Silva Balcanica, 18(1)/2017

Structure of egg clusters and egg parasitism characteristics of solitaria (Freyer) (: ) in THE Eastern Rhodopes, Bulgaria

Plamen Mirchev, Georgi Georgiev, Margarita Georgieva Forest Research Institute – Sofia Bulgarian Academy of Sciences Peter Boyadzhiev Department of Zoology, University of Plovdiv, Bulgaria

Abstract

Egg structure and main characteristics of egg parasitism of pistachio processionary (Thaumetopoea solitaria) were studied in six sites in the Eastern Rhodopes in Bulgaria. The results showed that T. solitaria lays eggs on branches with a diameter of 3.6-13.0 mm and the productivity of female butterflies varies between 43 and 187 eggs. Three parasitoids were reared from host eggs: Anastatus bifasciatus (Hymenoptera: Eupelmidae), Ooencyrtus masii and Ooencyrtus sp. nr. indefinites (Hymenoptera: Encyrtidae). A. bifasciatus was the most important parasitoid occupying 81.4-97.3% of the total egg production in different sites. A part of A. bifasciatus population emerged before hibernation. Its emergence period in 2014 was about 100 days, and in 2015 – 69 days. The emergence period of O. masii was shorter but almost coincided with mass emergence of A. bifasciatus. However, Ooencyrtus sp. nr. indefinites appeared after the mass emergence of the other two parasitoids. In 2014 and 2015, its emergence started 15 and 8 days after the completion of mass emergence of O. masii, respectively.

Key words: Thaumetopoea solitaria, egg parasitoids, phenology, impact, Eastern Rhodopes, Bulgaria

INTRODUCTION

The pistachio processionary moth, Thaumetopoea solitaria (Freyer, 1838) (Lepidoptera: Notodontidae) is an East Mediterranean-Turanian species, distributed from FYR Macedonia to , Afghanistan and (Androić, Serafimovski, 1954; Davatchi, 1958; Halperin, 1983; Roques, 2015). In Bulgaria, it is distributed in some regions of southern part of the country (Buresch, 1918-1919; Mirchev еt al. 2004). The host plant of T. solitaria is Pistacia terebinthus L. In this respect, the damage caused by the can be assessed as having no economic importance. However, the middle- and old-instar caterpillars possess urticating hairs. The ability of T. solitaria to cause severe allergies to humans and decreases or compromises the recreation functions of biotopes attacked in suburban zones and forest parks.

41 Some aspects of biology and ecology of T. solitaria were studied by Davatchi (1958), Serafimowsky (1975), Halperin (1983) and Mirchev et al. (2006). In Bulgaria a disease on larvae caused by Beaveria bassiana (Bals.-Criv.) Vuill. was established (Mirchev et al., 2012). In addition, first record of egg parasitoids of the species was reported (Mirchev et al., 2014a). This paper announces data about bionomics of T. solitaria in egg stage: structure of egg clusters, embryonic mortality, egg parasitoids and their impact on the host in the Eastern Rhodopes in Bulgaria.

MATERIAL AND METHODS

The study was conducted in 6 sites in the region of the town of Madzharovo (left bank of Arda River), town of Ivaylovgrad (Ivaylovgrad dam, Dupkata protected area, Quarry place), Belopolyane vill. (Likania protected area) and Meden buk vill. (left bank of Byala reka). The main characteristics of study areas are given in another publication (Boyadzhiev et al., 2017). In each site, cuttings of approximate length 4-5 cm from branches of P. terebinthus with egg clusters of T. solitaria were collected on 7 April 2014 and 16 April 2015 in xerophyte forest stands. After collection, the clusters were put singly in test tubes covered with cotton stoppers, and were transported to the laboratory of Forest Research Institute - Sofia. The scales of egg clusters were removed, and the samples were kept at room temperature (20-22ºC) for daily observation. The emerged parasitoids were removed from test tubes and separated in plastic capsules for further determination. Every egg with a hole in the eggshell was opened carefully and the meconia and remains of the emerged or dead were determined by a stereomicroscope (40 × magnification) according to Schmidt, Kitt (1994) and Tanzen, Schmidt (1995). The productivity of T. solitaria females was calculated by the number of eggs in different egg clusters. The differences in egg sizes in various samples were determined by F-factor (Schmidt et al., 1999), which indicates the number of eggs per 1 cm egg row length, as follows:

e F = , where: r.l e – egg number; r – number of rows; l – cluster length (mm). T. solitaria egg mortality was divided into 5 groups: caterpillars died; undeveloped eggs with dried-up yolk; eggs totally empty; parasitized eggs; and eggs destroyed by predators.

42 RESULTS Structure of egg clusters The egg productivity of T. solitaria females varied between 43 and 187 eggs (Table 1). The difference between the average egg number in clusters of samples with highest values established (Ivaylovgrad dam, 153.9) and those with the lowest (Likania, 116.6) was 24.2%. The sample from Quarry collected on7 April 2014 showed the greatest dispersion, and that from Madzharovo collected on 16 April 2015 was the most compact. The egg clusters were laid on branches with a diameter of 3.6-13.0 mm. Their mean diameter varied between 5.1 and 6.9 mm (Table 1). The length of egg clusters varied between 7.0 and 28.0 mm. The parameters of three main indicators of egg clusters (egg number, length of egg clusters, and row number), are mutually dependent. As concerns to average length of egg clusters, a difference of 25.3% has been registered between the values from Ivaylovgrad dam (22.1) and Likania (16.5) – the samples with the greatest differences in average egg number in 1 egg cluster. The number of rows in them (5-9) was less variable than both indicators already discussed. The difference in the average number of rows (6.4-7.1) was 9.9%. Factor F in samples averaged 10.35-10.82 (Table 1). The difference between the highest and the lowest values established was 4.3%, i.e. almost 6 times lower than the differences between the highest and the lowest values for the average egg number in one cluster. The diameter of one visible egg on a cluster was 0.98 mm. The survival rate of T. solitaria in egg stage is determined by influence of biological and ecological factors. The average number of hatched caterpillars varied between 63.6 and 87.6% (Table 1). The differences in average values of emerged caterpillars can be defined as substantial and it can be assumed that here the influence of ecological factors has been decisive, whereas the health and physiological condition of the butterflies has probably been the reason for the enormous difference from 6.6% to 100.0% in individual egg clusters. T. solitaria egg mortality The analyses showed that some larvae died during hatching, i.e. a presence of exit openings and dead caterpillars in the eggs was observed (Table 2). Other dead larvae were found in the eggs without exit openings – an indication that the death had occurred before the emergence period. In a part of dead caterpillars and undeveloped eggs with dried-up yolk presence of fungal mycelium was established, but the pathogen and the pathogenesis had not been identified. The parasitoids’ impact has the highest share in mortality at the egg stage. It approximate distribution among different groups was as follows: a half part was due to parasitization; a quarter part - to undeveloped eggs with dried-up yolk; and the remaining quarter part was divided among the above-mentioned factors. In almost all samples, the parasitized eggs were over 50%, and Ivaylovgrad dam sample reached close to this value – 46.3%. In eight samples – Ivaylovgrad dam being the exception again – eggs destroyed

43 16 91 14 5.8 1.6 3.8 8.7 2.5 Mb 153 buk 17.2 16.7 2014 1921 120.1 7 April 7 April Meden Meden

L 35 56 6.4 1.7 3.6 3.1 9.0 166 23.3 10.0 16.5 2014 4081 116.6 7 April 7 April Likania 8 D 95 16 5.8 0.9 4.5 7.1 3.6 187 27.2 22.1 2015 1231 Dam 153.9 16 April 16 April 38 43 5.8 1.6 3.9 3.8 7.0 173 Q 2 29.1 10.2 17.0 2015 4463 117.4 16 April 16 April Quarry 26 48 6.9 2.8 3.6 3.7 8.0 170 Q 1 30.8 13.0 17.5 2014 3158 121.5 7 April 7 April 29 73 5.9 1.1 4.5 9.0 3.0 165 D 2 23.8 18.0 10.0 2015 3569 123.1 16 April 16 April Dupkata 44 66 5.9 1.4 3.7 3.0 9.8 178 D 1 24.0 10.0 17.6 2014 5658 128.3 7 April 7 April 8 5.1 0.9 4.0 6.2 2.3 118 155 M 2 14.5 20.1 17.0 2015 1108 138.5 16 April 16 April Madzharovo 18 5.5 1.2 4.1 8.0 2.1 104 169 M 1 18.9 19.2 16.0 2014 2523 140.2 7 April 7 April Structure of egg clusters and rate of hatching of caterpillars in various regions of the Eastern Rhodopes, Bulgaria regions of egg clusters and rate hatching caterpillars in various 1. Structure Table Site of collection Site Date of collection Date Code Number of egg cluster s Number Total number of eggs number of eggs Total Mean Mean ±SD Minimum Minimum Maximum Maximum Diameter of branches on which egg of branches on which egg Diameter deposited clusters were (mm) Mean ±SD Minimum (mm) Minimum Maximum (mm) Maximum Length of egg clusters (mm) Mean ±SD Minimum (mm) Minimum

44 6 8 7.1 0.8 1.1 Mb buk 22.3 7.65 76.1 14.5 40.2 93.8 2014 10.35 11.34 7 April 7 April Meden Meden 5 9 L 6.7 0.9 6.6 23.2 10.7 0.89 7.95 77.5 99.1 2014 12.64 19.89 7 April 7 April Likania 6 8 D 28 6.5 0.9 9.9 0.54 80.3 10.7 57.9 91.3 2015 Dam 10.72 11.47 16 April 16 April 5 9 6.5 1.0 Q 2 24.0 1.03 7.89 81.2 14,2 28,2 97,7 2015 10.80 12.50 16 April 16 April Quarry 5 9 6.5 0.9 0.7 Q 1 24.0 1.05 7.93 77.9 19.2 96.6 2014 10.62 11.96 7 April 7 April 5 8 6.4 0.8 D 2 25.0 1.04 7.40 83.4 11.8 99.2 53.3 2015 10.63 12.50 16 April 16 April Dupkata 5 9 6.7 0.9 D 1 25.0 1.02 7.33 87.6 10.9 59.5 2014 10.82 13.15 100.0 7 April 7 April Table 1. Continued Table 6 7 6.5 0.5 M 2 24.0 0.81 9.21 63.6 22.5 21.2 91.5 2015 10.66 11.57 16 April 16 April Madzharovo 6 7 6.7 0.5 M 1 22.0 0.41 9.76 75.9 13.7 50.7 96.7 2014 10.82 11.39 7 April 7 April F

Site of collection Site Date of collection Date Code Maximum (mm) Maximum Number of egg rows per cluster per cluster of egg rows Number Mean ±SD Minimum Minimum Maximum Maximum Factor Factor Mean ±SD Minimum Minimum Maximum Maximum Caterpillars hatched, % Mean ±SD Minimum Minimum Maximum Maximum

45 by predators were found, although not in large quantities. Three egg parasitoids were reared from samples studied: Anastatus bifasciatus (Geoffroy, 1785) (Hymenoptera: Eupelmidae), Ooencyrtus masii (Mercet, 1921) and Ooencyrtus sp. nr. indefinites (Myartseva, 1982) (Hymenoptera: Encyrtidae) (Table 2). A. bifasciatus was the most important egg parasitoid of T. solitaria. It was found in all 222 egg clusters studied, and its percentage in parasitoid complexes of the host in different sites varied between 81.4 and 97.3 (Table 2). All adults, emerged after sample collection, as well as the dead adult individuals found in host eggs were male. The majority of emergence openings ofA. bifasciatus were found on the upper part of T. solitaria eggs (Table 2), which is an indication that this parasitoid is well adapted to the host. The share of dead parasitoids in the eggs of T. solitaria in different sites was high (19.7-41.5%) (Table 2). The mortality occurred predominately in larval stage and it is impossible to determine their species belonging. Emergence of egg parasitoids In both years, part of A. bifasciatus adults emerged before the date of sample collection. In 2014 and 2015, this share averaged 11.3% and 5.5%, respectively. Daily observations showed that no emergence of A. bifasciatus adults was observed during the first 7-16 days after collection. For example, in 2014, the samples were collected on 16 April but the first parasitoid emergence happened on 23 April only. It is known that T. solitaria lays eggs from early to late autumn (Roques, 2015), and this fact leads to the assumption that established early emergence of A. bifasciatus took place before hibernation. After the hibernation in 2014, the emergence period of A. bifasciatus was about 100 days – from 23 April to 1 August (Fig. 1). However, the mass emergence (time in which 90% of adults emerged) was 29 days – from 23 April to 21 May. In 2015, this process was more intensive: the emergence period was 69 days (from 25 April to 1 June), and the mass emergence was completed within 19 days (from 25 April to 1 May). The emergence period of O. masii was shorter but almost coincided with that of A. bifasciatus (Fig. 1). In contrast, the first specimens ofO. sp. nr. indefinites began to appear after the mass emergence of other two parasitoids. However, comparisons between both established representatives of Ooencyrtus genus should be made with the caveat that they are in small number. In 2014, emergence of O. sp. nr. indefinites started 15 days after the completion of mass emergence of O. masii and 8 days in 2015, respectively.

DISCUSSION

In the six investigated sites, the average productivity of T. solitaria (116.6-153.9) is lower than that in Israel (146-169) (Halperin, 1983, 1990a), and a little higher than in Macedonia (114.4) (Serafimowsky, 1975). In the locality Ivaylovgrad dam, a previous two- year study on T. solitaria productivity showed that the average number of eggs in one cluster

46 6 4 2 4 6 Mb 155 149 5 (1.1) 4 (0.9) 44 (9.6) 18 (3.9) 30 (6.5) 42 (9.2) 58 (12.6) 459 (100) 179 (100) 258 (56.2) 165 (92.2) - - L 49 19 30 28 19 298 279 3 (0.3) 85 (9.3) 11 (1.2) 27 (2.9) 918 (100) 397 (100) 234 (25.5) 558 (60.8) 375 (94.5) - - - - - 1 3 D 76 73 6 (2.6) 7 (3.0) 18 (7.9) 85 (100) 65 (28.4) 27 (11.8) 77 (90.6) 229 (100) 106 (46.3) 6 7 16 22 12 269 257 Q 2 2 (0.2) 51 (6.1) 16 (1.9) 19 (2.3) 31 (3.7) 86 (10.3) 839 (100) 366 (100) 100 (11.9) 534 (63.6) 298 (81.4) - 7 12 19 11 19 176 165 Q 1 9 (1.3) 5 (0.7) 5 (0.7) 7 (1.0) 83 (11.9) 699 (100) 236 (100) 219 (31.3) 371 (53.1) 214 (90.6) Codes (see Table 1) Table Codes (see and mortality of egg parasitoids in host eggs 3 8 19 16 12 239 227 D 2 1 (0.2) 6 (1.0) 6 (1.0) 16 (2.7) 13 (2.2) 81 (13.7) 85 (14.4) 591 (100) 275 (100) 383 (64.8) 266 (96.7) - - 49 15 34 15 11 212 197 D 1 34 (4.8) 10 (1.4) 28 (4.0) 706 (100) 285 (100) 112 (15.9) 400 (56.6) 122 (17.3) 272 (95.4) - 3 3 5 2 175 170 M 2 8 (2.0) 4 (1.0) 5 (1.2) 22 (5.4) 12 (3.0) 24 (6.0) 89 (22.1) 403 (100) 194 (100) 239 (59.3) 180 (92.8) - 9 2 7 9 21 198 177 M 1 7 (1.2) 60 (9.9) 17 (2.8) 11 (1.8) 53 (8.7) 608 (100) 222 (100) 320 (52.6) 140 (23.0) 216 (97.3)

with with

T. solitaria emergence, embryonic mortalityT. of 2. Parasitoids Table Parameters Total mortality of eggs, number (%) Total Caterpillars died without opening Caterpillars died without opening with Caterpillars died without opening with fungal mycelium Caterpillars died with opening Caterpillars died with opening Impact of egg parasitoids Impact Undeveloped eggs with dried-up yolk Undeveloped eggs with dried-up yolk Undeveloped fungal mycelium Eggs totally empty, without any remains totally empty, Eggs Determined egg parasitoids, number (%) Determined Eggs destroyed by predators by destroyed Eggs Anastatus bifasciatus Emerged before collection of egg clusters before Emerged emergence opening on top egg-shell emergence opening on the side of egg- shell after collection of egg clusters, Emerged all male emergence opening on top egg-shell emergence opening on the side of egg- shell died in eggs Adults

47 - - - - 14 14 79 Mb 14 (7.8) 7 (43.7) 16 (100) 83 (32.2) 258 (100) 175 (67.8) - - - - L 22 22 161 22 (5.5) 4 (11.4) 33 (94.3) 558 (100) 369 (66.1) 189 (33.9) - - - - 8 8 D 21 8 (9.4) 8 (100) 4 (50.0) 84 (79.2) 22 (20.8) 106 (100) 44 44 24 24 168 Q 2 6 (84.2) 24 (6.6) 44 (12.0) 12 (31.6) 10 (26.3) 534 (100) 359 (67.2) 175 (32.8) 11 11 11 11 135 Q 1 11 (4.7) 5 (19.2) 11 (4.7) 9 (34.6) 23 (88.4) 371 (100) 217 (58.5) 154 (41.5) Codes (see Table 1) Table Codes (see 8 8 1 1 108 D 2 8 (2.9) 1 (0.4) 1 (3.4) 5 (17.2) 27 (93.1) 383 (100) 267 (69.7) 116 (30.3) 9 9 4 4 115 D 1 9 (3.2) 4 (1.4) 3 (6.8) 7 (15.9) 40 (90.9) 400 (100) 274 (68.5) 126 (31.5) Table 2. Continued Table 3 3 11 11 45 M 2 3 (1.5) 8 (100) 11 (5.7) 4 (50.0) 1 (12.5) 47 (19.7) 239 (100) 192 (80.3) 5 5 1 1 98 M 1 5 (2.3) 1 (0.4) 1 (5.6) 3 (16.7) 18 (100) 320 (100) 213 (66.6) 107 (33.4) Parameters Egg clusters with found A. bifasciatus , Egg number (%) Ooencyrtus masii Emerged after collection of egg clusters Emerged emergence opening on top egg-shell , number clusters with found O. masii , number Egg (%) sp. nr. indefinitus nr. Ooencyrtus sp. Emerged after collection of egg clusters Emerged emergence opening on top egg-shell sp. nr. nr. clusters with found O. sp. Egg indefinitus , number (%) Undetermined larvae and pupae of Undetermined parasitoids, number Total egg parasitoids, number (%) Total Emerged adults , number (%) Emerged Died adults , pupae and larvae, number Died (%)

48 Month 15-30 April 1-31 May 1-30 June A.b. ▬▬▬▬▬▬▬▬▬▬▬▬▬═════════════════════════

2014 O.m. ▬▬▬▬▬▬▬▬▬══════════ O.i. ═══════▬▬═════ A.b. ▬▬▬▬▬▬▬▬════════════ O.m. ▬▬▬▬▬▬══════ 2015 O.i. ▬▬▬▬▬═══════

Fig. 1. Emergence of egg parasitoids in laboratory conditions; mass emergence (90%) of adults is indicated Fig. 1. Emergence of egg parasitoids in laboratory conditions; mass emergence (90%) of adults by a black bar; the scattered emergence is indicated by a white bar: A.b. - Anastatus bifasciatus (the period isof indicated emergence by in a 2014 black lasted bar; untilthe scattered 1August); emergence O.m. - Ooencyrtus is indicated masii; O.i.by a - white Ooencyrtus bar: A.b.sp. nr. - Anastatusindefinitus bifasciatus (the period of emergence in 2014 lasted until 1August); O.m. - Ooencyrtus masii; was 120 and 144 (Mirchev et al., 2006), i.e. differences of 22.0% and 6.4% compared O.i. - Ooencyrtus sp. nr. indefinitus with the value obtained in this study (an average of 153.9 eggs). The egg productivity of T. solitaria is close to the productivity of other two processionary distributed in Bulgaria, Thaumetopoea pityocampa(Denis et Schiffermüller, 1775) and Thaumetopoea processionea (Linnaeus, 1758), but the results of long-term studies have shown a great variability of this indicator even in one and the same biotope (Mirchev, 2005). Similar egg productivity was also reported for Thaumetopoea jordana (Staudinger, 1894) (197) (Furth, Halperin, 1979) and Thaumetopoea pinivora(Treitschke, 1834) (164-165) (Tsankov et al., 1993). In Italy, deterioration of egg characteristics of T. pityocampa at lower altitudes (below 500 m) was observed (Tiberi, Roversi, 1987). Mirchev (2005) reported that egg productivity of T. pityocampa is higher in the northern regions of its range. The author considered that fertility is not a constant value in a specific region or year, but is determined by a number of ecological factors and gradation phases. The female butterflies of T. solitaria lay their eggs on thin twigs, which diameter in this study is comparable to that in Israel (Halperin 1990a). Buresch (1918-1919) also reported that egg clusters are most frequently deposited on thin twigs, but sometimes they can be observed on stems. Similar deposition was reported for T. processionea: on twigs with diameter similar to that of this study (Mirchev et al., 2003) and rarely on twigs up to 21.5 mm (Dissescu, Ceianu 1968). Serafimowsky (1975) established that sterile eggs of T. solitaria usually do not exceed 10%, but in some cases can reach 71%. Similar data were obtained in this study: the undeveloped eggs with dried-up yolk varied between 2.2% (Dupkata, 7 April 2014) and 7.1% (Quarry, 7 April 2014). Among the biological factors regulating pistachio processionary moth number, larval and pupal mortality caused by entomolpathogenic fungus B. bassiana (Halperin, 1983, 1990b; Mirchev et al., 2012) and several parasitoids (Halperin, 1983, 1990b; Kugler, 1979) was established. Egg parasitoids of T. solitaria were reported for first time in Bulgaria. In the region of the Eastern Rhodopes two species (A. bifasciatus and O. pityocampae) were reared from egg clusters of the host with a numerical ratio of 997:2 (Mirchev et al., 2014a). The second parasitoid was found in a biotope with high number of T. pityocampa in the period of investigation. In this study, one more species (O. masii)

49 was added to the list of egg parasitoids of T. solitaria. It is polyphagous on T. processionea, Traumatocampa ispartaensis (Lepidoptera: Notodontidae) (Doğanlar, Avcí, 2001), Malacosoma neustria (Linnaeus, 1758) (Lepidoptera: Lasiocampidae) and Lymantria dispar (Linnaeus, 1758) (Lepidoptera: Erebidae) (Noyes, 2016). Relatively high mortality of egg parasitoids have been obtained but it is difficult to determine the reasons. It is unclear whether this is due to rearing in laboratory conditions or is determined by the host characteristics. Publications on egg parasitoids of T. solitaria are limited (Boyadzhiev et al., 2017; Mirchev et al., 2014a), which does not provide many opportunities for comparing and analyzing concrete data. High levels of egg mortality caused by parasitoids were reported in studies on other processionary moths, as well. O. pityocampae parasitized between 11.2 and 73.5% of T. pityocampa eggs in samples from various regions of its habitat (Mirchev et al., 1999). Halperin (1990b) studied the influence of temperature and established that O. pityocampae is more sensitive to temperatures over 320C than Baryscapus servadeii (Domenichini, 1965) (Hymenoptera: Eulophidae). Masutti (1964) reported that temperatures over 300C are unsuitable for this parasitoid. Mirchev (2005) examined a large number of T. pityocampa samples from countries in Balkan Peninsula in which mortality rate of 10- 20% of A. bifasciatus and O. pityocampae individuals was observed. It was not influenced by the duration of parasitized eggs’ stay in laboratory conditions. High survival rate of A. bifasciatus was registered at a lower parasitization level on T. processionea (Mirchev et al., 2003). Mirchev (2005) found dependence between location of parasitoid exit holes in the eggs of T. pityocampa and presence of covering scales. In case of removing covering scales, the share of exit holes of O. pityocampae, B. servadeii and A. bifasciatus on egg top parts increased. This increasing was most substantial forA. bifasciatus most probably due to light regime. The present study confirmed this hypothesis because of higher percentage of side holes before sample collecting compared to those in laboratory conditions after the scale removal. From an ecological point of view, the cohabitation of T. solitaria with the most dangerous insect pest for pine forests, T. pityocampa, ensures the exchange of parasitoids and entomopathogens as biological agents to maintain their population numbers. O. masii and A. bifasciatus are polyphagous parasitoids, so their survival in a specific biotope is not vitally dependent by synchronization of their emergence with the appearance of T. solitaria eggs, but rather by floral diversity which provides an environment for development of their alternative hosts.

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