Predators and Parasitoids of Pine Processionary Moth (Thaumetopoea wilkinsoni Tams) in Western Mediterranean Region in Turkey

The pine processionary moth, Thaumetopoea wilkinsoni Tams, 1924 (Lepidoptera: Notodontidae) is the most important defoliator pest of pine forests in the Mediterranean Basin and Turkey. Natural enemies of the pine processionary moth are various species of predators and parasitoids. In this study, field studies were performed in nine study areas which were chosen from four provinces (Isparta, Burdur, Antalya, Muğla) in the Western Mediterranean Region of Turkey to determine the potential predators, larva and egg parasitoids of pine processionary moth. Wintering nests and egg batches of the pine processionary caterpillars were sampled from selected study stations throughout 2018. Calosoma sycophanta (L.) and Forficula smyrnensis Serville were determined as predator species and Phryxe caudata (Róndani), Trichogramma sp., Ooencyrtus pityocampae (Mercet) and Anastatus bifasciatus (Geoffroy) were determined as parasitoids. Forficula smyrnensis is recoreded for the first time as a predator of T. wilkinsoni. Results may contribute to the literature on ecology, forestry studies and biological control efforts


INTRODUCTION
Pine Processionary Moth (PPM), Thaumetopoea wilkinsoni Tams, (Lepidoptera: Notodontidae) is the most important leaf defoilator pest of Southwest Europe, North Africa and the Near East (Battisti et al., 2000). It is the common pest in the Mediterranean Basin and in southern, western and northern parts of Turkey. Pine processionary larvae feed with pine needles in forest ecosystems, weaken the pines and make them vulnerable to secondary pests. Although PPM causes damage to other pine species, its main host is Turkish red pine (Pinus brutia Ten.) and its development on each pine species varies (Hodar et al., 2002). In addition to causing serious economic and ecological losses, the setae of the larvae cause allergic reactions and respiratory disorders such as asthma in humans and mammals (Ziprkowski and Roland, 1966;Lamy, 1990). Two species distributed in Turkey are Thaumetopoea pityocampa (Den. & Schiff.) and T. wilkinsoni (Barbaro and Battisti, 2011). Thaumetopoea wilkinsoni is mostly found in pine forests in the south, west and north of Anatolia, while T. pityocampa generally occurs in Thrace and northwestern Anatolia, and there is a potential hybrid zone of these two twin species in this region (İpekdal et al., 2015).
In this study, it is aimed to determine the potential parasitoids and predators of T. wilkinsoni that uses Turkish red pines as hosts in the western Mediterranean region of Turkey.

MATERIALS AND METHODS
Nine study stations selected from the Western Mediterranean region were visited during 2018 in order to collect samples from PPM (Thaumetopoea wilkinsoni Tams), taking into account the density of red pine (Pinus brutia Ten.). The stations were selected from three different elevation intervals (0-100 m, 400-650 m and 900-1100 m) within four different provinces (Isparta, Burdur, Antalya, and Mugla). Map of nine selcted study stations are shown in Figure 1. Sampling date, localities, coordinates, altitude and area characteristics of nine study stations are shown in Table 1. At each station, one nest from each 15 pine trees infested with PPM was collected with the help of high branch pruning shears and taken to three-liter pet bins. The 30x30 cm cut tulles were stretched to the openings of the bins by using rubber for the insects can continue to breathe. The pupae were searched by digging pits at a depth of 20 cm at the bottom of the infested trees. The pupae were taken together with the soil in which they were placed and put in 1 L canisters. Eggs in cylindrical clusters on the young pine needles were plucked together with the leaves and kept in 1 L bins with tulle on their openings. Samples were brought to Süleyman Demirel University, Faculty of Arts and Sciences, Entomology Laboratory within the same day.
The larvae and nests of PPM larvae were kept in bins in the climate chamber at 25 °C and 55% humidity. In order to observe parasitoid emergence, larvae were conserved under suitable conditions. Therefore, in addition to establishing favorable conditions, the larvae were regularly fed with Pinus brutia needles. The collected pupae and egg clusters were also stored under the same conditions.
A predator coleopteran and a dermapteran species, which were observed to be fed by larvae in nests, prepared for identification. In addition, larva parasitoids (Diptera:Tachinidae) were sampled from the nests that brought to the laboratory and hymenopteran parasitoids were obtained from egg containers and kept for identification. Samples were sent to experts for identification. Also Chopard (1922), Jeannel (1941), Askew and Aldrey (2004) and Samra et al. (2018) were used as diagnostic keys.
Geographical distribution: Europe, Asia and Africa (Narendran, 2009). Table 2 shows the number of sampled parasitoid and predator species in the studty stations.  The 3 rd station was determined to have the highest parasitoid density, while station 7 was the only area without natural enemies. This may be caused by antropogenic activities (marble mine) nearby. Nearly all Trichogramma individuals were sampled from 3 rd station. Forficula smyrnenis was sampled only from 8 th station. Percentages of individuals belonging to parasitoid and predator species were given in Figure 2. The most frequent parasitoid species was Phryxe caudata (59.47%) and was emerged from the eggs in all study stations except Number 7.

DISCUSSION AND CONCLUSİONS
The PPM has a wide range of natural enemies in terms of predators and parasitoids. Six of them were sampled in this study. Mirchev and Tsankov (2005) Pekel (1999) and Avcı and Kara (2002). Ooencyrtus pityocampae is recorded by Mirschev et al. (2004) in southwestern Anatolia. Kanat and Mol (2008) stated that Calosoma sycophanta is used as an effective predator in the biological control of PPM in our country. In addition, Özçankaya and Can (2004) reported Forficula species in the PPM nests.
Calosoma sycophanta, which is frequently used in the biological control of this pest in Turkey (Kanat and Özbolat, 2006;Stolbov et al., 2018), is the first predator species obtained from field studies. Eight individuals from four areas were found. According to Mirchev and Tsankov (2005), this species is the larvae predator of the PPM. However, it is known to feed on pupa (Kanat and Özbolat 2006;Toprak, 2014). C. sycophanta larvae fed by another harmful lepidopteran Lymantria dispar L. pupa has been demonstrated by Weseloh (1985).
Another predator species found in this study is Forficula smyrnensis, sampled in Kemer, Antalya with two individuals. Özçankaya and Can (2004), found Forficula sp. individuals on the PPM nests. They reported that they did not observe the feeding event, so they could not comment on whether they were predators or not. But it was known that these insects were omnivorous and therefore fed with soft bodied insects. On the other hand, it was reported by Kailidis (1962) in Greece that Forficula auricularia was a PPM predator and listed as a predator on the check-list of Mirchev and Tsankov (2005). Haas and Hendrickx (2002), in their study of the intestinal contents of the collected dermapterans, found some plant materials in the gut of F. smyrnensis, so they speculate that the species may be herbivore contrary to its close relatives. However, Tezcan and Kocarek (2009) emphasized that such an interpretation cannot be made from the intestinal contents of a single individual and F. smyrnensis is most likely omnivorous like F. auricularia. For this reason, F. smyrnensis, sampled in a larval nest in Kemer during field surveys, could potentially be a PPM predator and it is recorded for the first time.
Phryxe caudata, which is one of the most common tachinid species in Turkey (Lutovinovas et al., 2018) is sampled from all study sites except 7 th station. Adults began to be observed in containers in which the nests were kept in the laboratory in June. Avcı and Kara (2002) also stated that adults emerged in the second half of June. In terms of the number of individuals, this species was the most sampled with 317 individuals.
Trichogramma species are egg parasitoids of PPM (Mirchev and Tsankov, 2005) and in this study 109 individuals were collected. The members of this Hymenopteran genus cause taxonomic difficulties due to their small size and are difficult to identify (Nagarkatti and Nagaraja, 1977 Finally, hymenopteran egg parasitoid Anastatus bifasciatus was represented in this study with 9 individuals. Anastatus bifasciatus is listed on the chcklist of Mirchev and Tsankov (2005) and previously sampled in Turkey by Pekel (1990).
Results of this study may contribute to the literature on pest ecology, forestry and biological control efforts.