Population dynamics and parasitoid complex of Archips rosana (L.) (Lepidoptera: Tortricidae) in Western Turkey

The rose tortrix moth, Archips rosana (L.) (Lepidoptera: Tortricidae), is a pest that causes serious crop losses in apple orchards throughout the world. In this study, the population dynamics of A. rosana and its associated parasitoids were investigated in two provinces of Western Turkey (Denizli and Usak) in 2018 and 2019. A total of 318 egg masses, 300 larvae, and 129 pupae were collected from the survey areas. Although no parasitoids were detected in egg masses, ten parasitoid species belonging to Braconidae, Chalcididae, and Ichneumonidae (Hymenoptera), and Tachinidae (Diptera), were reared from the samples of larvae and pupae. Phytodietus astutus (Gravenhorst) (Ichneumonidae) was the most abundant parasitoid species, with a relative abundance of 35.1%, followed by Itoplectus maculator (Fabricius) (Ichneumonidae) represented by 27% of the recovered parasitoids. Moreover, P. astutus and Scambus inanis (Schrank) (Ichneumonidae) reared from the samples are the first records from Turkey, while Cotesia glomerata (L.) (Braconidae), Exochus sp.(Ichneumonidae), and Nemorilla maculosa (Meigen) (Tachinidae) are the first records from A. rosana. Using pheromone traps in the apple orchards, the first adult of A. rosana was caught on May 24 in Civril (Denizli) and on May 30 in Sivasli (Usak) in 2019. www.biotaxa.org/RSEA. ISSN 1851-7471 (online) Revista de la Sociedad Entomológica Argentina 79(4): 1-7, 2020 Copyright OZEN, M. et al.This is an open access article distributed under the terms of the Creative Commons Attribution Licence (CC BY 4.0) 1


Apple,
Malus domestica (Borkh) (Rosales: Rosaceae), is one of the most widely cultivated fruits in the world, constituting 12% of total world fruit production. According to the United States Department of Agriculture (USDA), in the 2019-2020 season, 75.8 million tons of apples were produced in a cultivated area of 5.3 million hectares (USDA, 2020). The origin of apple is Turkistan, the Caucasus, and Anatolia. Hence, it is not surprising that Turkey is an important production center for apple, with its 3.6 million tons accounting for 4.2% of the world's annual production. Globally, Turkey ranks third in apple production, following China and USA (FAOSTAT, 2020).
Archips rosana (L.) (Lepidoptera: Tortricidae) is a pest that causes significant losses in apple orchards if management efforts are not employed. It has been reported to damage the foliage and fruit of ornamental, forest, and fruit trees, especially apples, pears, quince, plums, walnuts, peaches, and cherries trees (Aysu, 1955;Kovancı et al., 2003;Piekarska-Boniecka et al., 2019). Females generally lay their eggs on the bark of the trunk and thick branches, where they overwinter, hatching the following spring. First instars feed in leaf shelters, causing leaves to drop, and later instars feed on the fruits (Erden, 1988;Polat & Tozlu, 2010;Canbay & Tozlu, 2013). The species is univoltine throughout its range.
Pesticides used to control pests and diseases in agriculture not only have an impact on target organisms, but also cause significant damage to non-target organisms such as natural enemies. In addition, pesticide misuse frequently drives the development of resistance to these chemical substances, requiring a gradual increase in the amount of the pesticides being used. According to the Republic of Turkey Ministry of Agriculture and Forestry, the amount of pesticides used in Turkey has increased by 59% to 60,000 tons over the last decade. Given that only 0.1% of pesticides used reaches target pests, the destructive effect of these chemicals on the environment is significant and widespread (Pimentel, 1995;Gill & Garg, 2014). To reduce pesticide usage, it is important to understand the composition and abundance of natural enemies of the target pest.
The present study was conducted to determine the field biology of A. rosana and its parasitoids and quantify rates of parasitism of this species in apple orchards in western Turkey.

Determination of the parasitoids
Surveys were conducted in apple orchards in six different locations in the provinces of Usak and Denizli, Turkey in 2018 and 2019 (Table I). All apple orchards are conventionally farmed, and pesticides are used to manage diseases and pests. Survey sites are at similar altitudes, between 800-950 m, and continental climatic conditions. Samples of eggs, larvae, and pupae were collected bimonthly from each location between February and June in both years.
Egg masses found during field surveys conducted in February and March were removed from bark using a knife, and placed in glass tubes (11 x 1.6 cm). The tubes were covered with muslin cloth and kept at room temperature until emergence of larvae or parasitoids. In order to determine larval and pupal parasitoids of the A. rosana, at least 50 samples of larvae were collected from each district in April and May of both years, following the protocol of Razmi et al. (2011). Larvae were reared in plastic boxes (10 x 10 x 3.5 cm) maintained at room temperature. The larvae were fed with fresh apple leaves. Emerging parasitoids were pinned and labeled using a binocular microscope and sent to experts for identification. Braconid (Hymenoptera: Braconidae) species were sent to Ahmet Beyarslan (Bitlis Eren University, Turkey), tachinid (Diptera: Tachinidae) species to Kenan Kara (Gaziosmanpaşa University, Tokat, Turkey), and ichneumonid (Hymenoptera: Ichneumonidae) species to Sasha Varga (I.I. Schmalhausen Institute of Zoology of National Academy of Sciences of Ukraine). Additionally, the identification of A. rosana was confirmed by Mustafa Özdemir (Directorate of Plant Protection Central Research Institute, Ankara, Turkey). Voucher specimens of all parasitoids are deposited in the Insect Museum of the Plant Protection Department, Faculty of Agriculture and Natural Sciences, Usak University, Usak, Turkey.

Population monitoring
Population monitoring of the pest was conducted in a 1.1 ha apple orchard in Usak, Sivasli (38.502095 N, 29.667049 E) and in a 1.4 ha orchard in Denizli,Civril (38.306233 N,29.775270 E) in 2019. In each location, one delta trap with a sticky board baited with pheromone (PH-104-1RR, Russel IPM) was deployed on the south Revista de la Sociedad Entomológica Argentina 79(4): 1-7, 2020 side of the trees about 1.5 m above the ground level in mid-May. The traps were checked twice a week until the first adults were trapped, and from then on once a week, with the number of adults recorded. The pheromone capsule was changed every five weeks, as recommended by Russel IPM.
To determine the first emerging date of larvae from egg masses, four trees with egg masses detected in Sivasli and Civril in 2019 were marked and checked weekly. The sum of effective temperatures for first hatching egg and first adult appearance of A. rosana was calculated using the following formula: where "C" refers to sum of effective temperatures, "T 1 ….T n " refers to mean daily temperature and "t 0 " refers to physiological threshold. Average temperature and relative humidity values regarding survey areas were obtained from the Turkish State Meteorological Service.

Data analysis
All statistical analyses were performed using the SPSS 16.0 software package. The groups were composed of parasitism rates of samples collected from Banaz, Civril and Sivasli districts in both years. The difference between the groups was examined using one-way (ANOVA) variance analysis and independent samples t-test. The parasitism rates, expressed as a proportion, were performed using arcsine transformation before the statistical analyses. The parasitism rate was calculated as the ratio of the number of a parasitoid species to the total number of larvae and pupae collected in the localities, whereas the relative abundance was determined as the ratio of the number of a parasitoid species to the total number of parasitoids.

RESULTS AND DISCUSSION
A total of 429 samples were collected during the study: 207 (150 larvae, 57 pupae) in 2018 and 222 Table I (150 larvae, 72 pupae) in 2019. Ten parasitoid species, belonging to Ichneumonidae, Braconidae, and Chalcididae (Hymenoptera), and Tachinidae (Diptera), were detected (Table II, Table III). Ichneumonidae was the most commonly encountered family with five parasitoid species, followed by Braconidae (three species), Chalcididae (one species), and Tachinidae (one species). Twelve individual parasitoids were reared from the samples in 2018 and 25 in 2019. Parasitism rates in 2018 and 2019 were 5.8% and 11.3%, respectively.
Overall, ichneumonid parasitoids accounted for 6.3% of total of parasitism rate (8.6%) and were the most effective species in the parasitization of the pest. This finding is consistent with those of Piekarska-Boniecka (2004), Kot (2007), and Piekarska-Boniecka et al. (2019), all of which found Ichneumonidae to be the most effective parasitoid. In Edirne province, northwestern Turkey, the parasitoid complex of A. rosana was studied by Aydoğdu (2014), and 23 parasitoid species were found. Because that study was conducted in an organic orchard, the number of parasitoid species observed was considerably higher than in our research. Phytodietus astutus (Gravenhorst) (Ichneumonidae) was the most abundant parasitoid species, with a relative abundance of 41.7% in 2018, while in 2019, Itoplectis maculator (Fabricius) (Ichneumonidae) was the most abundant (36%), followed by P. astutus (32%). Similarly, I. maculator was reported to be the most abundant species in studies conducted by Polat & Tozlu (2010) and Aydoğdu (2014).
No parasitoids were reared from the total of 318 egg masses collected in 2018 and 2019. By contrast, Ercan et al. (2015) reported two Trichogramma species (T. dendrolimi (Matsumura) and T. euproctidis (Girault)) as egg parasitoids of A. rosana in the Central Anatolia Region of Turkey. In a similar study, Wei et al. (1998) found no parasitoids in egg masses. In addition, none of the other studies conducted in Turkey recovered egg parasitoids from A. rosana.
In Civril, the first emergence of A. rosana larvae from egg masses was observed on March 21, when the maximum temperature was 19.1 °C, the first larvae were recorded on April 2 (15.1 °C) in Sivasli. Egg hatching commenced on the date when the sum of effective temperature (above 8 °C) reached 36 °C in Sivasli,34 °C in Civril. In a study conducted in Poland, Pluciennik & Tworkowska (2004) found this temperature to be about 60 °C in 1993, 1995, and 1996, 50 °C in 1994, and about 30 °C in 1997. Similarly, AliNiazee (1977 also indicated that the sum of effective temperatures necessary for the onset of egg hatching was 40 °C. Ulu (1983) and Doğanlar (2008) reported hatching dates of A. rosana eggs on February 15 and March 29, respectively. Polat & Tozlu (2010) determined the first date of hatching to be May 12 in eastern Turkey. The differences among dates are almost certainly the result of temperature differences of the regions, and varying from year to year.
The delta traps used to monitor the adult population of A. rosana were hung on trees on May 10 in Civril and on May 12 in Sivasli. The first moths were captured on May 24 in Civril, when average temperature and relative humidity were 19.4 °C, 65% respectively, whereas in Sivasli, they were captured on May 30 (21.9 °C and 39.3%). The moth flight lasted for about 30 days until the end of June in both localities (Figs. 1, 2). Pluciennik & Tworkowska (2004) found that the flight period of this species varies between 30 and 53 days.
In research conducted in eastern Turkey, Canbay & Tozlu (2013) found that the adult flight period began on June 16 and lasted 34 days. In dates of first catch, the Table III  sum of effective temperatures in Civril and Sivasli as of January 1 st was found to be 477 and 535 degree-days, respectively. In parallel with this study, Doğanlar (2008) established that the sum of effective temperatures necessary to initiate moth emergence is 512 degreedays. The highest number of individual moths in the traps of Sivasli and Civril were 36 on June 27 and 17 on June 14, respectively. Afterwards, the number of catches declined sharply. Similarly, the highest numbers of catches were reported to occur from the middle to the end of June in studies by Kovancı et al. (2003) and Pluciennik & Tworkowska (2004). The total number