Effects of climatic changes on olive fly, Bactrocera oleae (Rossi) population dynamic and its damages in olive orchards in Iran

doi:10.21203/rs.3.rs-5010523/v1

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Effects of climatic changes on olive fly, Bactrocera oleae (Rossi) population dynamic and its damages in olive orchards in Iran

https://doi.org/10.21203/rs.3.rs-5010523/v1

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The olive fruit fly Bactrocera oleae Rossi (Dip.: Tephritidae) is one of the most economically damaging pests of olives worldwide. The present study was conducted in Qazvin Province (Ghooshchi and Siahpoosh), Iran, between 2014 and 2016 to investigate seasonal fluctuations and the population's bio-ecology characteristics of B. oleae using sex pheromone traps and McPhail traps. Fruit sampling was also carried out to reveal pest development and the fruit infestation rate. The results showed that adult insects are active throughout the year, and their density varies depending on the weather conditions. In the areas where the study was conducted, there are three to four overlapping pest generations per year. In late spring and early summer, the oviposition of female insects on the fruits coincides with the hardening of the olive pit. Immature stages of the pest were observed in late May at different dates, indicating the beginning of the first generation of olive fruit flies. The second generation starts from late August to late September, and the third generation begins in early October. The population density and economic damage of the pest varied over the three years, depending on temperature, relative humidity, and orchard management. Cyrtoptyx latipes parasitized pest larvae at a maximum percentage of 2.16, which was very low.

Olive fruit fly

Climate Changes

Population dynamics

Cyrtoptyx latipes

Control

The olive fruit fly, Bactrocera oleae Rossi (Dip: Tephritidae), is a highly economically important pest in olive groves worldwide (Mojdehi et al., 2022). B. oleae e is monophagous and multivoltine, causing damage to cultivate and wild olive varieties (Miranda et al., 2019). The olive fly causes severe yield losses and degrades the quality of olives and olive products, resulting in economic losses estimated at US$800 million per year (Sinno et al., 2020). B. oleae attribute the damage caused to olive fruit directly and indirectly to their larvae. Direct damage, adult females lay eggs under the exocarp. In about two to three days, the eggs hatch and the larvae begin to feed on the pulp, resulting in an untimely fruit drop and a decrease in oil yield (Grasso et al., 2017). Moreover, oviposition provides passage for a secondary infestation of bacteria and fungi that decay the fruit (Podgornik et al., 2013) and influence the quality of the olive oil created, resulting in the hydrolysis of fatty acids and other protein reactions, leading to an increase in the acidity of olive oil by four to six times (Valencic et al., 2021, Malheiro et al., 2015). The climatic conditions, the geographic region, and the type of olive variety in the different regions affect the growth and development of the olive fly, the length of its life cycle, and the number of generations per year (Abd El-Salam et al., 2019). The adult olive fruit fly remains active year-round, and females can oviposit throughout the year, except for certain spring months when fruits are unavailable (Ordano et al., 2015). B. oleae e pupates on inner olives in summer. In any case, in autumn, most of the third-instar larvae leave the olive to pupate and overwinter in the soil. In addition, B. oleae can overwinter as larvae or adults in regions with mild winter temperatures. The following adults appear between March and May, and several generations of two to five complement each other depending on environmental conditions (Ortega et al., 2022; Weems and Nation, 2004). In regions where the olive fruit remains on the tree during winter and early spring, the olive fly completes 1 to 2 generations of these fruits in spring. This pest exhibits overlapping generations due to the prolonged survival of adult insects and the extended oviposition period (Wang et al., 2013; Mazomenos et al., 2002).

All stages of the life cycle of B. oleae can be found in the winter, particularly when fruit is present for oviposition and larval development. Adult fruit flies can survive temperatures between 5°C (41°F) and over 40°C (104°F) (Yokoyama et al., 2015; Wang et al., 2009).

In winter, low temperatures, unfavorable environmental conditions, and the absence of fruit are significant limiting factors for the pest population. Adult olive flies first appear in spring, which varies depending on climatic conditions and geographical location (Van Steenwyk et al., 2002; Abd El-Salam et al., 2019).

High mortality rates of eggs, larvae, and pupae occur when temperatures rise above 33°C during the summer, and No flies develop into adults at 35°C. This mortality is more pronounced when low relative humidity levels accompany high temperatures than in other conditions. An increase in relative humidity modifies the lethal effect of high temperatures (Wang et al., 2009).

Biological control has been the most commonly inquired about control strategy inside fruit fly management programs, and parasitoids have been the most natural enemies utilized against pestiferous fruit fly species (Garcia et al., 2020). Hymenopteran parasitoids have been used worldwide to biologically control fruit-infesting Tephritidae (Wang et al., 2021). C. latipes is the only natural enemy of B. oleae reported from Iran (Keyhanian, 2013).

Even though B. oleae is the main insect pest of the olive tree in the world, there are currently few studies about the monitoring of olive fly population dynamics, especially in a climate change scenario. This study examined seasonal variations, bio-ecological characteristics of the population of B. oleae, fruit infestation rate, and C. latipes parasitism percentage in Iran.

The field trial was conducted from 2014 to 2016 in two olive groves of about 1 hectare, with a density of 250 trees per hectare, at Siahpoosh (36° 67′ 77.3"N, 49° 299′ 17.6"E) and Ghooshchi (36° 68′ 86.6"N, 49° 36′ 37.9"E) in Qazvin province in the north of Iran. The local meteorological station obtained data for these areas throughout the three-year experiment.

Sampling of olive fruit fly

The insect sampling was conducted using yellow sticky traps with a synthetic sex pheromone to investigate the population dynamics of the olive fruit fly (Johnson et al., 2006). Three sticky yellow trap cards with sex pheromone (from the Agrisense Company) were installed in each grove. The traps were installed at a distance of 25 meters from each other and at a height of 2 to 3 meters within the tree canopy (Taghaddosi, 2013). The traps were visited weekly, and the pheromones in the traps were replaced every four weeks. The population dynamics graphs were drawn over time for each region and each year to reveal their changes and fluctuations. In order to survey the overwintering stage of the pest, in addition to tracking adult insects with traps, soil sampling was also conducted to examine the pupae.

Determination of fruit infestation rate

In order to investigate the level of fruit infestation in different developmental stages of the olive fly, fruit sampling started at the same time as pit hardening (mid-June) and continued until the oil fruit harvest, which lasted until late November. In fact, until this date, the fruit remains available for the biological activities of the olive fruit fly.

To assess the pest situation during the winter, the remaining fruits on the branches and fallen fruits under the trees were sampled. For sampling in each area, five trees from each orchard were sampled, and 40 fruits in four directions were randomly selected from each tree. 200 fruits were collected in each grove, and a total of 400 fruits were transferred to the laboratory. After examination, they were recorded at different binocular stages of infestation.

The eggs, larvae (total larval stages), pupae, and damaged larvae were counted to determine the infestation percentage. These developmental stages are considered damaging stages of the pest, and various reasons may cause some eggs laid inside the fruit not to hatch and perish.

Investigation of the parasitism percentage of C. latipes

In order to determine the parasitism percentage of C. latipes, 500 infected olive fruits were collected weekly from the study sites during the month of July and stored in five specially designed plastic compartments with adequate ventilation. Then 100 infested fruits were placed in each compartment to count the presence of parasitoids. The plastic compartments were dark black, and a transparent glass test tube was inserted through a hole at the top of each compartment. The test tube was positioned on top of the container to allow potential parasitoid insects to exit and move towards the light.

The parasitoids were then identified and counted. The parasitism percentage is calculated using the following formula:$\:\:\text{P}\text{a}\text{r}\text{a}\text{s}\text{i}\text{t}\text{i}\text{s}\text{m}\:\text{p}\text{e}\text{r}\text{c}\text{e}\text{n}\text{t}\text{a}\text{g}\text{e}=\frac{100*P}{(P+F)}$, where P represents the number of emerged parasitoids, and F represents the number of emerged flies (El-hajj et al., 2018).

To determine the relationship between weather variables (maximum temperature, minimum temperature, average temperature, minimum relative humidity, maximum relative humidity, average relative humidity, and rainfall) and the population of adult olive fruit flies, the data based on the sampling dates were organized.

The insect-day population was calculated using the equation: Insect-days =$\:\sum\:\frac{\text{n}\text{i}+1\:+\text{n}\text{i}}{2}\text{D}\text{i}$. This equation represented the population on the ith date as ni, the population on the (i+1)th to date as ni+1, and the interval between two sampling dates in days as Di (Carey, 1993). This data was considered the dependent variable. The weather data (independent variables) was organized for each region and examined the relationship between the dependent variable and independent variables using multiple regressions. The influence was determined by independent variables using the Stepwise variable selection method.

Statistical analysis of data

After completing the experiment and sampling, statistical analysis was performed using the software SAS. The mean number of captured insects between different generations and between the two regions was compared by Analysis of variance (ANOVA), followed by separation of means by Tukey’s test when significant differences were found at p ≤ 0.05 using the SAS programme, Version 9.1. In order to match the fluctuations of the B. oleae population with climate changes, meteorological data were collected and used from the local synoptic meteorological Station.

Seasonal activity of the olive fruit fly

Temperature, rainfall, and relative humidity information from Siahpoosh and Ghooshchi weather stations were summarized in Table 1.

The number of male insect captures during the study months exhibited a statistically significant difference at the 1% level. Therefore, the mean comparisons were performed using the Tukey method to conduct further investigation. The highest number of male insects was captured in November 2014, while the lowest number was observed in February 2014 (Figure 1).

The interactive effects of region and month on total pest capture were statistically significant at 1%. Ghooshchi had the highest average capture in November 2014, while the same area showed the lowest average in February 2014. In both study orchards, the highest number of trap captures occurred in November (Table 2).

The interactive effects of region and month on male insect captures reached statistical significance at the 1% level. Upon closer examination, Ghooshchi recorded the highest average pest capture in November 2014, whereas it had the lowest averages in February, December, and July 2014 (Table 1).

The olive fly overwinters as mature insects in various shelters and becomes active and preyed upon by traps with the relative warming of the weather. Additionally, during the winter, live larvae of this insect were observed inside infested fruits until April-May (Figures 1 and 2).

Therefore, the pest overwinters as larvae inside fruits and mature insects in shelters. By examining the pupae at a depth of two to three centimeteres under the shade of trees, we found that they cannot overwinter and immediately transform into mature insects when the weather becomes favourable. Mature insects were observed in early winter, and they disappeared due to cold temperatures. The pest overwinters as mature insects in various shelters and as pupae at depths of two to three centimeteres in the soil during early winter (Tables 2 and 3).

In 2014, the first egg-laying on olive fruit was observed on the 15th of June, and a week later, fruit infestation with the first instar larvae and pupae was observed on the 9th of July (Figure 2).

In 2015, The first egg-laying was observed on the 23rd of June, and fruit infestation with larvae was detected on the 31st of June, while pupae were observed on the 13th of July (Figure 3).

In 2016, The first oviposition of the olive fly was discovered on the 17th of June, followed by fruit infestation by its larvae and pupae (Figure 4).

Ghooshchi had a higher number of fly captures in trap stations compared to Siahpoosh. In 2014, the highest number of fly captures occurred 1th of November, while the lowest was in January/February. The number of female captures showed significant differences among the months studied at a 5% significance level. November 2014 had the highest number of female captures, while the lowest numbers were observed in August/September, July/August, July 2014, and September 2015 (Figure 1, Table 2).

Attractant traps were installed in olive orchards in two regions at the beginning of the year and performed their visitation and counting according to the specified method. The results of monitoring the population fluctuation of olive flies in the region showed that in 2014, the first trap captures in Ghooshchi occurred in early February, and we recorded the last capture in early January. No olive fruit flies were captured between January and early February, while the traps recorded the highest captures in mid-October.

In Siahpoosh, the first trap captures were recorded in mid-February and the last capture was in early January. The highest trap capture was observed in Siahpoosh region in early November. The increase in temperature and the higher activity of mature insects caused the first peak of insect captures in traps in Ghooshchi during the spring of 2014 (Figure 2).

In 2015, adult insects were captured throughout the winter and early spring in both Ghooshchi and Siahpoosh, but the amount was meagre.

In Siahpoosh and Ghooshchi, the highest traps captured by pheromone traps occurred in early and late October. Furthermore, in 2016, the highest trap captured by pheromone traps in both regions was recorded in early September (Figure 4).

Traps have minimised hunting activity during hot and cold days of the year, and the highest hunting activity occurs after the end of the summer heat, the cooling of the weather, and the arrival of fruits in autumn. The increase in trap hunting in late summer is due to the temperature decrease and the intensified activity of the olive fruit fly pest. Since fruits are not available in early spring, it can be concluded, based on the peak hunting periods and simultaneous observation of fruits, that B. oleae in Siahpoosh and Ghooshchi has three to four overlapping generations, with the most critical generation occurring in late September, related to the third generation of this insect (Figure 2).

Figures 5, 6, and 7 illustrate the status of fruit infestation in terms of larval population, pupae, and larval tunnels in the examined fruits over three years. With the increase in temperature and the fruit becoming suitable for oviposition, the infestation of fruits also increases. This situation intensifies in late September and early autumn and is also consistently observed in experiments conducted every three years. The highest level of fruit infestation was observed in late autumn (Figures 5, 6, and 7).

Sampling conducted during the years 2014–2015 in the region showed that the parasitoid wasp C. latipes is one of the controlling factors of the olive fly, but it has negligible efficiency in reducing the population of this pest. The emergence and activity of these wasps from the infested fruits observed collected in the region from late August to mid-October over three years resulted in a parasitism rate of 71.0% in the targeted years (Figure 8).

Emerging adult olive fruit flies were examined for sexual differentiation. The ratio favoured female insects in mid-September, but in mid-October, this trend reversed, favoring males. However, on average, late-season olive flies had an approximate sex ratio of 4:1 female to male (Figure 9).

Analysis of the relationship climate change and the population of B. oleae

In Siahpoosh, over three years, the minimum temperature variable exerted the highest significant explanatory effect on the population of the olive fly, with the maximum temperature variable following closely with a lower explanatory coefficient and a significant correlation with the olive fly population. The model excluded the remaining meteorological variables (Table 3).

Studies conducted on adult B. oleae in various shelters have shown that larvae overwinter inside leftover fruit on trees and in the soil (Figure 1).

This pest creates three overlapping generations in Siahpoosh and Ghooshchi, with the first generation starting from early July to late August, the second generation from early September to mid-October, and the third generation starting in mid-October and lasting until late December.

In the two studied areas, the foothills (Ghooshchi) and the plain (Siahpoosh), it was found that olive fly activity and trap catches were higher in the foothill region compared to the plain region. This difference was statistically significant at a 1% level (Table 1, Figure 1).

Figures 1 and 2 indicate that during the hot summer months, no hunting activity for the traps and no live insects inside the fruits were observed. As the temperature decreased in the autumn season, the population of these insects suddenly increased, with the most significant generation occurring during this time of the year.

The olive fly showed no activity throughout the hot summer and from late harvest time to late winter and was missed by the traps (Figure 1).

The seasonal impacts of weather and progressing changes in climatic conditions would lead directly to alterations in the dispersal and development of insect pest species. The change of the environment influences the pest population fluctuation either directly or indirectly through the host physiology (Abd El-Salam et al., 2019, Karuppaiah and Sujayanad, 2012). Olive flies population dynamics are impacted by global climate change (Marchi et al., 2016).

The olive fly has three to five overlapping generations per year with seasonal variations in fly densities (Kokkari et al. 2017; Voulgaris et al. 2013; Pontikakos et al. 2010; Boccaccio and Petacchi 2009). The results of the current study showed that B. oleae has three to four overlapping generations. In the initial two generations of the pest in Siahpoosh and Ghooshchi, the pupae form inside the fruit, but in the third generation, third-instar larvae abandon the fruit to transform into pupae in the soil beneath the trees. Dimou et al. 2003 and Sharaf 1980 showed in their studies earlier that during pupation, the final instar leaves the fruit, drops to the soil, and pupates at a profundity of one to nine centimeters. Under perfect conditions, during summer, it occurs inside the olive tree. At long last, mature adults emerge from the exuviae of the pupa.

In mid-spring, despite unfavorable conditions, a physiological and sexually immature stage appears in the olive fruit fly, accompanied by the formation of fresh olives that are unsuitable for oviposition. During this period, female insects captured by traps are either devoid of eggs or have a low egg count. In this phase, overwintering males and the spring generation do not respond to sexual pheromone traps, and most females lack sperm in their spermathecae (Burrack et al., 2011; Tzanakakis, 2003). Completing this insect's physiological stage coincides with the onset of pit hardening for the ovipositor. When the fresh olive fruit grows and matures in the summer, female flies break their diapauses and start laying eggs, attracted to the olive fruits. Changes in the ovaries of olive flies during the summer affect temperature, humidity, and fruit availability (Abd El-Salam et al., 2019; Kapatos & Fletcher, 1984). These findings are similar to the results of the current study.

Results showed that the infestation begins from June to July in Iran (Siahpoosh and Ghoshchi). The obtained results correspond to the beginning infestation of olive fruit in the US (California), Egypt, southern Italy, Yugoslavia, Spain, and central Greece (Abd El-Salam et al., 2019; Burrack et al., 2011; Katsoyannus, 1992).

The current study appeared during the hot summer months, with no hunting for the traps and no live insects inside the fruits observed. Perovic and Hrncic (2013) showed that higher temperatures cause olive fruits to lose moisture and shrivel, making them unsuitable for egg-laying B. oleae.

This study showed that adult B. oleae in different shelters had larvae overwintering in remained fruit on trees and in the soil, which is consistent with the findings of Ortega et al., (2022), Wang et al. (2013), Weems and Nation (2004), and Vargas et al. (1984). However, Sharaf (1980) reported that in Libya, the pest overwinters in the form of larval stages, pupae, and adult insects. Additionally, the depth of larval penetration into the soil does not exceed three centimeters, which aligns with the studies conducted by Dimou et al. (2003).

In this study, the olive fly activity was higher during the year's cooler seasons and in the foothill region, which is consistent with the findings of Yokoyama (2015). However, considering that the region studied has hot summers and relatively cold winters, the temperature in this region is outside the activity range of B. oleo in both cases. Therefore, during the hot summer and late autumn to late winter, this pest showed no activity and was missed by the traps.

In the areas studied that were infested with the olive fly, the parasitoid wasp C. latipes played a limited role in controlling this pest. Bozbua and Ulusoy's (2008) studies showed there were three to four peaks in the population of olive fruit flies in the Adana region of Turkey. However, the population of olive fruit flies was not high populations. The low population was caused by the presence of natural enemies in the orchards, cultural techniques (such as plowing), high temperatures, a lack of a delay in the harvest of olives, and even an early harvest (Helvac et al., 2018).

For planning effective B. oleae management measures, long-term observations, investigation of pest population dynamics, and weather conditions, are important. It was observed in this study that adult olive flies in Siahpoosh and Ghooshchi start mating three to eight days after emergence in November, which is in line with the results of Preu et al. (2020), Canale et al. (2012), and Mazomenos (1984).

The activity of the olive flies was subordinate to environmental conditions. The monitoring of the pest and, in turn, the assessment of the risk of infestation may be impacted by a limited understanding of dynamic populations and generations (Perovic and Hrncic, 2013; Petacchi et al., 2015; Caselli & Petacchi, 2021). In this research, it was found that the seasonal changes of the olive fruit fly population in Qazvin province, Iran, are affected by climate changes. The use of pest monitoring is crucial to enhancing product quality, dealing with environmental effects, and developing pest control strategies. Based on the obtained results, it is possible to estimate the precise timing for controlling the olive fly and implement proper management strategies to control this pest.

Author Contribution

"A.K. and M.M. wrote the main manuscript text and B.R. prepared all figures and all tables. All authors reviewed the manuscript."

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Tables 1 to 3 are available in the Supplementary Files section.

No competing interests reported.

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Effects of climatic changes on olive fly, Bactrocera oleae (Rossi) population dynamic and its damages in olive orchards in Iran

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