Ramos P, Campos M and Ramos JM, Evolucion del ataque dePrays oleae Bern. al fruto del olivo. I. Estudio de parametros ysus relaciones. Bol San Veg Plagas 13:129–142 (1987).

8 Ramos P, Ramos JM and Jones OT, The influence of asyn-chrony between olive moth (Prays oleae Bern.) adult emer-gence and olive fruit phenology in determining subsequentfruit infestation. Acta Hort 286:391–394 (1990).

9 Pralavorio R and Arambourg Y, Etudes de quelques particu-larites du developpement larvaire et des facteurs de reductionde la generation carpophage de Prays oleae Bern. CEE ReunionGroupe Experts, Antibes, France, pp. 227–240 (1981).

10 Ramos P and Ramos JM, Preliminary results on the actionof a plant growth regulator (Ethrel) in reducing the attackof Prays oleae Bern. on olive fruits. Experientia 45:773–774(1989).

11 Rosales R, Garrido D, Ramos P and Ramos JM, Ethylene canreduce Prays oleae attack in olive trees. Crop Prot 25:140–143(2006).

12 Rojo E, Solano R and Sanchez-Serrano JJ, Interactions betweensignalling compounds involved in plant defense. J PlantGrowth Regul 22:82–98 (2003).

13 Warner HL and Leopold AC, Ethylene evolution from 2-chloroethylphosphonic acid. Plant Physiol 44:156–158(1969).

14 Arambourg Y, Contribution a l’etude de Prays oleaellus F. enTunisie, cycle biologique et essais de lutte en 1957. Ann ServBot et Agr Tunisie 30:47–52 (1961).

15 Ministerio de Agricultura, Pesca y Alimentacion, Encuestasobre superficies y rendimientos de los cultivos. Boletin MensualEstadıstica Agraria. MAPA, Madrid, Spain (2007).

16 Ramos P, Campos M and Ramos JM, Evolucion del ataque dePrays oleae Bern. al fruto del olivo. I. Estudio de parametros ysus relaciones. Bol San Veg Plagas 13:129–142 (1987).

17 Ramos P, Campos M and Ramos JM, Evolucion del ataquede Prays oleae Bern. al fruto del olivo. III. Distribuciony agregacion de puestas. Bol San Veg Plagas 14:343–355(1988).

18 Herz A and Hassan S, Are indigenous strains of Trichogrammasp. (Hym., Trichogrammatidae) better candidates for biolog-ical control of lepidopterous pests of the olive tree? Biocon SciTechnol 16:841–857 (2006).

19 Sabouni I, Estudios agronomicos sobre el uso de la fitohormonaetileno como alternativa natural a los insecticidas contrala polilla del olivo (Prays oleae Bern.) Tesis Doctorales,Universidad de Granada, Granada, Spain (2005).

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