Thaumetopoea Pityocampa) in Bulgaria

Silva Balcanica, 19(1)/2018

FECUNDITY AND EGG ABORTION in two PHENOLOGICAL forms of pine processionary moth (Thaumetopoea pityocampa) in Bulgaria

Margarita Georgieva1, Lilia Bocheva2, Plamen Mirchev1, Georgi Tsankov1, Maria Matova1, Gergana Zaemdzhikova1, Sianna Hlebarska1, Georgi Georgiev1 1Forest Research Institute – Sofia Bulgarian Academy of Sciences 2National Institute of Meteorology and Hydrology – Sofia Bulgarian Academy of Sciences

Abstract

During the period 1991-2017, the fecundity and egg abortion of pine processionary moth (Thaumetopoea pityocampa) were studied in the region of Sandanski (Southwest Bulgaria) and Kirkovo (the Eastern Rhodopes) where two different phenological forms occur. In the region of Sandanski, a typical Mediterranean winter form develops, and in the region of Kirkovo – an early developing summer form. For the entire study period, 766 batches containing 174 132 eggs were collected and analyzed. Both areas are characterized by dry and hot summer. In Sandanski, the number of days with temperatures above 32°C (critical for eggs incubation) in June-August was twice as much as in the region of Kirkovo. In Sandanski, the period of consecutive days with maximum air temperature ≥32°C in some years lasted between 38 and 43 days. In Kirkovo, the average number of consecutive days with such high temperature was 10-12, only in 1998 it was 21 and in 2016 – 20 days. There was a similarity in the average fecundity of pine processionary moth females in Sandanski and Kirkovo (239.9 and 216.3 eggs, respectively). In egg stage, mortality as a result of abortion was significant – 40.4% in Sandanski and 37.0% in Kirkovo. Key words: Thaumetopoea pityocampa, phenological forms, fecundity, egg abortion, Bulgaria

INTRODUCTION

Pine processionary moth (PPM), Thaumetopoea pityocampa (Den. & Schiff.) (Lepidoptera: Notodontidae) is the most harmful pest defoliator of pine forests in Bulgaria (Mirchev et al., 2003), and in the countries of the Mediterranean region (Devkota, Schmidt, 1990; Masutti, Battisti, 1990; Alsamara et al., 2014, etc.). In addition to defoliating harmful effect, the urticating hairs of PPM’s caterpillars cause strong allergic reactions on skin of humans and animals, dermatitis and other severe reactions (Lamy, 1990). An expansion of the pest has been occurred in Bulgaria over the past decades (Mirchev al., 2011). Air temperature is one of the most important factors determining PPM’s distribution. Mild winters have a favourable effect on both the caterpillars’ development and growth, and reflect on higher females’ fecundity (Tiberi et al., 2015).

79 The temperature below -16°C is lethal for overwintering caterpillars (Démolin, 1969). High summer temperatures have also a crucial impact on PPM’s survival. Temperatures above 32°C are extremely dangerous for its egg incubation (Huchon, Demolin, 1970). Robinet et al. (2013) suggest that the upper temperature threshold for PPM’s survival is much higher than 32°C. According their study, its eggs masses could survive at temperatures of 40°C for several days, assuming that it could be a result of species’ adaptation to the climate warming. In Bulgaria, two different phenological forms of PPM, based on the timing of larval development, occur (Tsankov et al., 1996b). In the region of Sandanski – a typical Mediterranean winter form is distributed, and in the region of Kirkovo – an early developing summer form. Bulgaria is located in the South-eastern Europe and has unusually various climate conditions due to the influence of strongly different continental and Mediterranean climates, and diverse landscape. The climate has four distinct seasons and varies with altitude and location. According to the accepted in the National Institute of Meteorology and Hydrology (NIMH) – Bulgarian Academy of Sciences climate classification (Sabev, Stanev, 1959), the territory of Bulgaria is divided into two main climatic areas (European-Continental and Continental-Mediterranean), four climatic subareas (Moderate-Continental, Transition-Continental, South-Bulgarian and Black-Sea), and twenty-five climatic regions, which include the corresponding coastal and mountainous zones. Bulgarian mountains and valleys act as barriers or channels for air masses, causing sharp contrasts in weather over relatively short distances. The aim of present study is to compare data of the most important indicators determining the development of PPM in two different phenological forms: fecundity of female moths and egg stage survival as relative share of successfully hatched caterpillars, based on the long-term experimental material collected from the regions of Sandanski and Kirkovo.

MATERIALS AND METHODS

Studied areas and biological material During the period 1991-2017, in the region of Sandanski (Southwest Bulgaria) and Kirkovo (the Eastern Rhodopes) (Fig. 1), a total number of 766 egg batches of Thaumetopoea pityocampa were collected on Pinus nigra trees after caterpillars’ hatching. In the first region, 359 egg batches were collected in the outskirts of the town (293 m a.s.l.) and Marikostinovo vill. (86 m), located 15 km south of Sandanski (Table 1). For the second region, 407 egg batches were collected on the land of ten villages, situated between 400 and 600 m within a distance of 12 km (Table 1). The scaleless and analysis of egg batches are described in details in Tsankov et al. (1996a). Climate characteristic of Sandanski and Kirkovo regions Sandanski and Kirkovo belong to South-Bulgarian subarea of the Continental- Mediterranean climate area, but to different climatic regions with very specific

80 E of Greenwich 23 24 25 26 27 28

ROMANIA

44 44 e r

D a n u b e R i v

43 N 43

Black

Sea

42 O

E E Y C K

R 50 km

A Sandanski U T

M Kirkovo G R E E C E

23 24 25 26 27 28

Fig. 1. Studied localities

Table 1. Main characteristics of sample plots

Site Geographical coordinates (N, E) Altitude, m a.s.l. Sandanski Region Town of Sandanski 23º17’14’’ 41º34’20’’ 293 Marikostinovo vill. 23º18’55’’ 41º26’20’’ 86 Kirkovo Region Yanino vill. 25º17’30’’ 41º23’41’’ 411 Dyulitsa vill. 25º19’30’’ 41º22’31’’ 400 Medevtsi vill. 25º19’03’’ 41º22’27’’ 400 Kayaloba vill. 25º11’32’’ 41º21’54’’ 500 Drangovo vill. 25º15’27’’ 41º18’45’’ 650 Dzherovo vill. 25º17’53’’ 41º18’49’’ 450 Domishte vill. 25º22’09’’ 41º21’14’’ 430 Dobromirtsi vill. 25º12’05’’ 41º23’22’’ 450 Dolno Kapinovo vill. 25º17’35’’ 41º17’14’’ 450 Yakovitsa vill. 25º15’41’’ 41º18’35’’ 600

81 characteristics (Sabev, Stanev, 1959). The main features are mild and very humid winter and sunny, hot and dry summer. During the second half of the autumn (November) or in the beginning of winter (December) maximum of precipitation sums is observed – about 2.5-3 times more than in August or September. The summer is characterized by dry, hot weather – the most pronounced in the southwest (valley of Struma River), with average July temperatures 23-25°C. The driest month for this area is August or September in some parts of the East Rhodopes. Sandanski is located in Petrichko-Sandanski climatic region, which geographically includes Struma valley southerly from Simitli. It is surrounded to the east by Pirin, and to the west by Vlahina, Maleshevska and Ograzhden Mountains. The area is surrounded from the north by mountains and Kresna Gorge is very narrow – all this represent effective protection against cold air masses invasion, especially from northeast. That is why this area, with its small altitude, (average between 100 and 300 m) is the warmest one in the country. Kirkovo belongs to climate region which covers the East Rhodopes river valleys and the relatively lower hills separating them to the east of Maritsa valley to the south of Harmanliyska River. Compared to the valleys of Struma, it is considerably less protected from influence of cold air masses. The area has an altitude of 50 to 400 m and is relatively closer to the Aegean Sea. Winter here is also relatively mild, with average January temperatures above 0°C. But after the invasion of cold front from the north followed by an anti-cyclonic synoptic situation, the air temperatures in the area fall down rapidly. Orography of the area favours the retention of cold air masses and further fall of temperatures. Under such conditions, minimum temperatures in the lower parts of the area are sometimes from -10 to -12°C, and in some cases -24 ÷ -26°C. In the same time in Petrichko-Sandanski climatic region the minimum temperatures fall to -8 ÷ -9°C and in extremely cold weather can drop to -18 ÷ -19°C. The climate analysis of summer temperature for Sandanski and Kirkovo regions is based on data from NIMH for the period 1991-2017. Statistical analysis The statistical analysis of obtained data was carried out by MS Excel 2013 and Statistica 12 for Windows programs.

RESULTS

Comparative climate analysis for Sandanski and Kirkovo Both studied regions are characterized by dry and hot summer, but the weather in Sandanski is relatively warmer and drier than in Kirkovo. The highest mean monthly maximum temperatures were observed in August as well as the absolute maximum of temperature for both places was measured in July, according to meteorological data for the period 1991-2017. For the same period, the number of days with maximum air temperature ≥32°C (critical for PPM eggs and larval evolution) was calculated for

82 Table 2. Fecundity and egg abortion of winter form of T. pityiocampa from Sandanski region

Sample Fecundity Egg abortion

ear Percent Y Number of Total number M±SD Rang Number egg batches of eggs Average Rang

1991 89 21 614 242.9±45.0 68–308 10111 46.8 1.9–95.1

1992 58 14 077 242.7±47.6 69–315 8242 58.5 3.5–100

1994 37 8296 224.2±41.8 108–327 4879 58.8 1.8–100

1995 87 21 569 247.9±39.6 136–331 6231 29.0 0.4–100

1996 46 10 856 236.0±35.4 173–325 3375 31.1 0.4–88.2

1997 19 4546 239.3±36.7 168–312 446 9.8 0.6–24.5

2017 23 5161 224.4±40.9 105–284 1495 29.0 0.9–88.2

∑ 359 86 119 239.9±42.3 68–331 34779 40.4 0.4–100

Table 3. Fecundity and egg abortion of summer form of T. pityiocampa from Kirkovo region

Sample Fecundity Egg abortion

ear Percent Y Number of Total number M±SD Rang Number egg batches of eggs Average Rang

1994 30 6004 200.1±47.7 34–296 1845 30.7 0.8–98.9

1995 37 7488 202.4±38.4 58–256 2314 30.9 3.2–76.9

2013 6 1170 195.0±52.9 135–257 538 46.0 22.1–89.1

2016 137 30 404 221.9±40.9 104–306 9730 32.0 0.0–100

2017 197 42 947 218.0±38.3 75–299 18126 42.2 0.0–98.9

∑ 407 88 013 216.3±40.6 34–306 32553 37.0 0.0–100 summer months. The mean monthly number of days corresponding to these temperature conditions was 4 in June, 12 in July and 14 in August for Kirkovo, and 11 in June, 21 in July and 22 in August for Sandanski. In Sandanski, the highest number of consecutive days with maximum air temperature ≥32°C was 43 in 2012 (between 29 June and 10 August), followed by 41 in 2015, and 38 in 1998 and 2013. In this region, 15-20 consecutive days with such

83 temperature occur very often. In the same time in Kirkovo the maximum number of consecutive days with maximum air temperature ≥ 32°C was 21 in 2016 (between 22 July and 11 August) and there was only one year (1998) with 20. The normal seasonal number of consecutive days with such high temperature for Kirkovo is 10-12. Fecundity of PPM For the entire study period, 174 132 eggs of PPM were collected and analysed. The average number of eggs laid in batches in the region of Sandanski was 239.9 (Table 2), and in the region of Kirkovo – 216.3 (Table 3). However, the statistical analysis of PPM fecundity shows similarity in both studied areas (t-values for Kirkovo and Sandanski 107.4063 and 107.4056, respectively). The higher average fecundity rate in Sandanski region is not statistically proved (p=0.00). The obtained data on female fecundity demonstrate large fluctuations in the number of eggs per egg batch in both regions. For Sandanski it varies between 68 and 331 eggs/batch (Table 2), and for Kirkovo – between 34 and 306 eggs/batch (Table 3). Egg abortion of PPM A significant reduction of PPM population at the egg stage was established in both regions – 40.4% in Sandanski (Table 2), and 37.0% in Kirkovo (Table 3). The difference between the highest and the lowest value in Kirkovo region was 15.1. In Sandanski, however, a significant dispersion was observed – the difference between the highest and the lowest value was 49.0, i.e. 3.2 times higher than in Kirkovo. The mortality in individual egg batches was quite variable – between 0 and 100%. An exception was obtained in Kirkovo in 2013 (between 22.1 and 89.1%) when only six egg batches were studied. The average valueof aborted PPM eggs from Sandanski region (88.73) is higher compared to Kirkovo (75.34) (Fig. 2). The difference is statistically proven (p <0.01). In Kirkovo there was much greater homogeneity around the average egg mortality (Std. Dev.=14.65) compared to Sandanski (Std.Dev.=42.18).

DISCUSSION

The females of T. pityocampa usually lay only one egg batch (Douma-Petridou, 1990), so the number of eggs in batches corresponds to the real fecundity of the species in a different area. The established PPM fecundity is not a constant value in the studied regions. Mirchev (2005) noted that it depends both on the variety of environmental factors and the population density of a year. Studies of Carvalho et al. (1999) and Moura et al. (1999) showed that the biochemical composition of the host plant is a significant factor influencing the density of PPM population. Devkota, Schmidt (1990) observed the effects of different pines on the development and mortality of newly hatched larvae fed on 13 different species of pines and on one species of larch (Larix kaempferi), and found that the host plant affects the survival, pupal weight and cavity diapause. Lower

84 Fig. 2. Average egg abortion egg production occurs when the PPM’s larvae are fed on Pinus brutia compared to P. nigra, P. sylvestris and P. halepensis (Mirchev, 2005). This factor has been overcome in present study because the host plant in both studied areas was P. nigra. Özkazans (1987) reported for growth in PPM egg production with the increase in the altitude of its habitats. Mirchev (2005) concludeed that the fecundity of PPM is higher in the northern regions of its range in Bulgaria. Pimentel et al. (2010) came to the same inference that the fecundity grows with the latitude increasing. A significant difference in PPM fecundity was recorded in Marikostinovo with an average number of eggs of 241 pcs, compared to 161 in Achaia region (Peloponnese Peninsula, Greece) (Tsankov et al., 1997). For these two sites, apart from the differences in latitude, there were also differences in food plants – P. nigra in Bulgaria, and P. halepensis in Greece. In Algeria, Tsankov et al. (1995) reported an average number of 154 eggs, in Morocco – 175 (Schmidt et al., 1997), in Portugal – 183 (Mirchev, Tsankov, 2000). In Turkey, only one of four samples had more than 200 eggs, while in Bulgaria, the average egg number was more than 200 in 21 of 22 samples (Mirchev, 2005). Zamoum et al. (2015) found that low fecundity of PPM is typical for the habitats in the Mediterranean area in Algeria, which is growing southwards, up the country. However, Santos et al. (2015) did not establish a significant correlation between the average number of eggs per batch and the latitude. For the typical winter phenological PPM form, in which caterpillars develop mainly during the winter months, the egg production is directly dependent on the temperature regime. Mild winters facilitated larval feeding in the overwintering phase, so that the larvae reached maturity faster, and with substantial energy reserves to be spent on egg production

85 (Tiberi et al., 2015; Marcalas, 1989). These findings are not confirmed by our study. In the region of Kirkovo, the caterpillars develop in a climatic environment, avoiding the low winter temperatures that gives it a sufficient number of days favourable for its development. However, these conditions do not automatically lead to increase the fecundity compared to the second phenological form. In September 2017, the caterpillars in Sandanski were in the begging of their hatching, whereas in the region of Kirkovo, they were already in fifth instar with almost completed development following the classical life cycle (Mirchev et al., 2018). In the same period, on Thassos Island, Greece, the development of PPM caterpillars was similar with that observed in Sandanski region (Georgieva et al., unpublished). The detected differences in PPM phenology in Bulgaria confirm the suggestions that two clearly distinguishable phonological forms occur through the country. The studies of Huchon, Demolin (1970) and Robinet et al. (2013) proved that air temperature is a prerequisite for PPM survival in egg stage, as well as for forming new phenological forms. The climatic characteristics of the two studied regions show that in Kirkovo the summer is with moderately high temperatures and rarely overcome the threshold (32°C) that limits the development of PPM. The average relative share of aborted eggs in this region is lower than in Sandanski, if only by 3.4 points. Although the days with high summer temperatures above this threshold were rarely recorded, they occurred in some years and indirectly confirmed the conclusion of Robinet et al. (2013) that the temperature threshold is higher than 32°C. Aborted eggs could be classified into several groups: dead, unhatched embryos; sterile, non-fecundity eggs; empty eggs; parasitized eggs and such destroyed by predators (Mirchev, 2005). For the region of Kirkovo, the parasitoids had the most significant impact on PPM number in egg stage for the generations in 1994 and 1995. The number of parasitized eggs was frequentative higher compared with the aborted eggs from among the other three groups. Five primary parasitoids were reared from host eggs, Ooencyrtus pityocampae (Mercet) (Hymenoptera: Encyrtidae), Baryscapus servadeii (Dom.) – dominant species, Pediobius bruchicida (Rondani) (Hymenoptera: Eulophidae), Anastatus bifasciatus (Fonsc.) (Hymenoptera: Eupelmidae), Trichogramma embryophagum Htg. (Hymenoptera: Trichogrammatidae), and one hyperparasitoid, Baryscapus transversalis Graham (Hymenoptera: Eulophidae) (Mirchev et al., 1998). In Sandanski region, the most significant difference was observed at the share of the parasitized eggs. In addition to the mentioned above species, another polyphagе, Eupelmus vesicularis (Retz.) (Hymenoptera: Eupelmidae) was established as egg parasitoid of PPM (Mirchev, 2005). The main considerable difference between the two studied regions is the strange fact that O. pityocampae was the dominant parasitoid in the region of Sandanski. Masutti (1964) pointed that the species from Eulophidae family are more plastic and develop in regions with temperatures above 30°C – conditions that difficult the development of O. pityocampae. In the region of Sandanski in some years (1992 and 1994), a high proportion of non-fertilized, sterile eggs of PPM was registered (Tsankov et al., 1997). The reasons for that value have not cleared yet, but it is known that the number of non-fertilized eggs of 86 gypsy moth, Lymantria dispar (L.) (Lepidoptera: Erebidae) grows with increasing age of copulating individuals (Tobin et al., 2014). The comparison of results for PPM fecundity and aborted eggs in Sandanski and Kirkovo indicates no significant difference between studied regions. The caterpillars from Kirkovo develop in favourable temperature conditions, reach maturity more quickly and with higher reserves of energy, but these factors do not increase the rate of fecundity. In the same area, the earlier appearance of eggs in the summer did not increase the proportion of aborted eggs.

Acknowledgements: This study was supported by the project ‘Expansion of pine processionary moth (Thaumetopoea pityocampa (Denis et Schiffermüller, 1775) (Lepidoptera: Thaumetopoeidae) in Bulgaria – a dangerous allergen and economically important pest in the pine ecosystems’ funded by the National Scientific Fund (DN01/17, 22.12.2016).

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