Pesticides and Beneficial Organisms IOBC/wprs Bulletin Vol. 35, 2008 pp. 44-50

About the presence and abundance of beneficials in overwintering sites of (: ) in peach orchards of northern Greece

Petros Damos and Matilda Savopoulou-Soultani Aristotle University of Thessaloniki, Faculty of Agriculture, Laboratory of Applied Zoology and Parasitology, 54 124, Thessaloniki, Greece, e-mail: [email protected]

Abstract: A report is given about the presence and abundance of beneficials in overwintering sites of Anarsia lineatella Zeller (Lepidoptera, Gelechiidae). The study was conducted in two important regions of peach production in Northern Greece (Veria 40.32oN and Velvendo 40.16oN). For 3 years (2005-2007) hibernacula of overwintering larvae were collected from conventional and IPM peach orchards and transferred to the laboratory in order to ascertain the level and type of beneficial activity. The presence of two Braconid parasitoids was high, causing a significant high larval mortality. In some cases almost 57% of inspected samples were parasitized. In addition, a comprehensive number of beneficial mites were also observed inside the hibernacula. Despite the fact that some of them are not directly linked to the predation of A. lineatella, they had a high presence during the years. Moreover, most of the observed species belonged to the families Phytoseiidae, Pyemotidae and Tydeidae. The observations attest the fact that the overwintering sites of A. lineatella constitute an important microenviroment of beneficial activity. Considering the increasing interest in biological control and that all the above-mentioned beneficials are subjected to mortality induced by pesticides, the different strategies for the control of A. lineatella in Northern Greece peach orchards are discussed.

Key words: Anarsia lineatella, parasitoids, hibernaculum, Braconidae

Introduction

Sustaining biological diversity has become one of the principal goals of conservation and gradually the goals have moved from concern for specifically threatened species to the broader desire to protect different types of ecosystems (Lewis and Whitfield 1999). In particular for agroecosystems, the identification and conservation of native species potentially important as bio-control agents, along with the development of protocols to test side effects of pesticides on non target and beneficial organisms, are considered as a corner stone when enhancing biological control in integrated pest management (IPM) (Carl 1996, Norris et al. 2003). The peach twig borer Anarsia lineatella Zeller (Lepidoptera: Gelechiidae) is one of the major economic pests of stone fruits in the Old and New World (Balachowski and Mesnil 1935, Jones 1935, Summers 1955). In Greece, A. lineatella has 3-4 generations per year (Damos and Savopoulou-Soultani 2007). The species overwinters in bark crevices as 2nd or 3rd instar forming hibernacula. These tiny instars become active in spring and they are able to cause early season injury burrowing into new twigs. Later during summer, new hatched larvae originating from next generations, feed mainly on fruits causing significant injury on yield (Balachowski 1935, Jones 1935, Bailey 1948, Summers 1955, Balachowski 1966).

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In Northern Greece peach production is considered to be essential for economy and during the past few years efforts are made to improve pest control using IPM in order to qualify high standards of products. Moreover, A. lineatella has been increasingly damaging to some peach varieties, and along with the oriental peach Grapholitha molesta (Lepidoptera: Tortricidae), they are key pests for implementation of effective control strategies in terms of IPM (Kyparissoudas 1989, Damos and Savopoulou Soultani 2007, Damos and Savopoulou-Soultani 2008). This study reports the presence and abundance of a number of beneficial species, inside of hibernacula of A. lineatella in IPM and conventional orchards. In addition, the substantial mortality caused by the parasitoids on the overwintering larvae is also recorded. Finally the effects on the abundance and diversity of the observed beneficials are outlined in respect to IPM.

Materials and methods

The faunistic survey was conducted in two important regions of peach production in Northern Greece (Veria 40.32oN and Velvendo 40.16 oN). For 3 years (2005-2007) hibernacula of overwintering larvae were collected randomly from conventional and IPM peach orchards. Commercial orchards (4 plots of 1.5 acre each) were treated according to local pest manage- ment guidelines (all chemical treatments conducted using broad spectrum conventional pesticides), while IPM peach orchards (3 plots of 1.5 acre each) followed pest management practices under the guidelines of public IPM companies’ specialists. Decision making for pesticide application in IPM orchards was based on male moth flight monitoring with pheromone traps (Pherocon®) and degree-days heat accumulation. Environmentally sound pesticides, mostly Bacillus thuringiensis (B.t.) and growth regulators (IGR’s), were used for the IPM orchards. Finally, peach orchards (4 plots of 1 acre each) where no chemical treatment was applied were used as control. Each hibernaculum was considered as a sampling unit and the day of sampling all the collected material was transferred to the laboratory and examined. Each sampling unit was split open under a stereoscope and inspected in order to ascertain the level and type of beneficial activity. Larval mortality caused by parasitoids or predators was also recorded. Data analysis Analysis of variance (ANOVA) was carried out to test the effects of year and management practices on the different dependent variables of abundance. Frequency data were transformed to meet assumptions of normality and variance homogeneity if necessary. Means were compared using the Tukey multiple range test (a = 0.05) (Sokal and Rohlf 1995). Statistics were performed using SPSS 1.14. software (SPSS 2006).

Results

Two parasitoid species were reared from the overwintering larvae of A. lineatella. These species belong to the Braconidae family (Hymenoptera) and caused, in some cases, a significant mortality of A. lineatella larvae.

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Conventional IPM Control

2005

25% 36% 38% 41% 58% 40% 17% 21% 7% 14% 3%

2006 40% 45% 29% 34% 63% 40% 8% 18% 3% 18% 2% 0%

2007 14% 46% 40% 24% 40% 40% 57% 5% 12% 7% 13% 2%

Braconidae Tydeidae

Phytoseiidae Pyemotidae

Fig 1. Relative abundance (proportion) of beneficials inside of hibernacula of A. lineatella in relation to orchard management in Northern Greece (2005, 2006 and 2007).

In addition, the overwintering larval parasitization was especially high during the winter of the year 2006-2007. Moreover, the mortality of A. lineatella, which was due to Braconidae parasitization was significantly higher in the peach orchards, where no chemical treatment was applied (control). Parasitization level was also higher in most of the IPM orchards (10- 23%), when compared with the conventional orchards, where the usual conventional plant protection guidelines were applied (~ 10%) (Table 1). A comprehensive number of predatory mites was recorded inside of the hibernacula. The mite species belong to the Tydeidae, Pyemotidae and Phytoseiidae families. In addition, the mean number of individuals belonging to the Tydeidae family was higher when compared to those of the families Phytoseiidae and Pyemotidae (Table 1).

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Table 1. Hibernacula (n) of overwintering larvae of A. lineatella and corresponding number of beneficials from Conventional, IPM and Control peach Orchards

Beneficial Activity (mean number of individuals) Larval

Orchard Parasiti- Family Manage zation ment

Year (n) df Tydeidae Pyemotidae Phytoseiidae Braconidae (% )

2005 143 3 4 0 2 8 11 a1 Conven- tional 2006 187 3 7 0 0.3 7.4 10 a 2007 141 3 3 1 4 9 21 ab 2005 140 2 5 0 2 7 16 ab IPM 2006 190 2 16.8 0.3 0.6 9 10 ab 2007 140 2 11 0.5 3 10.3 23 b 2005 143 3 12 1 4 12 28 bc Control 2006 145 3 11 2 3 2 57 c 2007 142 3 11 2 3 12 28 bc

1 Percentages followed by the same letter within a column are not significantly different (p<0.05, Tukey HSD test)

The type of orchard management had no effect on the relative diversity of the beneficials that were recorded. During all years and under all different management strategies, beneficials belonging to all the above four families were collected (Fig.1).

Discussion

The lower number of beneficials recorded in the conventional peach orchards contrasted with higher populations of some IPM orchards and indicate that the present orchard pest management practices may interfere with the establishment and diversity of beneficials, although differences were not significant in all cases. A current theory suggests that the highest species diversity should be found in relatively undisturbed to moderate disturbed habitats (Petraitis et al. 1989), but if the disturbance is too severe or too frequent, species may be lost from the community (Lewis and Witfield 1999). Daane et al. (1993), demonstrated that dormant-season sprays with an organophosphate insecticide (diazinon) for the control of A. lineatella leads to a significant decrease on the related parasitoid microfauna. Consequently, the status of a pest in relation to its natural enemies within an agroecosystem is not fixed and it depends on a number of factors, among them type, time and frequency of pesticide treatments (Easterbrook et al. 1985). Braconidae, in general, constitute one of the most species-rich families of , estimated by the taxonomists to have 40-50.000 species worldwide. The vast majority of Braconids are primary parasitoids of other insects, especially of larval stages of Coleoptera, Heteroptera, Diptera and Lepidoptera (Askew 1971). Their natural role as potential biological agents is indisputable because of their ability to keep insect and other populations 48

under control through predation or parasitism (Hanson 1995, Hanson and Gauld 1995, LaSalle and Gauld 1993). Balachowski (1966) referred to a number of Hymenoptera parasitoids of A. lineatella. The species Apanteles emarginatus Nees, A. xanthostigmus Hal. var: anarsiae, Paralitomastix (Encyrtus) variicornis Nees, Paralitomastix (Copidosoma) pyralidis Ashm and Euderus (Secodella) cushmani Crowford, were the most common. In previous studies, Daane et al. (1993) reported the presence of one Braconidae species (unidentified) and also the species Macrocentrus ancylivorus Rowher, Spilochalcis n. sp. aff tovrina (Cresson), Paralitomastix pyralidis (Ashmead), Erynnia totricis (Coquillett) and Euderus cushmani Crawford parasitizing A. lineatella, while Molinari et al. (2005) report three parasitoid species from overwintering A. lineatella larvae, the Ichneumonidae Aethecerus discolor Wesmel, the Braconidae Baeognatha armeniaca Talenga and the Encyrtidae Paralitomastix variicornis Nees, which caused a significant larval mortality. The role of mites (acari) for pest control is discussed in detail by Gerson et al. (2003). On the other hand, a recent survey of the mite fauna in a large number of peach orchards in northern Greece revealed Euseius finlandicus (Acari: Phytoseiidae) as the dominant predatory species. Moreover, the overwintering Phytoseiidae females were mostly found in bark crevices of the hibernation cocoons of the peach moth Adoxophyes orana (Lepidoptera: Tortricidae) (Broufas et al. 2002). This study reveals that mite fauna expansion occurs also inside the hibernacula of A. lineatella. Furthemore, in some cases a limited number of Pyemotidae individuals was also recorded. The species most commonly referred to in bibliography is Pyemotes tritici which parasitizes about 150 insect species and P. ventricosus (Cross et al. 1975). Finally, Tydeids are very common and fast moving inhabitants of plant and soil, where they subsist on many plant and foods. Some species like Proctotydeus spp. live on insects (Kaźmierski 1998) and some other proved to be important in suppressing Eriophyiidae species (Hessein and Pering 1986). However, the nature of the relationship of these species with plant or insect hosts is still unclear (Gerson 2003). In northern Greece, the implementation of IPM in peach orchards has made a number of advances. Automatic data and monitoring systems have been installed in most representative regions. Phenological models are already developed and applied for the control of A. orana (Milonas and Savopoulou-Soultani 2000, Milonas and Savopoulou-Soultani 2006). Moreover, reliable intervention thresholds are established for A. lineatella and species can be successfully managed in terms of IPM using both monitoring and degree-days as a decision tool for targeting a particular developmental stage (Damos and Savopoulou-Soultani 2007). If proper time application is achieved, environmentally sound insecticides such as diflubezuron and Bacilus thuringiensis are applied, with high success and resulting in a significant decrease in the total number of sprays. In contrast, pest control in conventional peach orchards depends on the phenological stage of the peach-host. As a result, in most cases, preventive chemical treatments are applied without evident necessity. However, peach growers face difficulties in practice when trying to apply alternatives. Firstly, because of the near absence of registered narrow-spectrum substances in the market. Thus, most of the pesticides used are toxic or very persistent and do not fulfil the requirements in order to be used in integrated fruit production (Cross and Dickler 1994, Malavolta et al. 2003, Milonas and Savopoulou-Soultani 2000, Milonas and Savopoulou- Soultani 2006). Secondly, specific environmental conditions in Greece (e.g. prolonged high mean temperatures and relative humidity during the spring and summer season) as well as pesticide resistance, can cause pest population outbreaks. Thus, pest populations outbreaks are very difficult to be controlled without the use of conventional broad-spectrum pesticides (Cravedi and Jörg 1995, Cravedi 2000). As a result, the natural enemies action can be 49

disrupted extensively also in IPM orchards as well and this trend could explain the low number of beneficials that were observed during the field trial in some cases of IPM orchards. Moreover, the peach production landscape constitutes a mosaic of IPM and conventional orchards, where it is difficult to establish long scale IPM strategies. Finally, it is noticeable that in some cases evaluating the action of natural enemies is difficult, uncertain and demonstrating little practical relevance (Cravedi 2000). However, it is part of IPM aims to shift the system progressively from reliance on chemical control to reliance mostly on biological control. Additionally, species that appear as well established indigenous predators in the fruit growing areas of northern Greece should be brought in as potential biocontrol agents.

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