THE INFLUENCE OF CULTIVAR AND NATURAL ENEMIES ON RASPBERRY BEETLE (Byturus tomentosus De Geer)

SORDI JA LOODUSLIKE VAENLASTE MÕJU VAARIKAMARDIKALE (Byturus tomentosus De Geer)

LIINA ARUS

A Thesis for applying for the degree of Doctor of Philosophy in Entomology

Väitekiri filosoofiadoktori kraadi taotlemiseks entomoloogia erialal

Tartu 2013

EESTI MAAÜLIKOOL ESTONIAN UNIVERSITY OF LIFE SCIENCES

THE INFLUENCE OF CULTIVAR AND NATURAL ENEMIES ON RASPBERRY BEETLE (Byturus tomentosus De Geer)

SORDI JA LOODUSLIKE VAENLASTE MÕJU VAARIKAMARDIKALE (Byturus tomentosus De Geer)

LIINA ARUS

A Th esis for applying for the degree of Doctor of Philosophy in Entomology

Väitekiri fi losoofi adoktori kraadi taotlemiseks entomoloogia erialal

Tartu 2013 Institute of Agricultural and Environmental Sciences Estonian University of Life Sciences

According to verdict No 149 of August 28, 2013, the Doctoral Commitee of Agricultural and Natural Sciences of the Estonian University of Life Sciences has accepted the thesis for the defence of the degree of Doctor of Philosophy in Entomology.

Opponent: Prof. Inara Turka Latvia University of Agriculture Jelgava, Latvia

Supervisor: Prof. Emer. Anne Luik Estonian University of Life Sciences

Defense of the thesis: Estonian University of Life Sciences, Karl Ernst von Baer house, Veski st. 4, Tartu on October 4, 2013 at 11.00

The English language was edited by PhD Ingrid Williams. The Estonian language was edited by PhD Luule Metspalu.

Publication of the thesis is supported by the Estonian University of Life Sciences and by the Doctoral School of Earth Sciences and Ecology created under the auspices of European Social Fund.

© Liina Arus, 2013 ISBN 978-9949-484-93-5 (trükis) ISBN 978-9949-484-94-2 (pdf) CONTENTS

LIST OF ORIGINAL PUBLICATIONS ...... 7 ABBREVIATIONS ...... 9 1. INTRODUCTION ...... 10 2. REVIEW OF THE LITERATURE ...... 13 2.1. Raspberry beetle: biology and cultivar preference ...... 13 2.2. Raspberry beetle’s natural enemies ...... 14 2.3. Eff ects of cultivation technologies on the pests and their natural enemies ...... 17 3. HYPOTHESES AND AIMS OF THE STUDY ...... 19 4. MATERIALS AND METHODS ...... 20 4.1. Descriptions and design of the experimental areas ...... 20 4.1.1. Data collection in fi eld experiments ...... 23 4.1.2. Weather conditions ...... 24 4.2. Laboratory feeding experiment (IV) ...... 24 4.3. Statistical data analyses ...... 25 5. RESULTS ...... 27 5.1. Th e impact of cultivars (I) and mulching on raspberry beetle damage ...... 27 5.2. Th e carabids species composition and abundance; impact of cultivation technologies (II, III) ...... 28 5.3. Laboratory feeding experiment with carabids (IV) ...... 34 5.4. Th e impact of intercropping on the parasitisation level of raspberry beetle larvae (V) ...... 34 6. DISCUSSION ...... 36 6.1. Th e impact of raspberry cultivars and mulches on the raspberry beetle damage ...... 36 6.2. Th e infl uence of cultivation technologies on the natural enemies of raspberry beetle ...... 38 CONCLUSIONS ...... 42 SUMMARY IN ESTONIAN ...... 44 REFERENCES ...... 48 ACKNOWLEDGEMENTS ...... 61

5 ORIGINAL PUBLICATIONS...... 63 CURRICULUM VITAE ...... 109 ELULOOKIRJELDUS ...... 112 LIST OF PUBLICATIONS ...... 115

6 LIST OF ORIGINAL PUBLICATIONS

This thesis is a summary of the following papers, which are referred to by Roman numerals in the text. The papers are reproduced with due permission from the publishers of the following journals: Acta Agriculturae Scandinavica (III), Žemdirbystė/Agriculture (IV) and Agronomy Research (V).

I. Arus, L., Kikas, A., Kaldmäe, H., Kahu, K. and Luik, A. 2013. Damage by raspberry beetle (Byturus tomentosus De Geer) in different raspberry cultivars. (Accepted by Biological Agriculture and Horticulture).

II. Luik, A., Tarang, T., Veroman, E., Kikas, A. and Hanni, L. 2002. Carabids in the Estonian crops. In Proceedings of the scientifi cs international conference „Plant protection in the Baltic region in the context of integration to EU“, Kaunas, Lithuania Sept. 26-27. 2002: 68–71.

III. Arus, L., Luik, A., Monikainen, M. and Kikas, A. 2011. Does mulching infl uence potential predators of raspberry beetle? Acta Agriculturae Scandinavica, Section B - Plant Soil Science 61(3): 220–227.

IV. Arus, L., Kikas, A. and Luik, A. 2012. Carabidae as natural enemies of the raspberry beetle (Byturus tomentosus F.). Žemdirbystė/Agriculture 99(3): 327–332.

V. Hanni, L. and Luik, A. 2006. Parasitism of raspberry beetle (Byturus tomentosus F.) larvae in different cropping techniques of red raspberry. Agronomy Research 4 (special issue): 187–190.

7 The contribution of the author to the papers: Paper I II III IV V Idea and design LA, AL AL LA, AL LA, AL LA, AL Data collection LA, KK TT, EV, AK, LA LA, MM LA LA Data analysis LA All LA, MM LA LA Manuscript preparation All All LA, AL, AK All All

LA − Liina Arus; AL − Anne Luik; AK − Ave Kikas; KK − Kersti Kahu; MM − Martin Monikainen; TT − Tiiu Tarang; EV − Eve Veromann; All − all authors of the paper.

8 ABBREVIATIONS

ANOVA analysis of variance BP black plastic mulch cv. (cvs.) cultivar(s) LSD least signifi cant difference ns not signifi cant (statistics) p probability (statistics) PM peat mulch r correlation coeffi cient RB raspberry beetle SD standard deviation (statistics) SDM sawdust mulch SE standard error (statistics) SM straw mulch WM without mulching

9 1. INTRODUCTION

Raspberry (Rubus idaeus L.) is the most widely grown top fruit crop of all Rubus species throughout the world; most production is concentrated in northern and central Europe (Gordon et al., 1997; Graham and Jennings, 2009). According to Statistics Estonia, the cultivation area of small fruits has decreased during the last decade, with only 150 hectares of raspberries grown in 2012 in Estonia; however, at the same time on data of the Estonian Agricultural Board the organically-grown raspberry area has increased to about 27 hectares. Insuffi cient winter hardiness is the most essential factor reducing raspberry yield in Nordic conditions (Dénes and Kollányi, 1999; Kikas et al., 2002; Libek and Hanni, 2003; Arus et al., 2008a; Strautina et al., 2012; Arus and Libek, 2013) but also the abundance of diseases and pests. Pest regulation methods are still under-developed for environmentally-friendly fruit production (Gordon et al., 1997; Vétek et al., 2008).

Many growers of organic raspberry have large losses in yield and reduced quality of their products because of insect damage. The dominant pest – the raspberry beetle (RB) (Byturus tomentosus De Geer) (Coleoptera; Byturidae), affects raspberry yield as well as fruit quality (Birch et al., 2004). Most consumers and high quality producers have zero tolerance of larval contamination and fruit injury. Damaged fruits can also become infected by grey mould (Botrytis cinerea Pers.) thus further reducing their storage quality (Woodford et al., 2002).

The occurrence of the pest is dependent on the genetic properties of cultivars, natural enemies and cultivation technologies. In conventional production, control of RB generally relies on synthetic chemical insecticides, often sprayed prophylactically (Gordon et al., 1997; Gordon, 2008; Linder et al., 2011). This pollutes the environment and also kills the natural enemies of the pests. Sublethal doses of residues in nectar and pollen can cause physiological dysfunctions in bees, parasitoids and predators (Gels et al., 2002; Ramirez-Romero et al., 2005; Rogers et al., 2007; Peusens and Gobin, 2008; Mänd et al., 2010). Decreased pesticide use positively affects coccinellids, syrphid larvae and spider communities (Schumacher and Freier, 2008; Volkmar et al., 2008), while also improving the quality, including antioxidant activity, of the fruits (Worthington, 2001; Asami et al., 2003; Olsson et al., 2006; Wang et al., 2008; Tõnutare

10 et al., 2009; Reganold et al., 2010) thereby having a positive impact on human health (Rembiałkowska and Średnicka, 2009).

Raspberry cultivars from northern, central and southern Europe differ in morphological, phenological and biochemical properties (Finn and Hancock, 2008; Graham and Jennings, 2009). They can be different in susceptibility to the RB. Finding cultivars less susceptible to RB gives additional possibilities of keeping damage at a lower level, thereby reducing the need for chemical control of RB.

In environmentally-friendly raspberry production the use of less susceptible cultivars to RB could be combined with volatile-enhanced white sticky traps. The latter are an alternative method of controlling RB (Woodford et al., 2003; Schmid et al., 2006; Baroffi o et al., 2011). But one problem is that, in areas with wild raspberries, the traps are less attractive and do not work effectively probably due to high immigration rates from surrounding wild raspberry during fl owering (Trandem et al., 2008; Baroffi o et al., 2012). Raspberry is a common plant in Estonian and Northern hardwood forests (Hoegberg et al., 1990; Moora et al., 2007). Therefore additional measures need to be developed for RB control.

The role of natural enemies in regulating populations of raspberry pests has been little studied (Scanabissi and Arzone, 1992; Vétek et al., 2006, 2008). There are no data about the role of natural enemies in RB population regulation. Raspberry plants with their perennial roots and biennial canes may be kept for over 10 years. Long-term plantations are thus particularly suitable for local populations of predatory arthropods as well as permitting pests to increase over several years (Desender et al., 1994). In plantations, arthropod communities are dependent on the cultivation system (Kromp, 1999). The enemies’ hypothesis states that predatory and parasitoid insects are more effective in controlling populations of herbivores in diverse systems than in simple ones (Russel, 1989; Landis et al., 2000). In RB population regulation the role of natural enemies should also not be neglected. It is important to investigate which are the key enemies of RB and how to promote them with cultivation technologies.

For further development of environmentally-friendly crop management strategies of raspberry it is important to fi nd less susceptible cultivars

11 and maximise the biocontrol of RB by promotion of natural enemies.

The present study is focused on the susceptibility of raspberry cultivars to RB and on its natural enemies depending on cultivation technologies.

12 2. REVIEW OF THE LITERATURE

2.1. Raspberry beetle: biology and cultivar preference

A wide range of insects and other arthropod pests can reduce yield and fruit quality in raspberry (R. idaeus) (Gordon et al., 1997; Gordon and Williamson, 2004; Gordon, 2008; Stamenković et al., 2010). The genetic properties of cultivars are among the factors infl uencing susceptibility to pests (Gordon et al., 1997; Milencovic and Stanislavljevic, 2003; Vétek and Pénzes, 2008).

The dominant pest of raspberry in Europe is the raspberry beetle, B. tomentosus. Although it can be found in most raspberry-growing regions in Europe extending into Asia, RB is more numerous in western and northern Europe (Gordon et al., 1997; Birch et al., 2004). Adults RB feed and mate in raspberry, eating the leaves, fl ower buds and pollen. The females lay their eggs in fl owers or developing fruits. The larvae cause the most damage, fi rst gnawing the base of the receptacle and then digging galleries in the developing fruit (Gordon et al., 1997; Willmer et al., 1998; Gordon and Williamson, 2004). This results in fruit discolouration and contamination, and leads to the rejection or down-grading of the crop (Taylor and Gordon, 1975). Antonin (1984) established that one female RB adult lays usually one egg per fl ower, up to 120 eggs in total. It allows the conclusion that the larger amount of damaged fruits correlates with a bigger abundance of RB. Up to 50% of fruits damaged by RB have been found in some plantations (Tuovinen, 1997; Woodford et al., 2000; Hanni and Luik, 2001; Kikas et al., 2002; Woodford et al., 2003). On the one hand, the beetles fl ying activity should correlate with the fl owering period of raspberry cultivars; on the other hand, oviposition sites depend on cultivars fl oral morphological and biochemical properties. In choosing suitable oviposition sites, RB use visual and olfactory cues. They locate raspberry fl owers through response to their volatile profi le (Birch et al., 1996; Woodford et al., 2003). This (Woodford et al., 2003), as well as their production of nectar, varies with the phenological age of the fl owers (Willmer et al., 1998) conveying additional information to female beetles (Robertson et al., 1995). Raspberry fl owers are notable for the profusion of their nectar secretion and there are signifi cant differences between cultivars (Willmer et al., 1994; Schmidt et al., 2012).

13 The nectar attracts the beetles and Willmer et al. (1998) showed that its production is a factor limiting oviposition by the beetles.

Several wild Rubus species - R. coreanus Miq., R. crataegifolius Bunge, R. occidentalis L. and R. phoenicolasius Maxim. have been considered as resistant to raspberry beetle (Keep, 1976; Keep et al., 1980; Briggs et al., 1982; Finn and Hancock, 2008). Their derivates and the purple raspberry cultivar ‘Glen Coe’ (Jennings et al., 2003) and also primocane raspberry cultivars (Jennings et al., 1991) have all shown some level of resistance to larval damage. But it became evident that damage is absent because the beetle oviposition period does not coincide with the fl owering time of these primocane cultivars (Vétek et al., 2008). Therefore it is not cultivar resistance to the RB, but mainly phenological isolation between beetle oviposition and the fl owering period of primocane raspberries.

2.2. Raspberry beetle’s natural enemies

Phytophagous fauna are regulated by polyphagous predators, parasitoids and spiders, which depend on food resources and microclimatic conditions; they are usually abundant in fi elds where more nature- friendly growing technologies are used (Sunderland, 1975; Sunderland and Vickerman, 1980; Bryan and Wratten, 1984; Finch and Elliott, 1992; Kromp, 1999; Nõmmiste and Luik, 1999; Luik et al., 2000; Tuovinen and Tolonen, 2002).

Entomophagous fauna has been little studied in raspberry plantations. Due to their hidden lifestyle, RB larvae are quite safe from predatory and parasitoid arthropods. But, at one stage, the larvae are directly threatened by natural enemies. After a feeding period in the fruits, RB larvae fall to the soil for pupation and are then possible targets for natural enemies.

The introduction of ground-living predators and parasitoids to managed ecosystems has been suggested as a strategy for controlling insect pests (Price et al., 1980).

Predators Raspberry plantations are longterm and so particularly suitable for local populations of predatory arthropods (Levesque and Levesque, 1994; Barone and Frank, 2003) and thereby increase ecological stability in agroecosystems.

14 Of the ground-living predators, carabids are effective in regulating several pest populations (Hokkanen and Holopainen, 1986; Kromp, 1999; Büchs, 2003). They are abundant in agricultural fi elds all over the world, forming a predominant part of overground agrocoenosis (Tischler, 1980).

Carabids of the genera Pterostichus, Harpalus, Bembidium and Agonum, are common in European (Lövei and Sunderland, 1996; Helenius et al., 2001), including Estonian (Luik et al., 2005), agricultural fi elds and plantations. From these carabids, most species of the genus Pterostichus are nocturnal, highly polyphagous predators, consuming chiefl y animal food (Thiele, 1977; Lindroth, 1992) but also seeds, their diet being dependent on season (Pollet and Desender, 1985; Goldschmidt and Toft, 1997). For example, the intestines of Pterostichus cupreus L. contained 67% plant material in spring, but, at the end of summer insect material dominated (80%) (Thiele, 1977). This is apparently infl uenced by the greater availability of insects as a food source in summer.

It has been found that Pterostichus spp. consumed the blueberry pest, winter moth, Operopthera brumata L., pupae (Horgan and Myers, 2004) and the activity of beetles coincided with the time interval in which fi fth-instar codling moth, Cydia pomonella L., larvae wander on the ground prior to pupation (Riddick and Mills, 1996). They were also considered to be an important early season predator of larvae of C. pomonella in apple orchards (Riddick and Mills, 1994). It has been reported that Pterostichus niger Schaller., Pterostichus melanarius Illiger, Carabus nemoralis Mueller., and even Harpalus rufi pes (Degeer.) (syn. H. pubescens Muell.) might be effi cient predators of the larval stage of Leptinotarsa decemlineata Say. (Thiele, 1977; Sorokin, 1981; Koval, 1986).

Species of the genus Harpalus are mostly generalists, accepting a wide range of species of seed (Honek et al., 2007), preferring Viola L., Taraxacum G.H.Weber ex F.H.Wigg. and Cirsium Mill. seeds (Thiele, 1977; Jorgensen and Toft, 1997; Honek et al., 2007), as well as insect prey. Harpalus rufi pes is reported to be a predator, a biocontrol agent for the larvae of the brassica pod midge, Dasineura brassicae Winn., a pest of oilseed rape (Warner et al. 2000; Büchs, 2003), cabbage root fl y, Erioschia brassicae Bouche, eggs and larvae (Coaker and Williams, 1963), cabbage white butterfl y, Pieris rapae L., larvae (Dempster, 1967), contributed

15 to the suppression of bird cherry-oat aphid, Rhopalosiphum padi L., populations (Holopainen and Helenius, 1992) and play an important role in regulating medfl y, Ceratitis capitata Wiedemann, populations in citrus orchards (Monzo et al., 2011).

Adults of Carabus nemoralis (genus Carabus) are generalist feeders (Digweed, 1994). A carabid community is more species rich and contains more large species in eastern Europe than in western Europe (Kromp, 1999).

Carabid species breed in crop fi elds and plantations. Fields and plantations can be a source of recruitment to local populations. Large carabids have long lifecycles (Lövei and Sunderland, 1996); beetle activity is thus correlated with several pest accumulations. In carabid communities with adult beetles there are always their larvae, being active predators throughout the whole season. Larvae of Pterostichus are predators, soil pore explorers, moving within the soil structure; larvae of C. nemoralis are soil-surface walkers (Zetto-Brandmayr et al., 1998). Larvae of H. rufi pes are polyphagous, feeding on small arthropods and seeds (Zetto- Brandmayr, 1990), they are effective seed eaters capable of burrowing to a soil depth of almost 15 cm (Hartke et al., 1998).

Parasitoids In general, parasitoids infl uence the next generation of their hosts, but also infl uence the hosts’ vital functions. This may directly reduce pest damage. Insect parasitoids and parasitisation level on RB are unknown.

Several parasitoids have been found from larvae of strawberry blossom weevil, Anthonomus rubi Herbst., which is also an important raspberry pest in Estonia (Arus et al., 2008b). In Italy, research has focused on the parasitoids of strawberry blossom weevil in raspberry and bramble (Rubus fruticosus L.). A pteromalid, Spilomalus quadrinota Walk. and braconids, Bracon immutator Nees. and Triapsis aciculatus Ratz., have emerged from infested larvae; T. aciculatus were the most abundant with up to 68% parasitism (Scanabissi and Arzone, 1992). Several species of hymenopteran parasitoid have been isolated from galled canes, caused by Lasioptera rubi Heeger, but the role of these parasitic wasps in controlling L. rubi is unknown (Viggiani and Mazzone, 1978). Vétek et al., (2006) have found a parasitisation level of 15-33% in raspberry cane midge,

16 Resseliella theobaldi (Barnes.) larvae, by the chalcidoid species, Aprostocetus epicharmus Walker. Also rose stem girdler, Agrilus cuprescens Ménétriés, is attacked by the hymenopterous parasitoid, Tetrastichus heeringi Del. which plays an important role in the control of this raspberry pest in Hungary (Vétek et al., 2006, 2008).

2.3. Eff ects of cultivation technologies on the pests and their natural enemies

The agroecosystem of fruit plantations can be affected by choice of cultivation technologies which infl uence plant growth and other organisms associated with plants (Percival et al., 1998; Libek and Kikas, 2000; Pedreros et al., 2008). A common goal of conservation biological control is to enhance biodiversity and increase abundance and effectiveness of predators and parasitoids, thus increasing the sustainability of pest management. In northern Europe, raspberry is often grown in a 10–15-year rotation. Longterm plantations are thus particularly suitable for local populations of pests as well as their natural enemies to increase over several years. Perennial crop systems are more compatible with conservation biological control than annual systems; resident populations of natural enemies may persist from year to year in perennial crops (Landis et al., 2000).

Mulches Using mulches as ground cover is one of the cultivation technologies in raspberry growing. Raspberry rows are mulched with synthetic or organic mulches, but raspberry rows without any mulching materials are also very common. Mulches suppress weed emergence, improve moisture conditions, help maintain a stable soil temperature, available potassium and phosphorus, and thereby having a positive effect on crop yield (Treder et al., 1993; Radics and Bognar, 2004; Sønsteby et al., 2004; Petersen and Röver, 2005; Jodaugienė et al., 2006; Sinkevičienė et al., 2009). They also favour soil micro-organisms (Larsson, 1997), thereby infl uencing plant health. Considering raspberry cane diseases, mulches, depending on the material used, can have positive but also negative side effects. Mulching with peat has decreased spur blight, Didymella applanata (Niessl./Sacc.) and anthracnose, Elsinoë veneta (Burkh.) Jenkins, infections, whereas mulching with straw has increased spur blight infection (Hanni and Libek, 2003).

17 Microclimatic conditions changed by mulches also infl uence the occurrence of insects, including carabids communities. Of phytophagous insects, black plastic mulch has been shown to increase the population of mites in strawberry plantations (Metspalu et al., 2001; Kivijärvi et al., 2002; Tuovinen et al., 2010). In Latvia, trials with three different organic mulches in strawberry showed that living grass mulch facilitated the spread of strawberry blossom weevil, A. rubi. At the same time, the percentage of damaged fl owers decreased in treatments with mulches of straw, shavings and bare ground (Laugale et al., 2006). The infl uence of mulches on RB damage has not been studied.

Carabid species respond differently to different mulches as their ecological requirements are determined by size, shape, food preferences, temperature, humidity and season (Lövei and Sunderland, 1996). Several studies report that organic mulches have a positive infl uence on the abundance of carabids and spiders in horticultural crops (Jõgar et al., 2001; Kikas and Luik, 2002; Minano and Dapena, 2003; Kikas and Luik, 2004) but there are few studies on the effect of mulches on insects, including carabids, in raspberry.

Intercropping Intercropping with different crops is a cultivation technology that helps reduce accumulation of pests by dispersing and disguising odours of each other (Uvah and Coacer, 1984; Wiech, 1991; Patt et al., 1997). Also, this diversity is attractive to benefi cial organisms (Rämert, 1993; Wyss et al., 1995; Wyss, 1996; Kromp, 1999; Altieri and Nicholls, 2003). Monocultures, where every plant in a crop is genetically identical lead to vulnerability to stress, whether caused by pathogens, pests, or the weather, and hence to unstable yields (Altieri and Nicholls, 2003). Intercropping with fl owering plants provide alternative prey, nectar, pollen and shelter for many invertebrate predators, parasitoids and pollinators which can increase survivorship, fecundity and retention of natural enemies (Coll, 1998; Landis et al., 2000; Pontin et al., 2006; Fiedler et al., 2008). The infl uence of intercropping on pests and their natural enemies has been studied in several horticultural crops (Wyss, 1996; Landis et al., 2000; Luik and Tarang, 2000) but there is still no data on raspberry.

18 3. HYPOTHESES AND AIMS OF THE STUDY

In plants, the damage caused by pests depends on plant genetic properties and environmental factors. The infl uence of cultivars on raspberry beetle damage is still poorly studied. Knowledge on the interactions between raspberry beetle and their possible arthropod natural enemies is scarce.

Hypotheses:

• Raspberry beetle damage depends on cultivar properties and on cultivation technologies. • Raspberry beetle has predators whose occurrence depends on raspberry phenology and on cultivation technologies. • Raspberry beetle has parasitoids and the parasitisation level of larvae depends on cultivation technologies.

The aims of the present study were:

1. To estimate raspberry beetle damage to raspberry cultivars with different fl owering times (I) and cultivation technologies. 2. To estimate carabid, as potential predators of raspberry beetle, species composition and abundance dependence on different raspberry cultivation technologies (II, III). 3. To establish the correlation between aggregation of dominant carabid species and raspberry beetle larvae (as prey), falling time to the soil for pupation (III). 4. To confi rm the predatory role of a dominant carabid with laboratory experiments by feeding them with raspberry beetle larvae (IV). 5. To establish whether raspberry beetle larvae have parasitoids and whether the level of parasitisation depends on different intercropping systems (V).

19 4. MATERIALS AND METHODS

4.1. Descriptions and design of the experimental areas

The research is based on four fi eld experiments:

Experiment 1: Cultivar evaluation trial conducted in 2003-2011 (I).

The study of cultivar susceptibility to RB larval damage was carried out in the collection of raspberry cultivars at Polli Horticultural Research Centre of the Estonian University of Life Sciences in Southern Estonia (58˚7´N, 25˚33´E). The collection was established in 2000. The canes were planted in rows with 3.0 m between rows and 0.5 m between canes. Coarse grasses consisting mostly of Gramineae Juss. with Trifolium L. and Taraxacum Wigg. grew between the raspberry rows; this was cut regularly. No pesticides were applied and no mulching or irrigation were used.

The damage level of RB larvae from total yield was estimated in 17 cultivars: ‘Aita’, ‘Alvi’, ‘Helkal’, ‘Tomo’ (cvs. of Estonian origin), ‘Herbert’, ‘Algonquine’, ‘Ottawa’, ‘Haida’, ‘Veten’ (cvs. of Canada), ‘Ivars’ (Latvia), ‘Novokitaivska’ (Ukraine), ‘Preussen’ (Germany), ‘Glen Ample’, ‘Glen Magna’, ‘Glen Rosa’ (cvs. of U.K.), ‘Nagrada’ (Russia), ‘Norna’ (Norway).

Plots of each cultivar were allocated in three replicates, with four plants in every replicate.

Experiment 2: Evaluation of carabid abundance and species composition in raspberry plantation conducted in 1999 (II).

The evaluation of carabid species composition and their abundance were studied in the 16-year-old raspberry plantation. The experiment was carried out at Rõhu Experimental Station (58˚21´N, 26˚31´E) at the Estonian University of Life Sciences. The plantation with six raspberry cvs. (‘Novokitaivska’, ‘Tomo’, ‘Meteor’, ‘Norna’, ‘Nagrada’ and ‘Herbert’) was established in 1983. The canes were planted in rows with spacing 3.0 m between rows and 0.5 m between canes. Between rows the soil

20 surface was cultivated and was without plant and weed cover. On the raspberry rows the rough herbage consisted: several Gramineae, Trifolium, Cirsium Mill. species, Elymus repens (L.) Gould, Taraxacum offi cinale Wigg. and Urtica dioica L. No pesticides were applied.

Different cultivars were allocated at random, each cultivar in four replicates, with 15 plants in every replicate.

Experiment 3: Evaluation of mulching on RB damage conducted in 2003 and on carabid abundance and species composition conducted in 2001-2003 and 2006 (III).

The effects of mulching on RB damage and on carabid species composition and abundance were studied in the raspberry plantation where raspberry rows were differently mulched. The experiment was carried out in a raspberry plantation at Polli Horticultural Research Centre. The plantation with two raspberry cvs. (‘Novokitaivska’ and ‘Tomo’) was established in 1998. The canes were planted in rows with spacing 3.0 m between rows and 0.5 m between canes. Between rows the rough herbage consisted mostly of Gramineae and Trifolium, but included some weeds, such as Elymus repens and Taraxacum offi cinale; this was cut regularly. No pesticides were applied.

Experimental mulch treatments were: • sawdust mulch (SDM), • peat mulch (PM), • barley straw mulch (SM), • black plastic mulch (BP) and • for control soil without any mulch (WM).

Black plastic was set before planting, natural organic mulches (ca 15 cm) were added after planting and new layers of sawdust, peat and straw were added every spring at the end of May.

Different mulching treatments were allocated at random, each treatment in four replicates.

21 Experiment 4: Evaluation of the effect of intercropping systems on carabid abundance and species composition and on parasitism level of RB larvae conducted in 2004-2005 (V).

The effect on carabid abundance and species composition (2004-2005) and on parasitism level of RB larvae (2005) was studied in a small private organic fruit production farm in Viljandi County in Southern Estonia and from wild raspberry, from a clear cut area in the neighbourhood of the plantation (58˚7´N, 25˚49´E). The raspberry plantation with different intercropping systems with two raspberry cvs. (‘Novokitaivska’ and ‘Tomo’) was established in 2002. The canes were planted in rows with 3.0 m between rows and 0.5 m between canes. The plantation was surrounded by a 10 m width of thick grass, which was regularly cut. Near the plantation was a forest with a clear cut area, natural grassland and a little body of water. Thick grass, consisting mostly of Gramineae and Trifolium, and including some weeds like Elymus repens and Taraxacum offi cinale grew between rows. No chemical treatments or mineral fertilisation were used on the plantation.

The experimental treatments were: • control, raspberry monoculture, 15x15 m. • raspberry rows alternating with rows of fl owering plants, 15x10 m (7 different herbs). • raspberry rows alternating with rows of black currant, 15x15 m. • wild raspberry, from clear cut area in the neighbourhood of the plantation.

The experimental treatments in three replicates were separated by a vegetable fi eld (width 25 m). Weeds were mechanically controlled twice in the vegetation period. In spring, decayed manure was spread on the raspberry rows, about 5 kg per rowmeter, and cut grass was used as mulch. The fl owering plants were Achillea millefolium L., Anethum graveolens L., Borago offi cinalis L., Calendula offi cinalis L., Foeniculum vulgare Mill., Chamomilla recutita (L.) Rauschert, and Tanacetum vulgare L.

22 4.1.1. Data collection in fi eld experiments

Evaluation of raspberry beetle damage (I)

The amounts of damaged raspberry fruits were used for RB abundance estimation. Thus, the abundance of RB was determined indirectly. In this study the RB damage level is showing the proportion of damaged fruits from total yield of experimental treatment.

In these experimental treatements all ripe raspberry fruits were harvested 3 times per week for 3−5 weeks (depending on the year’s weather conditions) in all study years. Fruits damaged by RB (including fruits with damaged husks) and undamaged fruits were picked and weighed separately. The damage level of RB was calculated as a percentage of different cultivars’ yields.

Evaluation of carabid abundance and species composition (II, III)

Pitfall traps were used to sample carabids. This is the most widely used sampling technique for carabids, particularly in agricultural habitats, where they provides a cheap and simple method of catching a large number of individuals of diverse species (Kromp, 1999; Luff, 1987). Carabids fall into the traps where they are preserved in liquid.

In this study the plastic traps (9 cm diameter, 10 cm high, fi lled with a 10% salt water solution) were placed in position before fl owering of the raspberries and removed at the end of fruit ripening. Traps were placed in the middle of the raspberry plots between plants (one trap per plot, in total four traps in every variant). Traps were checked and arthropods collected at 7-day intervals. Captured carabids were identifi ed and counted in the laboratory. Identifi cation to species was aided by the extensive university collection of carabids. The taxonomic nomenclature of carabid species follows that of Haberman (1968) and Silferberg et al. (2004).

Evaluation of parasitisation level of raspberry beetle larvae (V)

In the intercropping experiment, explained before, the occurrence of RB parasitoids and parasitisation level were investigated. The RB larvae

23 from ripe fruits were collected during the ripening period of raspberry from different intercropping treatments and from wild raspberry in the neighbourhood of the experiment. The larvae were deep-frozen in distilled water. After thawing, the larvae were dyed and were dissected under a microscope at about 25 x magnifi cation. The larvae of parasitoids appeared after the adipose tissue and haemolymph of pest larvae were dyed. The parasitisation level of RB larvae was calculated as a percentage of the total amount.

4.1.2. Weather conditions

Temperature and precipitation were recorded at a weather station in Polli. May, June and July weather conditions are important for the development of RB damage because during these months, the raspberry fl owers and fruits form and the beetles are mating and ovipositing. During most study years, the mean temperature in May was more than 1 ºC higher than the long-term average. June mean temperatures varied from year to year and were more than 2 ºC higher in 2002, 2006 and 2011 than the long term average. In most of the study years the average temperatures in July and August were higher than the long term average. The spring and summers 2006 and 2011 could be described as the hottest and driest since the total amount of rainfall was much less than the long term average; it wasn’t suitable for raspberry plant growth, fl owering and yield formation and also infl uenced the insect’s behaviour. By contrast, June in 2002, 2004 and 2008−2009 and July 2001 were wet, since the amount of rainfall exceeded the long term average (Tables 1 in I and 1 in III); conditions for plant growth and yield were good but not so suitable for adult RB mating and oviposition.

4.2. Laboratory feeding experiment (IV)

A laboratory feeding experiment was conducted in 2006. Carabids and their food (RB larvae, aphid and weed seeds) were randomly collected from the collection of raspberry cultivars at Polli Horticultural Research Centre. The carabids were caught with dry pitfall traps, checked every 24 h; as the beetles are nocturnal this was done early each morning to avoid the beetles being in the traps for too long. The captured beetles were kept in a laboratory for 24 h without food before the experiments to standardize their hunger state. They were then placed individually in

24 small containers with water supplied on soaked cotton wool in the shade at room temperature (20 ºC). The prey items, i.e. RB fourth instar larvae from ripe fruits (with an average biomass of 4.46 ± 0.171 mg), the large raspberry aphid (Amphorophora idaei Börner) (0.63 ± 0.029 mg) and dry seeds of Thlaspi arvense L. (1.1 ± 0.017 mg), were collected at the same locality as the beetles directly before each experiment.

In: • no-choice feeding tests, P. niger, P. melanarius, C. nemoralis carabids were presented with either 10 RB larvae or 10 aphids while the H. rufi pes carabids were presented with either 10 RB larvae or 10 T. arvense seeds. • choice feeding tests, P. melanarius, P. niger and C. nemoralis carabids were presented with 10 RB larvae together with 10 aphids while H. rufi pes carabids were presented with 10 RB larvae together with 10 seeds.

A total of 135 carabids of each species were tested in each type of feeding test. All tests were made in 9 replicates. Each carabid was tested only once; it was placed together with the prey items on moist fi lter paper in a Petri dish at room temperature (20 ºC). Tests were conducted in the dark as carabids are night active and terminated after different periods of time: 1, 2, 3, 6 and 12 h. After the specifi ed time, dishes were taken into the light and the number of prey items consumed was recorded.

4.3. Statistical data analyses

The RB damage level data depending on different years, on cvs., on mulching treatments and the data of carabid abundance dependence on different cultivation technologies were analysed by one- and two-way ANOVA. Standard deviations or standard errors (vertical bars, SD and SE, respectively) were calculated and the signifi cances of differences were controlled by Tukey test at p<0.05 level. Signifi cantly different data values are followed by different letters (a, b, c…) in tables and fi gures (I, III).

A linear regression analysis was applied to fi nd the relationship (r) between the beginnings of fl owering times of raspberry cvs. and RB damage level (I).

25 In the laboratory feeding experiment the mean number of items consumed per defi ned time unit and its standard error (±SE) were calculated and the signifi cance of data differences determined using the Tukey-Kramer’s test as p<0.05*, p<0.01**, p<0.001***, ns (not signifi cant differences) (IV).

The parasitsation level of RB larvae was calculated and analysed by one- way ANOVA and differences were compared by using LSD post-hoc test at p<0.05 level (V).

26 5. RESULTS

5.1. The impact of cultivars (I) and mulching on raspberry beetle damage

The raspberry beetle damage level in different years

During the study years two RB population peaks are apparent with quite high damage levels in 2003 and 2010-2011 (Figure 1 in I). The highest damage level was in 2003 (21.0% on average). Thereafter, the population gradually decreased with very low damage levels of only 0.1- 0.2% during 2006-2009. A new population increase started from 2010 when the damage level reached 11.5% increasing in the following year, to 15.9% although this was still lower than in 2003.

The effect of cultivars

The biggest differences in damage levels between cvs. appeared in years when the beetle population was high; 2003, 2010 and 2011(Table 2 in I). In all these years the early fl owering cvs. ‘Novokitaivska’, ‘Ivars’ and ‘Aita’ were more damaged (>20%) than late fl owering cvs. ‘Glen Magna’ and ‘Glen Ample’(<5%).

Linear regression analysis showed that the early fl owering cvs. were clearly more damaged by RB than the late fl owering cvs. in fi ve study years 2003, 2006 and 2008-10 (r=-0.443, p=0.014 in 2003; r=-0.418, p=0.030 in 2006; r=-0.546, p=0.020 in 2008; r=-0.439, p=0.030 in 2009 and r=-0.566, p=0.018 in 2010). Thus, overall, the linear regression analysis of all study years and for all study years and for all cvs. showed that there is a strong relationship (r=-0.736, p<0.001) between the beginning of fl owering and RB damage levels of cvs. (Figure 2 in I). The early fl owering cvs. were more damaged than late fl owering cvs.

Comparison of the average RB damage levels of cvs. during the study years (Figure 3 in I) showed that the early fl owering cvs. ‘Novokitaivska’, ‘Ivars’, ‘Preussen’ and ‘Aita’ with their highest damage levels of 10.2, 9.7, 8.6 and 8.3% were the most susceptible to RB. From the late fl owering cvs. ‘Glen Ample’ and ‘Glen Magna’ with damage levels 2.1 and 2.6% were less susceptible to RB.

27 The effect of mulching

In the mulching experiment, differences between mulching treatment and fruit damage by RB larvae were found (Figure 1). In cv. ‘Novokitaivska’ the fruits growing on straw mulch were signifi cantly less damaged (40.3%) by RB than fruits in the treatment without any mulch material, sawdust and black plastic mulch (over 49.6%). In ‘Tomo’ plants there was tendensy that fruits were less damaged by RB in all mulching treatments. On an average of these two cvs. the fruits growing on mulching treatment with straw mulch were over 10% less damaged (37.3%) by RB than fruits in the treatment without any mulch material (49.8%).

60 ns b b b b a ab ab ab ab a b a 40

20 Damaged fruits % fruits Damaged

0 T N BP BP BP SM SM SM PM PM PM WM WM WM SDM SDM SDM Novokitaivska Tomo Effect of Effect of mulching cultivar

Figure 1. Average percentages of raspberry beetle damages from total yield in different cultivation technologies in 2003 (calculated as means±SE). Different letters in columns indicate signifi cant differences between treatments, two-way ANOVA, Tukey test, p<0.05).

WM−Without mulching treatment; SDM−Sawdust mulch; PM−Peat mulch; SM− Straw mulch; BP−Black plastic; N−’Novokitaivska’; T−’Tomo’.

5.2. The carabids species composition and abundance; impact of cultivation technologies (II, III)

The carabid species composition and abundance was dependent on experimental sites. In 1999, in Rõhu raspberry plantation, 26 carabid species from 13 genera were found (Table 1 in II; Table 1). Dominant

28 (more than 5% from whole catches) carabid species were Pterostichus melanarius (25.8%), Amara fulva Mueller (19.3%), Harpalus rufi pes (13.0%), Carabus nemoralis (12.4%), Pterostichus niger (8.6%), Bembidion lampros Herbst (5.7%) and Agonum assimile Payk. (5.1%).

In the mulching experiment, the species richness of carabids increased with plantation age (Table 2 in III; Table 1). In 2001-2003, species number increased from 29 to 32 species belonging to 15 genera. In 2006, 45 species from 18 genera were found. Dominant carabid species were P. niger (34.8%), Pterostichus cupreus (14.7%), P. melanarius (10.4%), H. rufi pes (8.1%) and C. nemoralis (7.7%). Carabid abundance was infl uenced by year and by the type of mulch (Figure 1 in III). In 2001, 2002 and 2006, there were signifi cant differences in the total carabid catches between different mulching treatments. On average, in all study years, carabids signifi cantly preferred beds with straw mulch (p<0.05) to the peat mulch.

Comparing the infl uence of mulches on the occurrence of dominant carabid species then P. melanarius did not prefer any mulch to the others in an average of 4 study years (Figure 2A in III). Signifi cant differences between mulches of P. melanarius were only in the very dry year 2006, when in the beginning of ripening time of fruits the straw mulch beds were preferred (Figure 3D in III). P. niger and C. nemoralis preferred straw mulch to the peat, sawdust and the without mulch treatment in an average (Figures 2B-C in III). The preference of mulching treatments to the no mulch beds was very clearly seen in 2006, in the extremely dry year. In that case, the straw treatment was preferred to the peat, sawdust and black plastic (p<0.05). H. rufi pes did not prefer any mulch over others in an average of 4 years (Figure 2D in III); but there were differences in different years − in 2002, straw and black plastic were preferred to the peat mulch; in 2006, sawdust was preferred to the peat and straw mulch but very few specimens were present.

There is a clear tendency for the most numerous carabids P. niger, P. melanarius to prefer straw mulch raspberry beds (Figures 3-6 in III). Comparing the abundance of dominant carabid species with raspberries ripening then the numbers of P. niger, P. melanarius, H. rufi pes and C. nemoralis were increasing during fruit ripening time, when RB larvae were falling down to soil for pupation. The increase in abundance was especially clear in the case of P. niger.

29 In the intercropping experiment, 33 species from 14 genera were found in 2004 and 2005, the most abundant carabid species were P. cupreus (15.4%), H. rufi pes (14.1%), P. niger (9.9%) and P. melanarius (9.7%) (Table 1). The carabid abundance was infl uenced by year and by cultivation technologies (Figure 2). In 2004, the carabids were signifi cantly more abundant in raspberry + fl owering plants and raspberry + black currants row treatments than in the monocropping treatment. In 2005, carabid abundance was very low, apparently because of very warm weather conditions in June-July; therefore these differences between treatments can not show the real infl uence of cultivation technologies.

180.0

150.0 a a a

120.0 b

90.0

c 60.0 c b

Number of individuals per trap d 30.0

0.0 I II III I II III 2004 2005 2004 2005 Effect of the year

Figure 2. Number of carabids in different intercropping systems of raspberry plantation in 2004-05 (calculated as means±SE). Different letters in columns indicate signifi cant differences between treatments, two-way ANOVA, Tukey test, p<0.05).

I – raspberry monoculture; II – raspberry + fl owering plants; III – raspberry + black currant.

Comparing the infl uence of raspberry intercropping systems on the occurrence of dominant carabid species (Figure 3) then P. melanarius did not prefer any intercropping system to the others. In P. niger has an apparent tendency to prefer the raspberry + fl owering plant treatment which is also signifi cantly preferred by H. rufi pes (p<0.05).

30 40.0 a

30.0 ab

20.0 a c bc bc a c b 10.0 c c c Number of individuals per trap 0.0 I II III I II III I II III I II III P. melanarius P. niger H. rufipes Average effect of cultivation technology Figure 3. Effect of intercropping cultivation systems to the dominant carabid species in 2004 (calculated as means±SE). Different letters in columns indicate signifi cant differences between treatments, two-way ANOVA, p<0.05.

I – raspberry monoculture; II – raspberry + fl owering plants; III – raspberry + black currant.

31 Table 1. Species composition, (D) dominance (more than 5% of catches) and (+) presence of carabids in different experimental sites. In In mulch experiment In intercropping Rõhu experiment (II) Species 1999 2001 2002 2003 2006 2004 2005 Agonum assimile Payk.D D+++++ A. dorsale Pont. + + + + A. muelleri Herbst. + + A. sexpunctatum L. + + + Amara aulica Panz. + + + + + A. aenea De Geer + + + + A. bifrons Gyll. + + + + A. consularis Duftschmid + + A. communis Panz. ++++++ A. curta Dejean + + + + A. fulva Muell. D + + + + + A. plebeja Gyll. + + A. similata Gyll. + + + + + Asaphidion fl avipes L. ++++++ Badister sp. + Bembidion lampros Herbst D D D + + + D B. quadrimaculatum L.+ ++++ B. properans Stephens + + + Calathus fuscipes Goeze + C. erratus Sahlberg + + + C. melanocefalus L. +++++ Carabus arvensis Herbst. + C. cancellatus Ill. + + + + + + C. granulatus L.+ +++ + C. hortensis L. + C. nemoralis Muell. D D D + D + + C. violaceus L. + + + Clivinia fossor L. + ++++++ Cychrus caraboides L. + + + + Dromius sigma L. + + Dyschirius sp + Harpalus aeneus F.+ ++ + H. affi nis Schrank + H. latus L. + + + +

32 Table 1 continued

In In In mulch experiment Rõhu intercropping (II) experiment H. luteicornis Duftschmid + + H. rufi pes De Geer (syn. H. pubescens Muell.) D DDD+DD H. punctatulus Duftschmid + + H. seladon Schaub. ++++++ H. tardus Panz. + + + + Lebia crux-minor L. + Leistus ferrugineus L. + L. rufescens Fabr. + + + + + Loricera pilicornis Fabr. + + + + + Nebria gyllenhali Sch. + Notiophilus bigutatus Payk. + + + + N. palustris Duftschmid + N. rufi pes Curt. + Oodes helopoides Fabr. + Panagaeus crux-major L. + Patrobus atrorufus Strom. + Pterostichus anthracinus Ill. + P. coerulescens L.+ +++++ P. cupreus L. + +DDDDD P. diligens Sturm + P. minor Gyll. + + + + P. niger Schaller DDDDDDD P. nigrita F. + P. oblopunctatus Fabr. ++++++ P. obscurus + P. vernalis Panz. + + P. versicolor Sturm + P. melanarius Ill. (syn. P. vulgaris L.) D DD+DDD Stomis pumicatus Panz.+ ++++++ Synuchus vivalis Ill. + Trechus secalis Payk. + + carabids larvae + ++++++ nr. of individuals 932 692 725 899 1214 1089 318 nr. of species 26 29 30 32 45 33 33

33 5.3. Laboratory feeding experiment with carabids (IV)

In no-choice feeding tests (Table 1 in IV) P. melanarius, P. niger and C. nemoralis consumed most of the RB larvae during the fi rst hour of the experiment, whereas most of the aphids were eaten two to three hours after the experiment started. H. rufi pes at the same time interval had eaten less food. P. melanarius had consumed signifi cantly more beetle larvae than aphids after both the fi rst and second hours (Tukey-Kramer’s test, p<0.001 and p=0.011). According to the biomass of the food, beetle larvae were consumed signifi cantly more (p<0.001) than aphids at every control point. P. niger, C. nemoralis and H. rufi pes had consumed similar numbers of the two food items. According to the biomass of the food, beetle larvae were consumed signifi cantly more than aphids at every control point.

In the choice feeding tests (Table 2 in IV), the quantity of consumed food items was less than in the no-choice feeding tests. For P. melanarius and P. niger a signifi cant preference for beetle larvae was seen in the choice feeding tests after the 1st hour (p=0.025 and p=0.043). Later, such signifi cant preferences for the larvae were lost. According to the biomass of the prey, larvae were preferred to the aphids at every control point. C. nemoralis was at fi rst confused in choice tests and consumed less food than in no-choice tests. In choice tests, there was no signifi cant preference between consumed food items. According to the biomass of the prey, a signifi cant preference for beetle larvae occurred after three hours. H. rufi pes showed a clear signifi cant preference for beetle larvae in choice tests after three hours. According to the biomass of the larvae and seeds, the larvae were consumed signifi cantly more. Thus choice feeding tests gave clear evidence that P. melanarius, P. niger, C. nemoralis and H. rufi pes prefer to consume RB larvae over aphids.

5.4. The impact of intercropping on the parasitisation level of raspberry beetle larvae (V)

In general intercropping offers new habitats for several insects including potential parasitoids. The study showed that RB larvae had endoparasitoids (Figure 4) and parasitation level was infl uenced by intercrops (Figure 1 in V). In one parasitised RB larva from 1 to 6 parasitoid larvae were found. The most parasitised (26.1%) were the

34 larvae from wild raspberry. The intercropping system raspberry + fl owering plants increased larval parasitisation level (9.4%), while in the intercropping system raspberry + black currant, it decreased (2.2%). In the monocropping conditions the larval parasitisation level was 4.4%. The species of RB parasitoid is still unknown and needs identifi cation in future studies.

Figure 4. The parasitoids larvae from the raspberry beetle larva (Photo by L. Arus and M. Heidema).

35 6. DISCUSSION

6.1. The impact of raspberry cultivars and mulches on the raspberry beetle damage

Several authors (Willmer et al., 1996; Szántóné Veszelka and Fajcsi, 2003; Woodford et al., 2003) have shown that the occurrence of RB on the host plant is extremely variable in different seasons. This nine year study has shown two damage peaks of RB which is explainable by the higher number of specimens of the species. Population dynamics is infl uenced by weather conditions. Temperature and precipitation conditions infl uence raspberry development as well as RB activity and behaviour. Temperature and moisture conditions during overwintering and spring determine the emergence success of beetles from the soil after hibernation. Temperature also infl uences feeding, mating and oviposition behaviour of adults of RB, under laboratory conditions, RB is capable of fl ight at 15 ˚C, so fl ight activity is therefore common only in the early afternoon of warm days; furthermore, compared to mature beetles, the young adults are very sensitive to water loss reducing their hygric stress by remaining in humid microclimates (Willmer et al., 1996). Extreme weather conditions of spring are unfavourable for RB development. Comparing temperature and precipitation conditions from May to June (Table 1 in I) and RB damage levels (Figure 2 in I) then it seems that drier (2006) and wetter (2004, 2008-2009) or warmer (2005-2007) weather conditions correlate with lower damage levels − that means with low RB population.

Raspberry fl owering depends on weather conditions and cultivar. Cultivars have differing phenologies, fl ower and fruit sizes and ripening speeds (Jennings, 1988). Woodford et al. (2003) reported that adult RB are on the raspberry plants at least 3 weeks before they start to fl ower and that the highest number of beetles is usually recorded before fl owers open. However, the beetles stayed in the plantation during the whole fl owering period. The latest studies have also shown that RB activity in raspberry plantations is much earlier than previously expected (Baroffi o et al., 2011; Baroffi o and Mittaz, 2011). Our study has shown that early fl owering raspberry cultivars are, on average, more damaged by RB than later fl owering cultivars (Figure 2 in I). This indicates that the phenology of the beetle is better correlated with early fl owering

36 cultivars. It should be noted that the physical proximity of one cultivar to another in the cultivar collection might infl uence oviposition decisions by beetles differently than if beetles were exposed to an entire fi eld of one cultivar. On the other hand, cultivar choice in the collection shows cultivar susceptibility to the pests or other organisms in a better way. The highest damage levels occurred in the early fl owering cultivars ‘Novokitaivska’, ‘Aita’, ‘Preussen’ and ‘Ivars’. The attractiveness of ‘Novokitaivska’ to RB has been also mentioned in other studies (Hanni and Luik, 2001; Kikas et al., 2002). Possibly, these cultivars have also more attractive plant-specifi c factors (fl ower volatiles, nectar secretion) which affect oviposition choice. Willmer et al. (1998) indicated that RB prefers to oviposit in cultivars with drier fl owers which apparently emit a short-lived attractive volatile cue. The lowest damage levels were in the late fl owering cultivars ‘Glen Ample’ and ‘Glen Magna’ (Table 2 in I; Figure 3 in I); these cultivars may emit less attractive volatiles or nectar compounds. But, an average lower damage level of late fl owering cultivars indicates that beetles’ egg laying period is apparently not well correlated with late fl owering raspberry cultivars.

Oviposition by RB in raspberry fl owers is a function of insect and plant phenology, both of which vary somewhat independently among years. Growing technologies like mulching can change plant phenology (Libek and Kikas, 2000) and have infl uences also on insects (Laugale et al., 2006). Mulching materials’, covering the raspberry rows, offers good pupation and wintering conditions for RB larvae and beetles. During berry maturation, the larvae of RB drop to the ground, where they pupate in cradles at a depth of 5-20 cm, immature beetles and larvae winter in the ground. Mulches, including black plastic fi lm, could be a mechanical barrier for larvae, after a feeding period they have to burrow into the soil to pupate as quickly as possible to avoid ground living predatory insects. RB emerges as adults in spring from the soil and litter, and ascends the growing raspberry canes. The results confi rmed that raspberry cultivation technologies may be a factor infl uencing the level of RB damage, where the raspberry fruits in the treatment with straw mulch were less and the without mulch treatment was more damaged. The same results have been found comparing strawberry blossom weevil, A. rubi, damage in different mulching treatments in raspberry and strawberry fi elds (Laugale et al., 2006; Arus et al., 2008b). Probably the adults of RB are very local, even the fl ight distance reaches 120 m;

37 the trials by Woodford et al. (2003) with marked RB caught with volatile- enhanced traps showed that local beetles moved less than 5m from the release sites. Organic mulch materials, especially straw mulch, increased the occurrence of carabid beetles (III), potential key predators of RB (III; IV). That could be reason for the lower RB damage in the plots with straw mulch.

6.2. The infl uence of cultivation technologies on the natural enemies of raspberry beetle

This experiment showed that predatory carabids were abundant in experimental raspberry plantations. Their abundance depended on cultivation tehnologies (II, III; Table 1). Species composition varied from 26 to 45 species depending on plantation, age and cultivation technologies of plantations (Tabel 1). The most numerous carabid species, P. niger, P. melanarius, H. rufi pes and C. nemoralis, were similar to those reported other studies in raspberry and strawberry plantations in Estonia (Luik et al., 2000; Luik and Tarang, 2000; Kikas and Luik, 2002, 2004) and in Finland (Tuovinen et al., 2006). P. cupreus were dominant in the spring and during raspberry fl owering but them abundance was not correlated with RB larvae dropping to the soil for pupation. The seasonal activity of dominant carabid species adults was typical for autumn breeding species, with peak catches in July and the beginning of August (III). Carabid species vary in their foraging preferences; animal food in their diet is dependent on season. All stages of slugs, aphids, weevils, moths and midges can be present as food for large carabids all year round (Thiele, 1977; Sorokin, 1981; Evenhuis, 1982; Koval, 1986; Symondson, 1989; Holopainen and Helenius, 1992; Riddick and Mills, 1996; Kromp, 1999; Warner et al., 2000; Büchs, 2003; Horgan and Myers, 2004; Monzo et al., 2011). The key pest of raspberry – the larvae of RB − could be among the other prey items. The abundance of dominant carabid species increased signifi cantly when raspberry fruits were beginning to ripen. This is time when mature RB larvae drop to the soil for pupation and may provide potential food items for P. niger, P. melanarius, C. nemoralis and H. rufi pes (III).

Cultivation technologies infl uenced the presence of carabids in general including the dominant species (III). Veromann et al., (2006b) also found that the presence of carabids in spring oilseed rape was infl uenced by

38 cropping systems and that they were at their maximum abundance just before the time when the larvae of the pollen beetle, Meligethes aeneus (Fab.), drop to the soil for pupation. The raspberry beds mulched by straw and using intercropping system – raspberry + fl owering plants, were signifi cantly preferred by carabids. Carabids are more abundant in plantations with suffi cient food and suitable microclimatic conditions. Mulches change microclimatic conditions − temperature and humidity (Treder et al., 1993; Jodaugienė et al., 2006; Sinkevičienė et al., 2009). Soil temperature, humidity, food availability, organic matter and shelter may be infl uenced by husbandry practices, such as providing ground cover with mulch materials. Organic mulches could provide proper shelter and better food resources for carabids, especially in dry weather (Johnson et al., 2004) in raspberry plantations. The mulch infl uence is more apparent in extreme climatic conditions as in the extremely dry summer of 2006, when the straw mulch was signifi cantly preferred by all dominant species − P. niger, P. melanarius and C. nemoralis. For example, P. niger and P. melanarius are sensitive to moisture conditions (Sustek, 1994). Soil moisture is apparently higher and soil temperature lower under the straw than in the other treatments. In a hot summer, straw mulch is possibly better at retaining moisture and therefore these beds might be preferred by P. niger and P. melanarius. Straw mulch also promoted C. nemoralis occurrence. This could explain the signifi cantly greater abundance of carabids in the straw mulch, especially at the ripening time of raspberry (III). Periods with high air temperature and low rainfall are very common at that time in Estonia. Black plastic raises soil surface temperature (Tarara, 2000). Therefore, especially in cool and rainy summers, the abundance of carabids was higher with the black plastic treatment. In less hot and dry years, the catches of carabids in the no mulch control were probably higher because here they had additional food resources in raspberry rows. Presence of some weeds and hence their seeds, are an important and preferred food source for some carabids, especially for H. rufi pes (Thiele, 1977; Honek et al., 2007).

Carabid abundance and species richness increased with the age of the plantation (III). Barone and Frank (2003) also reported that the age of the habitat increases the abundance of generalist predator species, Levesque and Levesque (1994) found that adult P. melanarius were more abundant in old raspberry plantations than in young ones. Also, in this study the abundance of P. melanarius was higher in older plantations. In

39 older plantations, increase of carabids is supported through the presence of inter-row plant cover which offers further and different refuges. Such plant cover with Gramineae, Trifolium, Elymus repens and Taraxacum offi cinale dominating also became more diversifi ed with the age of plantation.

In this study, with laboratory feeding experiments, P. melanarius and P. niger fed well on RB larvae. This explains their higher abundance in raspberry plantations during fruit ripening time when RB larvae are available to them as prey items (III). In choice feeding tests, H. rufi pes signifi cantly preferred RB larvae to T. arvense seeds. This indicates that, if RB larvae are available, as they are at raspberry ripening time in plantations, they may be preferably eaten also by H. rufi pes beetles. Probably some volatile signal compounds from RB larvae which drop to the soil during raspberry ripening time attract aggregation of H. rufi pes, P. melanarius and P. niger to the raspberry plantation. C. nemoralis ate RB larvae and aphids at an equivalent level and did not show a signifi cant preference (IV). In raspberry plantations, aphids are available for a longer time in the vegetation period. Different authors have studied carabid diet and aphid control potential in the laboratory and fi eld (Ekbom et al., 1992; Kielty et al., 1999). Even if aphids are an important food for several polyphagous predators, a diet of aphids alone provides low-quality nutrition for a wide range of generalist insectivores (Bilde and Toft, 1994; Jorgensen and Toft, 1997). The impact of carabids on RB larvae is not necessarily associated with a high preference for larvae but also with the need for a mixed diet. It is important to note that pure diets of all prey types are nutritionally incomplete and most predators can improve their fi tness and fecundity by choosing a mixed diet (Toft, 1996; Saska, 2008). Laboratory feeding experiment confi rmed that the aggregation of H. rufi pes, P. melanarius, P. niger and C. nemoralis during raspberry fruit ripening (III) time when RB larvae drop to the soil for pupation suggests that they are concentrating to the available food source. Therefore, it is possible to conclude that H. rufi pes, P. melanarius, P. niger and C. nemoralis are regulating the RB population (III, IV).

Although RB larvae are safe from parasitoids due to their hidden lifestyle, this preliminary study shows that RB has parasitoids during their larval developmental stage and that the level of parasitisation is dependent on the cultivation system (V). Several pests with a hidden larval lifestyle have parasitoids. For example cabbage seed weevil,

40 Ceutorhynchus assimilis Payk., and the pollen beetle, M. aeneus, are hosts to wide range of parasitoids and their parasitisation level is dependent on cultivation technologies (Williams, 2003; Kevväi et al., 2006; Veromann et al., 2006a). Raspberry growing in the intercropping system with raspberry + fl owering plants promoted the parasitisation level of pest, and consequently also the presence of parasitoids (V). Wyss (1996) found that a strip-managed area with similar herbaceous plants was colonized by predators and parasitoids in higher number than the control. It is known that Anethum graveolens and Foeniculum vulgare are potentially suitable fl oral hosts for two eulophid parasitoids, Edovum puttleri Grissel and Pediobius foveolatus Crawford (Patt et al., 1997). Flowering plants, growing for example at fi eld margins, offer nectar and pollen for food, which are critically important for the survival and successful procreation for the Syrphidae and Hymenoptera (Lavandero et al., 2005; Winkler et al., 2006). The presence of natural meadow as a fi eld margin increased the abundance of potential pests, their parasitoids and also the diversity of carabid species (Tarang et al., 2004). Wild fl ower strips have been sown as special fi eld margins to promote benefi cial insects, including pollinators, predators and parasitoids as well as soil organisms, all of which help by providing “ecological services” to crop plants (Patt et al., 1997; Landis et al., 2000; Pontin et al., 2006; Fiedler et al., 2008). The parasitoid reduces the RB populations, thus infl uencing the RB larval damage in following years. Further studies are needed for taxonomical identifi cation of RB parasitoids and to fi nd growing technologies which enhance their occurrence.

41 CONCLUSIONS

Many raspberry growers have large yield losses and reduced quality of their products because of raspberry beetle (RB), B. tomentosus, damage. The current study has shown that by choice of cultivars and promotion natural enemies with cultivation technologies it is possible to regulate the RB population.

All hypotheses of this study were confi rmed. In host plant/insect interactions phenological synchronisation between beginning of fl owering of cultivars and RB oviposition period play key role. Early fl owering raspberry cultivars are phenologically better synchronized with the oviposition period of RB. Of the 17 cutivars tested, the early fl owering cultivars ‘Novokitaivska’, ‘Aita’, ‘Preussen’ and ‘Ivars’ were the most damaged, being the more susceptible to RB. Late fl owering cultivars are phenologically more isolated from the RB oviposition period. Of the late fl owering cultivars tested, ‘Glen Ample’ and ‘Glen Magna’ were signifi cantly less damaged than the others. Thus, by choice of late fl owering less susceptible raspberry cultivars is possible to decrease RB damage (I).

Cultivation technologies like mulching and intercropping infl uence plant growth and development but also insect communities. In mulching raspberry with straw, the RB damage level was signifi cantly lower. This can be explained by unfavourable conditions for RB development and also by higher pressure from its natural enemies (III).

In raspberry plantations the species composition and abundance of carabids, potential natural enemies of RB larvae during their falling time to soil for pupation, were established. This is the fi rst time that it has been shown that the abundance of dominant carabid species is related with phenology of RB. Carabids: Pterostichus melanarius, P. niger, Carabus nemoralis and Harpalus rufi pes – aggregate in the plantation during raspberry ripening time when RB larvae as prey objects are available (III). Laboratory feeding tests confi rmed that RB larvae are preferred food objects for these carabids (IV).

42 These dominant carabid species are potential key predators of RB larvae and their occurrence is enhanced by cultivation technologies, like straw mulch and intercropping system with fl owering plants (III).

This is the fi rst time that parasitoids have been found in the larvae of RB. Their level of parasitisation was enhanced in raspberry intercropping with fl owering plants (V). Thus in addition to predators, parasitoids can also play a role in RB population regulation.

Results of current study are very important for sustainable RB production practice. Growing late fl owering cultivars that are less susceptible to RB and combining them with cultivation technologies like mulching and intercropping – which enhance RB natural enemies, there is a possibility to regulate RB populations without use of pesticides and thereby to minimize pollution of the environment.

Future prospects

For breeding raspberry cultivars which are less susceptile to pests more profound knowledge is needed about factors infl uencing plant/insect interactions. Different plant qualities like fl ower colour and volatile compounds depending on plant genetic properties and also cultivation technologies should be studied, because they play a key role in insect attraction. Further studies are needed for taxonomical identifi cation of RB parasitoids and to develop cultivation technologies which enhance further the occurrence of parasitioids as well as predators. Also, more diversifi ed cultivation technologies should be developed to increase the effi ciency of natural enemies in RB population regulation.

43 SUMMARY IN ESTONIAN

SORDI JA LOODUSLIKE VAENLASTE MÕJU VAARIKAMARDIKALE (Byturus tomentosus De Geer)

Sissejuhatus

Aedvaarikas (R. idaeus) on kogu maailmas enamkasvatatav perekonna Rubus liik, kuid suurem osa tootmisest on koondunud Kesk- ja Põhja- Euroopasse (Gordon et al., 1997). Põhjamaades piiravad vaarika- kasvatust talvekahjustused aga ka vähene vastupidavus haigustele ja kahjuritele (Kikas et al., 2002; Strautina et al., 2012). Viimastest on olulisim vaarikamardikas, B. tomentosus, kes rikub viljade kvaliteedi ning võib põhjustada väga suuri saagikadusid (Tuovinen, 1997; Woodford et al., 2000; Hanni and Luik, 2001; Kikas et al., 2002; Woodford et al., 2003). Tõrjet tehakse enamasti keemiliste taimekaitsevahenditega. Need saastavad keskkonda ning hävitades kahjurite looduslikke vaenlasi, rikuvad kahjurite-kasurite looduslikku tasakaalu. Vaarikamardika arvukust piiravate keskkonnasõbralike lahenduste leidmine aitaks vähendada pestitsiidide kasutamist ja säilitada elurikkust.

Vaarikat kahjustavad nii vaarikamardika valmikud kui vastsed. Emased munevad õitele või arenevatele viljadele. Kõige suuremat kahju tekitavad vastsed, kes toituvad alguses noore vilja pinnal, hiljem tungivad vilja ning söövad viljaliha, rikkudes nii saagi kvaliteeti. Vigastatud viljadel väheneb säilivus (Taylor and Gordon, 1975; Gordon et al., 1997; Woodford et al., 2002; Birch et al., 2004). Vastseareng kestab 5-7 nädalat, millest enamuse aja ollakse viljas (Antonin, 1984). Sellise elukorralduse tõttu on vaarikamardika vastne nii entomofaagide kui entomopatogeenide eest suhteliselt hästi kaitstud. Looduslikele vaenlastele kättesaadavaks muutub täiskasvanud vastne siis, kui ta lahkub viljast ning laskub mullapinnale, et minna mulda nukkuma. Vaarikamardika looduslikke vaenlasi on vähe uuritud, ei tunta nende liigilist koosseisu ega mardika arvukust mõjutavaid võtmeliike. Vähe on teada kasvatustehnoloogiate mõjust nii vaarikamardikale kui tema võimalikele looduslikele vaenlastele. Samuti pole selge, kas ja kuidas vaarika sordiomadused koos erinevate kasvatustehnoloogiatega avaldavad mõju vaarikamardika arvukusele. Selleks, et arendada keskkonnasõbralikke kasvatussüsteeme on vajalik kindlaks teha, millised on vaarikamardikale vastupidavamad sordid ja kes

44 on mardika looduslikud vaenlased. Tähtis on leida kasvatustehnoloogiad, mis soosivad vaarikamardika looduslikke vaenlasi ning tagavad mardikapopulatsiooni võimalikult loodusliku regulatsiooni.

Lähtuvalt eeltoodust olid käesoleva töö eesmärgid järgmised:

1. Selgitada välja vaarikasortide kahjustuskindlus: hinnata vaarikamardika kahjustusi erineva õitsemiseaja algusega vaarika sortidel (I) ning võrrelda erinevate kasvatusviiside mõju kahjustuse tasemele. 2. Määrata vaarikamardika võimalike looduslike vaenlaste − jooksiklaste, liigiline koosseis ja arvukus sõltuvalt erinevatest vaarikakasvatuse tehnoloogiatest (II, III). 3. Teha kindalaks, kas jooksiklaste dominantsete liikide arvukuse tõus seostub vaarikamardika vastsete mullalelaskumise ajaga ning selgitada kas nende liikide hulgas on võtmeliike (III). 4. Kinnitada laboratoorsete söötmiskatsetega domineerivate jooksiklaste liikide rolli vaarikamardika arvukuse regulatsioonis (IV). 5. Selgitada kas vaarikamardika vastsetel esineb parasiteeritust ning selle ulatus sõltuvalt kasvatusviisist (V).

Materjal ja metoodika

Vaarikamardika esinemist hinnati kahjustatud viljade koguhulga järgi. Kahjustusi määrati 2003-2011. a. Pollis vaarikasortide kollektsioon- istandikus 17 erineval vaarikasordil (I) ja 2003. a. multšide katses (variandid: multšimata, saepuru-, turba-, põhu- ja kilemultš). Vaarikamardika võimalike looduslike vaenlaste − jooksiklaste − liigilist koosseisu, arvukust (II, III) ja dominantsete liikide arvukuse dünaamika ja vaarikamardika vastsete bioloogia vahelisi seoseid (III) määrati Rõhul, multšide katses Pollis ja segaviljeluse katses Kärstnas (V). Segaviljeluskatse variandid olid vaarikas monokultuurina, vaarikaread vaheldumisi õitsevate taimede ridadega ja vaarikaread vaheldumisi musta sõstra ridadega. Laboratoorsetes söötmiskatsetes uuriti nelja dominantse jooksiklaseliigi isendite toidueelistusi (IV). Parasitoidide esinemist vaarikamardika vastsetes määrati vaarika segaviljeluskatses, lisaks koguti vastseid istandiku läheduses asuval raielangil kasvavalt metsvaarikalt (V).

45 Peamised tulemused ja järeldused

Keskkonnasõbraliku viljelustehnoloogia arendamisel eelistatakse kahjuritele hea vastupidavusega sorte. Käesolevast tööst selgus, et vaarikamardika kahjustuse taseme kujunemisel oli oluline roll sordi omadustel, sealhulgas taime ja kahjuri fenoloogilisel sobivusel. Oluline oli ka kahjuri looduslike vaenlaste, jooksiklaste ja parasitoidide, olemasolu vaarikaistandikes. Vaarikasortide võrdleval uurimisel selgus, et vaarikamardika kahjustuse tase oli tugevas korrelatsioonis nende õitsemise aja algusega. Varjasema õitsemise algusajaga sordid olid vaarikamardika valmikute munemisajaga fenoloogiliselt paremini sünkroniseerinud kui hilisema õitsemisaja algusega sordid. Nendest sortidest kahjustas vaarikamardikas rohkem sorte ‘Novokitaivska’, ‘Aita’ ja ‘Ivars’. Hiljem õitsevate sortide rühmast olid ’Glen Ample’ ja ’Glen Magna’ oluliselt vähem kahjustunud. Selliste hilisõitsemisega sortide kasvatamisega on võimalik vähendada vaarikamardika kahjustusi (I).

Vaarikamardika võimalike looduslike vaenlaste selgitamisel ilmnes, et valdavalt röövtoidulise eluviisiga jooksiklaste rühm oli vaarikaistandikes liigirikas ja arvukas ning mõlemad näitajad suurenesid istandiku vananedes. Domineerivateks liikideks olid Pterostichus melanarius, Pterostichus niger, Carabus nemoralis ja Harpalus rufi pes (II, III) ning nende arvukus sõltus vaarikakasvatusviisidest. Põhumultš ja segaviljelus õitsevate taimedega soosis nende jooksiklaste esinemist. Põhumultši kasutamisel olid vaarikad teiste variantidega võrreldes vähem kahjustatud, mis viitab vaarikamardika looduslike vaenlaste suuremale survele. Esmakordselt tehti kindlaks, et jooksiklaste dominantsete liikide kogunemine istandusse satub kokku vaarikamardika vastsete mulda laskumise perioodiga. Sellest järeldub, et just toidubaasi suurenemine meelitab sellel ajal jooksiklaste teatud liigid istandusse (III). Neid tulemusi kinnitasid samade liikidega läbi viidud laboratoorsed söötmiskatsed, millest selgus, et toiduks eelistati vaarikamardika vastseid (IV). Järelikult on jooksiklased P. melanarius, P. niger, C. nemoralis ja H. rufi pes Eesti tingimustes vaarikamardika olulised looduslikud vaenlased ning neid võib pidada võtmeliikideks kahjuri arvukuse reguleerijatena (II, III, IV). Nende esinemist mõjutasid positiivselt nii põhumultš kui ka õistaimedega segaviljelussüsteem. Uurimuses selgus, et lisaks jooksiklastele mõjutasid vaarikamardika arvukust ka parasitoidid, kelle esinemise kohta siiani andmed täiesti puudusid. Vaarikamardika vastsetest leiti endoparasitoide, kusjuures

46 parasiteeritud vastsete hulk sõltus vaarikakasvatusviisist. Parasiteeritud vastseid oli oluliselt rohkem segaviljelussüsteemis, kus vaarikaread olid vaheldumisi õitsevate taimede ridadega (V).

Käesoleva töö tulemustel on otsene väljund keskkonnasõbralikku vaarikakasvatusse. Kasvatades hiljem õitsevaid, vaarikamardika poolt vähemkahjustuvaid vaarikasorte ning kombineerides neid erinevate kasvatusviisidega (multšid ja segaviljelus) on võimalik vähendada kahjuri arvukust istandikus. Keskkonnahoidliku tootmisega suureneb nende vaarikamardika looduslike vaenlaste hulk, kes reguleerivad kahjuri ohtrust. Kokkuvõttes kahaneb keemilise taimekaitse vajadus ning väheneb keskkonna saastekoormus.

Edasist uurimist vajavad küsimused:

Kahjurikindlamate vaarikasortide aretuseks on vaja põhjalikke uuringuid nii peremeestaim/putukas vaheliste seoste kui ka neid mõjutavate tegurite kohta. Selgitamist vajavad kahjuri käitumist mõjutavad taime (sordi) erinevad omadused: õite värvus, lõhnaainete sisaldus, vahakiht, nektariproduktsioon ja selle koostis jne. Need omadused sõltuvad peamiselt taime ja sordi geneetilistest omadustest aga neid võivad mõjutada ka kasvatusviisid. Parasitoidide liikide määramiseks on vajalikud täiendavad uuringud. Ka mitmekesistatud taimestikuga kasvatustehnoloogiad, mille eesmärgiks on suurendada looduslike vaenlaste mõju vaarikamardika arvukuse regulatsioonis, vajavad täiendavaid uuringuid.

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60 ACKNOWLEDGEMENTS

The study was carried out at the Polli Horticultural Research Centre and in the Department of Plant Protection of the Institute of Agricultural and Environmental Sciences, Estonian University of Life Sciences.

My deepest gratitude to my supervisor Prof. emer. Anne Luik for her advice, valuable comments and suggestions throughout the preparation of the manuscripts and thesis and for her encouragement, guidance, patience and support during my studies.

I am very grateful to the colleagues from the Polli Horticultural Research Centre for their help and support, my special thanks goes to dr. Asta Libek. I would like to thank the co-authors of the experimental work presented in the current thesis. I am very thankful to Luule Metspalu and Ingrid H. Williams for their valuable comments, suggestions and the linguistic corrections of manuscripts and this thesis. I thank Marge Starast and Taimi Paal for being the opponents of my pre-defence and giving me good advises to improve my work.

Identifi cation to species was aided by the extensive university collection of carabids (EAA(Z)).

My greatest thanks to my best friend Liina, the only friend who was able to help me with advices related to thesis preparation and with whom I can always share the other passions of ours.

Olen väga tänulik oma abikaasale ja suurepärastele poegadele. Aitäh, et olite nii kannatlikud ja alati uskusite minusse. Tänan oma sugulasi, kes aitasid mind doktoritöö kirjutamise ajal minu rohkete kodutöödega.

This study was carried out as part of projects “Improvement of assortment of fruit crops, maintenance of genetic diversity and development of environment-friendly cultivating methods II” No. SF1092711s06, “Plant protection for sustainable crop production”, No. SF0170057s09 and Grants No. 4109, 5736 supported by the Estonian Science Foundation.

61

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ORIGINAL PUBLICATIONS Arus, L., Kikas, A., Kaldmäe, H., Kahu, K. and Luik, A. 2013. DAMAGE BY RASPBERRY BEETLE (Byturus tomentosus De Geer) IN DIFFERENT RASPBERRY CULTIVARS. Biological Agriculture and Horticulture (accepted for publication) Damage by raspberry beetle (Byturus tomentosus De Geer) in different raspberry cultivars

Biological Agriculture & Horticulture Manuscript ID: TBAH-2013-0095.R1

Corresponding author:

Liina ARUS Polli Horticultural Research Centre, Institute of Agricultural and Environmental Sciences, Estonian University of Life Sciences. Kreutzwaldi 1, Tartu, 51014, Estonia. E- mail: [email protected]

Co-authors:

Ave KIKASa, Hedi KALDMÄEa, Kersti KAHUa and Anne LUIKb a Polli Horticultural Research Centre, Institute of Agricultural and Environmental Sciences, Estonian University of Life Sciences. Kreutzwaldi 1, Tartu, 51014, Estonia. E- mail: [email protected] b Department of Plant Protection, Institute of Agricultural and Environmental Sciences, Estonian University of Life Sciences. Kreutzwaldi 1, Tartu, 51014, Estonia.

Abstract

Growing cultivars less susceptible to raspberry beetle (Byturus tomentosus De Geer) reduces the need for chemical control and therefore has great impact in environmentally friendly raspberry production. To determine the susceptibility of raspberry cultivars to raspberry beetle, larval damage to raspberry cultivars in the collection at Polli Horticultural Research Centre of the Estonian University of Life Sciences, Estonia was determined during the years 2003-2011. 17 cultivars: Aita, Alvi, Herbert, Ivars, Novokitaivska, Preussen, Tomo, Algonquine, Ottawa, Haida, Helkal, Glen Ample, Glen Magna, Glen Rosa, Nagrada, Norna and Veten were assessed. The early flowering cultivars were significantly more damaged than the late flowering cultivars. The most damaged cultivars were Ivars and Novokitaivska. The lowest damage occurred in late flowering cultivars Glen Ample and Glen Magna. Late flowering cultivars are phenologically more isolated from the raspberry beetle. Growing the late flowering and less susceptible cultivars is a promising alternative to minimise raspberry beetle damage in integrated pest management and organic farming systems.

Keywords: Byturus tomentosus; fruit damage; raspberry beetle; raspberry cultivars; Rubus idaeus,

65 1. Introduction

Raspberry (Rubus idaeus L.) yield loss or reduction in the quality of fruits caused by a wide range of insects and other arthropod pests depends on several factors including cultivar (Gordon et al. 1997; Vétek and Pénzes 2008). Raspberry beetle (Byturus tomentosus De Geer) (Coleoptera: Byturidae) is the major pest of cultivated raspberry in many countries of Europe (Gordon et al. 1997), especially in northern Europe, where up to 50% of fruits damaged by raspberry beetle have been found in some plantations (Tuovinen 1997; Woodford et al. 2000; Hanni and Luik 2001; Kikas et al. 2002; Woodford et al. 2003). Both adults and larvae can cause damage (Willmer et al. 1998). After hibernation in the soil, adult beetles feed and mate on raspberry, eating the leaves, flower buds and pollen (Gordon et al. 1997). The females lay their eggs in flowers or developing fruits. The main damage is caused by the larvae which tunnel into the developing fruits resulting in their discolouration and contamination, and leading to the rejection or down-grading of the crop (Taylor and Gordon 1975). Damaged fruits can also become infected by grey mould (Botrytis cinerea Pers.) thus further reducing their storage quality (Woodford et al. 2002).

In choosing suitable oviposition sites, raspberry beetles use visual and olfactory cues. They locate raspberry flowers through response to their volatile profile (Birch et al. 1996; Woodford et al. 2003). The volatile profile of the flowers as well as their production of nectar varies with the phenological age of the flowers (Willmer et al. 1998) conveying additional information to female beetles (Robertson et al. 1995). Two components of the volatile profile are particularly attractive to the raspberry beetle (Woodford et al. 2003). Raspberry flowers are notable for the profusion of their nectar secretion and there are significant differences between cultivars (Willmer et al. 1994; Schmidt et al. 2012). The nectar attracts the beetles and Willmer et al. (1998) showed that its production is a factor limiting oviposition by the beetles.

Therefore, it is important to determine the susceptibility of raspberry cultivars to this pest and to find cultivars which will reduce the need for chemical control. Raspberry beetle is commonly controlled by synthetic chemical insecticides, often sprayed prophylactically (Gordon et al. 1997). Decreased pesticide use has a positive impact on the environment and also improves the quality, including antioxidant activity, of fruits (Worthington 2001; Asami et al. 2003).

Finding less susceptible cultivars to raspberry beetle gives additional possibilities for integrated pest management. Therefore, a long term study (2003-2011) was carried out to compare raspberry beetle damage to 17 raspberry cultivars with different flowering times.

2. Materials and methods

Experimental site and growth conditions The study was conducted over nine years, 2003-2011, in the collection of raspberry cultivars at the Polli Horticultural Research Centre of the Estonian University of Life

66 Sciences in Southern Estonia (58˚7´N, 25˚33´E). The collection was established in 2000. Plots of each cultivar were allocated in three replicates, with four plants in each replicate. The canes were planted in rows with 3.0 m between rows and 0.5 m between canes. Coarse grasses consisting mostly of Poaceae with Trifolium and Taraxacum grew between the raspberry rows; these were cut regularly. No pesticides were applied and no organic mulch material or irrigation was used.

Sampling and damage estimation

All ripe raspberry fruits were harvested three times per week for 3-5 weeks, depending on the year’s weather conditions, in all study years. Fruits damaged by the raspberry beetle, including fruits with damaged husks, and undamaged fruits were picked and weighed separately. The damage level of the raspberry beetle was calculated as a percentage of the total yield. The damage level was estimated in 17 cultivars: Aita, Alvi, Tomo (cvs of Estonian origin), Ivars (Latvia), Novokitaivska (Ukraine), Preussen (Germany), Algonquine, Ottawa, Haida, Herbert, Veten (Canada), Helkal (Estonia), Glen Ample, Glen Magna, Glen Rosa (UK), Nagrada (Russia) and Norna (Norway).

Meteorological conditions

Temperature and precipitation were recorded at a weather station in Polli, close to the experimental site. Weather conditions are important for successful overwintering of the beetles and for the development of raspberry beetle damage. During spring and summer months, the raspberry flowers and fruits form and the beetles are mating and ovipositing. During most study years, the mean temperature in May was more than 1 ˚C higher than the long-term average. June mean temperatures varied from year to year and were about 3 ˚C higher in 2006 and 2011 than the long term average (Table 1). The spring and summer of 2006 was the hottest and driest; the total rainfall was much less than the long term average and unsuitable for raspberry plant growth, flowering and yield formation and also influenced the insect’s behaviour. By contrast, June in 2004 and 2008-2009 was wet, and the amount of rainfall exceeded the long term average; conditions for plant growth and yield were good but less suitable for adult raspberry beetle mating and oviposition.

Statistical analysis

Raspberry beetle damage levels were analysed by one- and two-way ANOVA. The significance of differences was controlled by Tukey test at p<0.05 level. Regression analyses were used to find the relationship between the start of flowering of cultivars and raspberry beetle damage levels.

3. Results

The dates for the beginning of flowering varied with cultivar. Early flowering cultivars Aita, Alvi, Herbert, Ivars, Novokitaivska, Preussen and Tomo started to flower between 5

67 and 7 June. Late flowering cultivars Glen Ample, Glen Magna, Glen Rosa, Nagrada, Norna and Veten started flowering 10 days later (Table 2).

Comparing average damage levels of all studied cultivars during the study years, two raspberry beetle population peaks are apparent with quite high damage levels in 2003 and 2010-2011. The highest damage level was in 2003 (21.0% on average). Thereafter, the population gradually decreased with very low damage levels of only 0.1-0.2% during 2006-2009. A new population increase started from 2010 when the damage level reached 11.5%, increasing in the following year, to 15.9% although this was still lower than in 2003 (Figure 1).

The biggest differences in damage levels between cultivars appeared in years when the beetle population was high; in 2003, 2010 and 2011 (Table 2). During these years early flowering cultivars tended on average to be more damaged than late flowering cultivars. In 2003, more than a quarter of the fruits of the early flowering cultivars Novokitaivska, Preussen, Ivars and Herbert were damaged. By contrast, late flowering cultivars Glen Magna and Glen Ample had damage levels of less than 5%. In 2004, some of the early flowering cultivars Alvi, Aita and Herbert had 10% damaged fruits, whereas most of the late flowering cultivars had no damage. Cultivars Novokitaivska and Ivars, which are usually more attractive to the raspberry beetle, did not have any damage in 2004. In 2005, the damage level was low in all cultivars, although early flowering cultivars still tended to have more damage. From 2004 to 2009, all cultivars had a very low damage level; a little higher but significantly different damage level appeared only in cultivar Novokitaivska. In 2010, again early flowering cultivars Herbert, Novokitaivska, Aita, Tomo and Ottawa were more damaged (>15%) than late flowering cultivars Glen Rosa, Glen Magna, Nagrada and Glen Ample (<5%). In 2011, raspberry beetle damage level increased in all cultivars (Table 2). Linear regression analysis showed that the early flowering cultivars were clearly more damaged by raspberry beetle than the late flowering cultivars in five study years 2003, 2006 and 2008-10 (r=-0.443, p=0.014 in 2003; r=-0.418, p=0.03 in 2006; r=-0.546, p=0.02 in 2008; r=-0.439, p=0.03 in 2009 and r=-0.566, p=0.018 in 2010). Thus, overall, the linear regression analysis for all study years and for all cultivars showed that there is a strong relationship (r=-0.736) between the beginning of flowering and raspberry beetle damage levels and early flowering cultivars were more damaged than late flowering cultivars (Figure 2).

Comparison of the average damage levels of cultivars during the study years showed that the early flowering cultivars Novokitaivska and Ivars with their highest damage levels of 10.2 and 9.7% were the most susceptible to raspberry beetle (Figure 3). In contrast, the late flowering cultivars Glen Ample and Glen Magna were the least susceptible to raspberry beetle with the lowest damage levels of 2.1 and 2.6%.

4. Discussion

This nine year study has shown two damage peaks of raspberry beetle explainable by the higher number of individuals in the population dynamics of the species. A low damage level should correlate with a low number of beetles. Several authors (Willmer et al. 1996;

68 Szántóné Veszelka and Fajcsi 2003; Woodford et al. 2003) have shown that the occurrence of raspberry beetles on the host plant is extremely variable between seasons. Population dynamics is influenced by weather conditions. Temperature and precipitation influence raspberry development as well as raspberry beetle activity and behaviour. Temperature and moisture conditions during overwintering and spring determine the emergence success of beetles from the soil after hibernation, temperature also influences feeding, mating and oviposition. Under laboratory conditions, raspberry beetle is capable of flight at 15 ˚C, so flight activity is therefore common only in the early afternoon of warm days; furthermore, compared to mature beetles, the young adults are very sensitive to water loss reducing their hygric stress by remaining in humid microclimates (Willmer et al. 1996). Comparing temperature and precipitation levels in May to July (Table 1) and raspberry beetle damage levels (Figure 2) then it seems that drier (2006) and wetter (2004, 2008-09) or warmer (2005-07) weather conditions in spring months correlate with lower damage levels and hence with low raspberry beetle population.

Raspberry flowering depends on weather conditions and cultivar. Modern cultivars have differing phenologies, flower and fruit sizes and ripening speeds (Jennings 1988). Woodford et al. (2003) reported that adult beetles are on the raspberry plants at least 3 weeks before they flower and that the highest number of beetles is usually recorded before flowers open. However, the beetles stayed in the plantation during the whole flowering period. The latest studies have also shown that pest activity in raspberry plantations is much earlier than previously expected (Baroffio et al. 2011; Baroffio and Mittaz 2011). The present study has shown that early flowering raspberry cultivars are, on average, more damaged by raspberry beetle than later flowering cultivars. This indicates that the phenology of the beetle is better synchronized with early flowering cultivars. It should be noted that the physical proximity of one cultivar to another in the cultivar collection might influence oviposition decisions by beetles differently than if beetles were exposed to an entire field of one cultivar. On the other hand, cultivar choice within a collection may show cultivar susceptibility to the pests or other organisms in a more pronounced fashion. The highest damage levels occurred in the early flowering cultivars Novokitaivska and Ivars. The attractiveness of Novokitaivska to raspberry beetle has been mentioned in earlier studies (Hanni and Luik 2001; Kikas et al. 2002). Possibly these cultivars have more attractive plant-specific factors which affect oviposition choice. Willmer et al. (1998) indicated that raspberry beetles prefer to oviposit in cultivars with drier flowers which apparently emit a short-lived attractive volatile cue. The lowest damage levels were in the late flowering cultivars Glen Ample and Glen Magna; these cultivars may emit less attractive volatiles or nectar compounds. But, an average lower damage level of late flowering cultivars indicates that beetles’ egg laying period is apparently not well correlated with late flowering.

Several wild Rubus species, R. coreanus Miq., R. crataegifolius Bunge, R. occidentalis L. and R. phoenicolasius Maxim. have been considered as sources of resistance for raspberry beetle (Keep 1976; Keep et al. 1980; Briggs et al. 1982; Finn and Hancock 2008). Their derivates and the purple raspberry cultivar Glen Coe (Jennings et al. 2003) and also primocane raspberry cultivars (Jennings et al. 1991) have all shown some level of resistance to larval damage. But it became evident that damage is absent

69 because the beetle mating period does not coincide with the flowering time of these primocane cultivars.

The present study has shown that, in general, late flowering cultivars are less damaged by raspberry beetle. Apparently, beetles are not well adapted for oviposition in late flowering times. In environmentally friendly raspberry production the use of late flowering, more resistant cultivars is recommended first, combined with the use of volatile-enhanced white sticky traps which are an alternative to insecticide control (Woodford et al. 2003). Their use could be an alternative method to control raspberry beetle especially in integrated pest management and organic production (Schmid et al. 2006; Baroffio et al. 2011). In areas with wild raspberries the traps are less attractive and do not work effectively probably due to high immigration rates of adult raspberry beetles from surrounding wild raspberry during flowering (Trandem et al. 2008; Baroffio et al. 2012).

Oviposition by raspberry beetle in raspberry flowers is a function of insect and plant phenology, both of which vary somewhat independently among years. The dates that beetles emerge from overwintering depend on winter and spring temperatures, and the latter also influence beetle flight, mating and egg-laying. Thus, even for susceptible cultivars, the timing of mated egg-laying females will not always coincide with the timing of open raspberry flowers. For further development of integrated production of raspberry and breeding of less susceptible cultivars to raspberry beetle the raspberry plant and beetle mutual interactions need to be studied in detail. Further investigations are needed to find correlations between flower specific factors and beetle damage in different cultivars.

Acknowledgements

This study was supported by the grant from the Estonian Ministry of Agriculture and by target financed projects, Estonian, SF0170057s09 and SF1092711s06. The authors thank I. Williams for correcting the English.

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Table 1. May-July mean temperatures and precipitation rates in 2003-2011 and long- term averages in Estonia.

2003 2004 2005 2006 2007 2008 2009 2010 2011 Long-term averages (1922-2008) Temperature (˚C) May 11.8 11.3 11.7 11.8 11.7 10.8 11.2 12.0 11.3 10.2 June 14.1 14.6 15.3 17.0 15.9 13.3 13.6 14.1 17.8 14.4 July 20.5 17.8 18.7 20.2 16.4 16.1 16.6 21.5 20.4 16.7 Precipitation (mm) May 74.9 38.7 73.7 20.2 63 26.2 14.4 74.2 58.2 50 June 68.5 125.4 78.2 28.3 46 114.9 148.8 84.2 21.7 67 July 81 74.8 68.9 13 81.4 77.6 120.6 92.8 66.9 81

25.0 21.0 a

20.0 15.9 b

15.0 11.5 c

10.0

Damaged fruits (%) 4.2 d 5.0 2.7 e 0.2 fg 0.1 g 0.1 fg 0.2 f 0.0 2003 2004 2005 2006 2007 2008 2009 2010 2011 Year

Figure 1. The raspberry beetle average damage level (± standard deviation) from total yield on an average of all cultivars in 2003-11. Means followed by the different letter differ significantly (p<0.05; two-way ANOVA, Tukey test).

73 7.4 i 7.4 i 8.8 h 8.8 h 8.2 hi 8.2 hi 12.1 f f 12.1 f 11.5 16.0 e e 16.0 c 21.1 17.2 d d 17.2 b 23.5 3.5 f 3.5 f 3.4 f 3.9 f 3.9 f 24.2 a a 24.2 a 26.4 8.6 def 8.6 def 20.5 ab ab 20.5 b 23.3 20.9 ab ab 20.9 f 12.5 12.4 b-e b-e 12.4 b 24.5 12.4 b-e b-e 12.4 e 15.5 a-d 16.8 a-d 14.7 e 16.0 g 10.2 b-e 12.0 e 15.3 16.4 abc abc 16.4 0.1 d 0.1 d 0.1 d 0.1 d 0.1 cd 0.1 cd 4.8 f 0.2 a-d 0.2 a-d 0.2 a-d 0.2 a-d 9.0 c-f 0.1 bcd 0.1 bcd 0.1 bcd 0.1 bcd 0 c 0 c 0.1 bc 0.1 bc 0.1 bc 0.1 bc 0.1 bc 0.1 bc 0.1 bc 0.1 bc 0.1 d 0 c 0 c 0.1 bc 0.1 bc 0.1 bc 0.1 d 0.1 abc 0.1 abc 0.1 abc 0.1 abc 0.1 abc 0.1 ab 0.1 abc 0.2 ab 0.1 abc 0.2 ab 0.3 abc 0 c 0 c 0.4 a 0.4 a 0.3 a 0.3 a 0.4 a 0.1 c 0.1 abc 0.1 bc 0.1 bc 0.1 bc 0.1 bc 0.1 bc 0.2 ab 0.1 abc 0.1 bc from total yield in raspberry in 2003-11. total cultivars Means from yield followed 7.5 a 7.5 a 0.2 ab 0.1 abc 0.1 abc 0.3 ab 0.9 g 0.9 g 1.2 fg 1.2 fg 3.9 bc 3.9 bc 3.9 bc 5.6 ab 0.2 ab 0.2 ab 0.1 ab 0.3 ab 5.7 ef 2.6 c-f 2.6 c-f 0.3 a 0.2 ab 2.5 c-f 2.5 c-f 0.3 a 0.2 ab 0.2 ab 0.3 abc 6.1 ef 1.7 efg 1.7 efg 0.3 a 0.1 abc 0.2 ab 0.2 abc 1.3 efg 1.3 efg 1.3 efg 1.3 efg 0.1 c 0.1 c 0.1 abc 1.2 efg 1.2 efg 0.3 a 0.1 abc 0.2 ab 0.3 ab 1.8 d-g 1.8 d-g p <0.05; one-way ANOVA, test). Tukey 3.8 bcd 3.8 bcd 3.4 bcd 3.4 bcd 0 d 0 d 0 d 0 d 0 d 0 d 0 d 0 d 0 d 4.1 c 4.1 c 2.7 cde 7.2 b 7.2 b 7.6 b 5.7 bc 5.7 bc 6.6 bc 6.6 bc 3.8 j 3.8 j 3.0 j 2003 2003 2004 2005 2006 2007 2008 2009 2010 2011 5 June 5 June 5 June 5 June h 15.9 5 June ef 21.1 5 June a 12.3 cd 25.2 a 15.3 7 June bc 28.1 a 12.3 5 June a 52.7 b 31.5 def 22.1 12 June 12 June 11 June 14 June ef 21.4 14 June gh 17.9 15 June d 24.8 15 June fg 20.4 16 June 15 June 15 June h 17.0 15 June h 15.4 i 12.7 de 24.2 Beginning of flowering. Average of 2003-11 Cultivar Aita Alvi Herbert Ivars Novokitaivska Preussen Tomo Alonquine Ottawa Haida Helkal Ample Glen Glen Magna Rosa Glen Nagrada Norna Veten Table 2 . The average percentages of beetle raspberry damage levels by the same letter in the column did not differ significantly significantly ( differ not the did in same the column letter by

74

12.0

Novikitaivska y = -0.7403x + 48.434 Ivars 10.0 R2 = 0.5414 Preussen r= −0.736; p<0.001 8.0 Aita Veten Alvi Tomo Haida 6.0 Herbert Algonquine Helkal Glen Rosa Ottawa Norna 4.0 (%) fruits Damaged Nagrada Glen Magna 2.0 Glen Ample

0.0 53.0 54.0 55.0 56.0 57.0 58.0 59.0 60.0 61.0 62.0 Flowering after beginning of vegetation (days)

Figure 2. Relationship between the raspberry beetle damage level (%) and beginning of flowering times of cultivars in 2003-11.

12.0 a ab 10.2 9.7 10.0 ab ab 8.3 abc abc 8.6 abc 8.0 7.4 a-d 7.1 abc a-d 7.2 6.4 a-e a-d 6.0 6.0 cde b-e 6.0 5.6 5.2 4.9 4.8 de 3.6 4.0 e Damaged fruits (%) e 2.6 2.1 2.0

0.0

Aita Alvi Ivars Tomo Haida Norna Veten Ottawa Helkal Herbert Nagrada PreussenAlonquine Glen Rosa Glen AmpleGlen Magna Novokitaivska Cultivars

Figure 3. The study years (2003-11) average percentages of raspberry beetle damage level from total yield in raspberry cultivars. Means followed by the same letter did not differ significantly (p<0.05; one-way ANOVA, Tukey test).

75

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83 Arus, L., Luik, A., Monikainen, M. and Kikas, A. 2011. DOES MULCHING INFLUENCE POTENTIAL PREDATORS OF RASPBERRY BEETLE? Acta Agriculturae Scandinavica, Section B - Plant Soil Science 61(3): 220–227. This article was downloaded by: [Estonian University of Life Sciences] On: 05 October 2011, At: 22:03 Publisher: Taylor & Francis Informa Ltd Registered in England and Wales Registered Number: 1072954 Registered office: Mortimer House, 37-41 Mortimer Street, London W1T 3JH, UK

Acta Agriculturae Scandinavica, Section B - Soil & Plant Science Publication details, including instructions for authors and subscription information: http://www.tandfonline.com/loi/sagb20 Does mulching influence potential predators of raspberry beetle? Liina Arus a , Anne Luik b , Martin Monikainen b & Ave Kikas a a Estonian University of Life Sciences, Institute of Agricultural and Environmental Sciences, Polli Horticultural Research Centre, Kreutzwaldi 1, Tartu, Estonia b Estonian University of Life Sciences, Institute of Agricultural and Environmental Sciences, Department of Plant Protection, Kreutzwaldi 1, Tartu, Estonia

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85 Acta Agriculturae Scandinavica Section B Soil and Plant Science, 2011; 61: 220227

ORIGINAL ARTICLE

Does mulching influence potential predators of raspberry beetle?

LIINA ARUS1, ANNE LUIK2, MARTIN MONIKAINEN2 & AVE KIKAS1

1Estonian University of Life Sciences, Institute of Agricultural and Environmental Sciences, Polli Horticultural Research Centre, Kreutzwaldi 1, Tartu, Estonia, 2Estonian University of Life Sciences, Institute of Agricultural and Environmental Sciences, Department of Plant Protection, Kreutzwaldi 1, Tartu, Estonia

Abstract The effect of different mulches on carabid abundance and species composition was studied using pitfall traps in the Polli experimental raspberry plantation in the years 20012003 and 2006. Experimental treatments compared were: control soil with no mulch and different mulch treatments birch sawdust, milled peat, barley straw and black plastic. To estimate the potential role of carabids in raspberry beetle population regulation, the population dynamics of the dominant carabid species in relation to raspberry phenophases was determined. The activity density and species richness of carabids increased with plantation age and were influenced by mulching. In all study years, at the time of ripening of the raspberry fruits, when the raspberry beetle larvae leave the fruits to pupate in the soil, the most dominant carabid species were: Pterostichus vulgaris, Pterostichus niger, Carabus nemoralis and Harpalus pubescens. The barley straw mulch was significantly preferred to the other mulches by P. niger, P. vulgaris and C. nemoralis. H. pubescens did not exhibit a preference for a particular mulch. These four carabid species could be potential key predators of raspberry beetle larvae in Nordic plantations of perennial raspberry.

Keywords: Abundance, barley straw, black plastic, Carabus nemoralis, Harpalus pubescens, peat, Pterostichus niger, Pterostichus vulgaris, sawdust.

Introduction reported (Tuovinen, 1997). Raspberry beetle is gene- rally controlled by pesticides, but pesticide residues in Raspberry (Rubus idaeus L.) is the most widely grown flowers and fruit can be detrimental to organisms that top fruit crop of all Rubus species throughout the world. In Estonia, 220 hectares of raspberry planta- feed on them. Sublethal doses of residues in nectar tion were grown in 2008 (Statistics Board, 2009). and pollen can cause physiological dysfunction in In northern Europe, raspberry is often grown in a bees, parasitoids and predators (Gels et al., 2002; 1015-year rotation and, in many cases, synthetic and Ramirez-Romero et al., 2005; Rogers et al., 2007). organic mulches are used. Mulching for weed control is Clinical research has revealed that residues in food can cause dysfunction of the immune and hormonal

Downloaded by [Estonian University of Life Sciences] at 22:03 05 October 2011 used in agriculture worldwide (Gupta, 1991). Straw and other organic mulches, as well as black plastic, systems in humans leading to the development of suppress weed emergence (Jodaugiene˙ et al., 2006). allergies and tumours (Walsh, 2000; De Roos, 2003). Organic mulches improve the moisture conditions of Therefore, it is desirable to investigate alternative the soil by reducing water evaporation and also favour strategies for the regulation of raspberry beetle soil micro-organisms, thereby influencing plant health. populations without pesticides by developing agro- Although many arthropods are found in raspberry nomic practices which enhance the natural enemies of plantations, only a few of them can cause yield loss the beetle. After a feeding period in the berries, or reduction in fruit quality (Gordon et al., 1990). raspberry beetle larvae fall to the soil for pupation and In northern Europe, the raspberry beetle (Byturus are then possible targets for carabids and other tomentosus F.) is the most serious pest attacking ground-living predators. Phytophagous fauna are raspberries. Yield losses of up to 50% have been regulated by polyphagous predatory insects and

Correspondence: L. Arus, Estonian University of Life Sciences, Institute of Agricultural and Environmental Sciences, Polli Horticultural Research Centre, Kreutzwaldi 1, Tartu, 51014, Estonia. E-mail: [email protected]

(Received 8 October 2009; revised 16 February 2010; accepted 22 February 2010) ISSN 0906-4710 print/ISSN 1651-1913 online # 2011 Taylor & Francis DOI: 10.1080/09064711003720261

86 Does mulching influence potential predators of raspberry beetle? 221

spiders, which are dependent on food resources and area was 1250 m2. Between raspberry rows (a 2-m microclimatic conditions and are usually abundant in wide area) the rough herbage consisted mostly of fields where more nature-friendly growing technolo- Gramineae and Trifolium, but included some weeds, gies are used (Sunderland & Vickerman, 1980; Luik such as Elymus repens L. and Taraxacum officinale; et al., 2000). The relationship between carabids and this was cut regularly. raspberry beetle larvae has not been studied. In Experimental treatments were mulches of birch Europe, potential prey species for carabids, depend- sawdust, milled peat, barley straw, black plastic and ing on their life style, include different insect larvae, for control soil without any mulch. Black plastic was set including those of the raspberry beetle, thrips, Otior- before planting, as a synthetic mulch. The organic hynchus spp. weevils, eggs of Lepidoptera and the larvae mulches (15-cm layer) were added after planting and of Resselia theobaldi. Large carabids, in sufficient new layers of sawdust, peat and straw were added every densities, can be efficient predators of the egg and spring at the end of May. No pesticides were applied. larval stages of Coleoptera; experiments have shown Pitfall traps were used to sample carabids. Pitfall that those of the genus Carabus, Pterostichus vulgaris, trapping is the most widely used sampling technique and P. n i g e r effectively control Leptinotarsa decemlineata for carabids (Luff, 1987; Kromp, 1999), particularly in (Thiele, 1977). Raspberry beetle larvae are also agricultural habitats, where it provides a cheap and attacked by hymenopterous parasitoids, up to 26% simple method of catching a large number of indivi- in some cases (Hanni & Luik, 2006). Considering the duals of diverse species. Carabids fall into the traps predatory polyphagous nutrition of most carabids they where they are preserved in liquid; their abundance and can play a definite role in agro-ecosystems as natural activity density can then be characterized at the same pest-control agents (Kromp, 1999). time. The traps were placed in the middle of the Several studies report that organic mulches influ- raspberry experimental plots between plants (one trap ence the abundance of carabids and spiders in per plot, in total four traps in every experimental horticultural crops. In apple orchards, fewer carabids treatment). The traps (9-cm diameter, 10-cm high) were trapped where black plastic rather than a straw were made of plastic and filled with a 10% salt water mulch was used (Minano & Dapena, 2003). In solution. The traps were placed in position 2 weeks strawberry plantations, black plastic mulch increased before flowering of the raspberries and removed at the the population of cyclamen mites and spider mites but end of fruit ripening. Traps were checked and arthro- did not significantly influence carabids (Kivija¨rvi et al., pods collected at 7-day intervals. Captured carabids 2002); spiders were more abundant in the treatment were identified and counted in the laboratory. Identi- with straw mulch (Jo˜gar et al., 2001). fication to species was aided by the extensive university The aim of the present study was to establish the collection of carabids. The taxonomic nomenclature of effect of birch sawdust, milled peat, barley straw and carabid species follows that of Haberman (1968) and black plastic mulches on carabid abundance and Silferberg et al. (2004). species composition in raspberry plantations. Also, Temperature and precipitation for the experi- the population dynamics of dominant carabid spe- mental site were recorded at a weather station in Polli. cies in relation to raspberry growth stages was The carabid data from different mulch treatments studied to estimate the potential role of carabids in were analysed with the one- and two-way ANOVA, raspberry beetle population regulation. post-hoc LSD and Tukey’s multiple comparison test.

Downloaded by [Estonian University of Life Sciences] at 22:03 05 October 2011 Materials and methods Results The experiment comparing different mulches on Weather data for JuneAugust of each experimental carabid abundance was carried out in the years year are summarized in Table I. In June of experi- 20012003 and 2006 in a raspberry plantation mental years the mean air temperature was similar to at Polli Horticultural Research Centre, in south the average of many years. Averages of temperatures Estonia (latitude 5887?N and 25833?E). In 2004 of July and August of study years were higher than 05, there were no studies of carabids. The plantation average of many years. Total rainfall from June to with two raspberry varieties (‘Novokitaivska’ and August of 200103 and 2006 was 313 mm, 183 mm, ‘Tomo’) was established in 1998 and 2001 was the 274 mm and 99 mm, respectively. Thus summer first yielding year. The canes were planted in rows 2001 could be described as wet since the amount of with spacing 3.0 m between rows and 0.5 m between rainfall exceeded the average of many years in all canes. There were five raspberry rows, to which the three months. By contrast, summer 2006 was dry; different mulching treatments were allocated at the total rainfall was less than half the average of random, each treatment in four replicates. Each many years (202 mm). From the end of June to the replicate area was 7.5 m2. The total experimental end of July in 2006 there was only 13 mm of rain.

87 222 L. Arus et al. Table I. Weather data for the summer months June August in preferred barley straw beds (pB0.05) to the milled 2001, 2002, 2003 and 2006 in south Estonia. peat; differences between these two mulches and the Temperature (8C) June July August others were not significant (p 0.05) (Figure 1). In an average of study years, from flowering time 2001 14.9 21.0 17.6 until the end of ripening time of raspberries, the 2002 16.8 19.8 18.8 most abundant carabid species (more than 7%) 2003 14.1 20.5 17.0 2006 17.0 20.2 18.5 were Pterostichus niger (23.9%), P. vulgaris (9.7%), Harpalus pubescens (9.4%) and Carabus nemoralis Monthly mean 19661998 15.1 16.8 15.7 (7.7%) (Table II). Activity density of these species Rainfall (mm) June July August increased with the beginning of fruit set, which is the time of the raspberry beetle larval development, and 2001 86 135 92 decreased at the end of this period (Figures 36). 2002 111 60 12 The increase in abundance was especially clear in the 2003 68 81 125 2006 28 13 58 case of P. niger. Comparing the influence of mulches on the Total monthly mean 19611990 51 73 78 occurrence of dominant carabid species then P. vulgaris did not prefer any mulch to the others in Species richness of carabids increased with the an average of 4 study years (Figure 2A). Significant plantation age (Table II). In 20012003, species differences between mulches (weekly catches) of P. number increased yearly from 29 to 32 species vulgaris were found only in the very dry year 2006, belonging to a total of 15 genera. In 2006, 45 when in the week before ripening time of fruits the species from 18 genera were found. In all study barley straw mulch beds were preferred to the others years, the specimens of the genera Pterostichus and (Figure 3). Pterostichus niger and C. nemoralis pre- Harpalus dominated in all experimental treatments. ferred barley straw mulch to the peat, sawdust and In 2006, the genus Pterostichus (61% of all indivi- no mulch treatments on average (Figure 2B,C). The duals) dominated with specimens of the genus preference of mulching treatments to the no mulch Carabus also numerous (more than 10%). beds was very clearly seen in 2006, in the extremely Carabid abundance was influenced by year and by dry year. In that case, the barley straw treatment was the type of mulch (Figure 1). In 2001, 2002 and preferred to the peat, sawdust and black plastic (pB 2006, there were significant differences in the total 0.05). carabid catches between different mulching treat- In P. niger, there were significant differences ments. In 2001, carabids preferred barley straw between mulching treatments in weekly catches in mulch to the black plastic mulch, with 43 and 27 the first and second week of the raspberry ripening individuals respectively per trap (pB0.05). In 2002, period in 2001, 2002 and 2006 (Figure 4). In 2001, all mulches were preferred, even black plastic (5154 P.niger preferred barley straw to the black plastic and individuals per trap), to the no mulch control (36 the peat mulches. In 2002, P. niger preferred in the individuals per trap). In the last experimental year second week barley straw to the other mulches, and (2006) barley straw beds were also preferred by in the third week sawdust to the control. In the last carabids (114 specimens) while the milled peat year also barley straw was significantly preferred to

Downloaded by [Estonian University of Life Sciences] at 22:03 05 October 2011 mulch was preferred least (59 specimens). On the other mulching treatments in the second and average, in all study years carabids significantly third weeks (Figure 4AD).

Table II. The abundance of carabids and of the dominant species caught in pitfall traps in different years from flowering to the end of ripening period and in the fruiting period.

Species 2001 2002 2003 2006 % of the years

Carabus nemoralis 29 (13.4%) 25 (4.5%) 2 (0.4%) 116 (11.6%) 7.7 Harpalus pubescens 30 (9.6%) 83 (14.9%) 52 (11%) 26 (2.6%) 8.1 Pterostichus niger 68 (31.5%) 204 (36.7%) 72 (15.3%) 437 (43.8%) 34.8 Pterostichus vulgaris 35 (16.2%) 76 (13.7%) 17 (3.6%) 106 (10.6%) 10.4 Total no. of individuals 692 725 899 1214 Total no. of individuals in fruiting period 216 556 472 998 Total no. of species 29 30 32 45 Total no. of species in fruiting period 22 28 29 35

88 Does mulching influence potential predators of raspberry beetle? 223

140 d

120 ns c b b 100 bc b ab ab ab 80 a ab b bbb a a 60 b ab a ab ab a 40 a

20 Number of individuals per trap ± SE

0 Peat Peat Peat Peat Peat y2001 y2002 y2003 y2006 Sawdust Sawdust Sawdust Sawdust Sawdust Straw litter Straw litter Straw litter Straw litter Straw litter Black plastic Black Black plastic Black Black plastic Black plastic Black Black plastic Black Without mulching Without mulching Without mulching Without mulching Without mulching 2001 2002 2003 2006 Effect of mulching Effect of the year

Figure 1. Number of Carabidae in different mulching treatments of raspberry in 20012003 and 2006, calculated as replicate means9SE. Different letters in columns indicate significant differences between treatments, two-way ANOVA, pB0.05, nsnot significant.

In C. nemoralis in weekly catches differences was a preference for the control no mulch treatment between mulches were not significant in all experi- to the others (Figure 6). mental years (Figure 5). Harpalus pubescens did not prefer any mulch to the Discussion others over an average of 4 years (Figure 2D); but there were differences in different years in 2002, The abundance of the carabid community in rasp- barley straw and black plastic were preferred to the berry varied with the age of the plantation and with peat mulch; in 2006, sawdust was preferred to the the different treatments applied. peat and barley straw mulch but very few specimens The most numerous carabid species trapped were present. In weekly catches of H. pubescens there in this experiment, namely P. niger, P. vulgaris,

Without mulching A – Pterostichus vulgaris 50 B – Pterostichus niger 12 Saw dust Without mulching 45 Peat ns c Saw dust c Barley straw bc Peat 10 40 Black plastic abc Barley straw bc ns 35 Black plastic b ns b 8 30 ab ns 6 25 ab a a 20 a a a a 4 a a a a a 15 a ab a a ab 10 a 2 a a b 5 b Number of individuals per trap ± SE

Number of individuals per trap ± SE 0 0

Downloaded by [Estonian University of Life Sciences] at 22:03 05 October 2011 2001 2002 2003 2006 Av. effect of 2001 2002 2003 2006 Av. effect of mulching mulching

Without mulching 20 Without mulching D – Harpalus pubescens C – Carabus nemoralis Saw dust 14 Saw dust 18 Peat Peat b 12 Barley straw 16 Barley straw ns Black plastic ab 14 Black plastic 10 b 12 ns a b b 8 ab ab ns a 10 b a 6 ns 8 a ab ab a a 6 4 ab aa a ab b b 4 ab a ab 2 b ab a 2 a Number of individuals per trap ± SE

Number of individuals per trap ± SE 0 0 2001 2002 2003 2006 Av. effect of 2001 2002 2003 2006 Av. effect of mulching mulching

Figure 2. Effect of mulching treatments on the dominant carabid species (A Pterostichus vulgaris,B P. niger,C Carabus nemoralis and D Harpalus pubescens). Different letters in columns indicate significant differences between mulching treatments (two-way ANOVA, pB0.05, nsnot significant).

89 224 L. Arus et al.

6 6 A–Pterostichus vulgaris 2001 B–Pterostichus vulgaris 2002 Without mulching 5 Saw dust 5 Without mulching ns Peat ns Saw dust 4 Barley straw 4 Peat Black plastic Barley straw 3 3 Black plastic

2 2

1 1

0 0 Average no. of individuals ± SE Average no. of individuals ± SE 7.7 14.7 28.7 2.8 9.8 26.6 2.7 11.7 17.7 24.7 31.7 Ripening time Ripening time

2.5 C–Pterostichus vulgaris 2003 12 c D–Pterostichus vulgaris 2006 Without mulching 10 2 Saw dust Without mulching ns Peat 8 Saw dust 1.5 Barley straw Peat Black plastic 6 bc Barley straw 1 b Black plastic 4 ab a b 0.5 b 2 a a ab a aa ab a

Average no. of individuals ± SE 0 Average no. of individuals ± SE 0 24.6 30.6 7.7 14.7 5.7 11.7 19.7 28.7 2.8 9.8 Ripening time Ripening time

Figure 3. The effect of mulching treatments on Pterostichus vulgaris occurrence in different weeks in 2001, 2002, 2003 and 2006 (AD). Different letters in columns indicate significant differences between treatments (one-way ANOVA, pB0.05, nsnot significant).

H. pubescens and C. nemoralis were similar to those Both abundance and species richness in our reported earlier in raspberry and strawberry planta- experiment were greatest in the last study year. tions in Estonia (Luik et al., 2000; Kikas & Luik, Abundance of P. niger, P. vulgaris, H. pubescens and 2002, 2004) and in strawberry fields in Finland C. nemoralis generally increased with the age of the (Tuovinen et al., 2006). The genera Pterostichus, plantation. Barone and Frank (2003) have reported Harpalus and Agonum are common in European that the age of the habitat increases the abundance agricultural fields (Lo¨vei & Sunderland, 1996). of generalist predator species, and Levesque and

8 A–Pterostichus niger 2001 14 B–Pterostichus niger 2002 b 7 b Without mulching 12 Saw dust 6 Without mulching b 10 b Peat ab Saw dust Barley straw 5 ab ab Black plastic b Peat 8 4 Barley straw abab a Black plastic 6 ab 3 ab ab ab 4 ab 2 ab ab a a 2 a 1 aaa a Average no. of individuals ± SE 0 Average no. of individuals ± SE 0 Downloaded by [Estonian University of Life Sciences] at 22:03 05 October 2011 7.7 14.7 28.7 2.8 9.8 26.6 2.7 11.7 17.7 24.7 31.7 Ripening time Ripening time

8 C–Pterostichus niger 2003 25 D–Pterostichus niger 2006 Without mulching b Saw dust 7 Without mulching Peat ns 20 ab c 6 ab Barley straw Saw dust Peat 5 Black plastic 15 4 Barley straw Black plastic 3 10 ab a ab b 2 5 ab 1 a Average no. of individuals ± SE Average no. of individuals ± SE 0 0 24.6 30.6 7.7 14.7 5.7 11.7 19.7 28.7 2.8 9.8 Ripening time Ripening time

Figure 4. The effect of mulching treatments on Pterostichus niger occurrence in different weeks in 2001, 2002, 2003 and 2006 (A D). Different letters in columns indicate significant differences between treatments (one-way ANOVA, PB0.05, nsnot significant

90 Does mulching influence potential predators of raspberry beetle? 225

5 Without mulching A - Carabus nemoralis 2001 4 B - Carabus nemoralis 2002 4.5 Saw dust 3.5 Without mulching 4 Peat ns ns Barley straw Saw dust 3.5 3 Peat Black plastic 3 2.5 Barley straw 2.5 Black plastic 2 2 1.5 1.5 1 1 0.5 Average no. of individuals ± SE Average no. of individuals ± SE 0.5 0 0 7.7 14.7 28.7 2.8 9.8 26.6 2.7 11.7 17.7 24.7 31.7 Ripening time Ripening time

6 C - Carabus nemoralis 2006

5 Without mulching Saw dust ns 4 Peat Barley straw Black plastic 3

2

Average no. of individuals ± SE 1

0 5.7 11.7 19.7 28.7 2.8 9.8 Ripening time

Figure 5. The effect of mulching treatments on Carabus nemoralis occurrence in different weeks in 2001, 2002 and 2006 (AC). Different letters in columns indicate significant differences between treatments (one-way ANOVA, pB0.05, nsnot significant).

Levesque (1994) found that adult P. vulgaris were further support increase of carabids through the more abundant in old raspberry plantations than in presence of inter-row plant cover which offer further young ones. Raspberry plants with their perennial and different refuges. Such plant cover with Gramineae, roots and biennial canes may be kept for over 10 Trifolium, Elymus repens L. and Taraxacum officinale years thereby increasing ecological stability. Long- dominating also became more diversified with the term plantations are thus particularly suitable for age of plantation. The enemies’ hypothesis states local populations of predatory arthropods. They may that predatory insects and parasitoids are more

Without mulching A- Harpalus pubescens 2001 1.4 Saw dust 1.2 Peat Barley straw ns 1 Black plastic 0.8

0.6

0.4

0.2 Average no. of individuals ± SE Downloaded by [Estonian University of Life Sciences] at 22:03 05 October 2011 0 7.7 14.7 28.7 2.8 9.8 Ripening time

4.5 Without mulching B - Harpalus pubescens 2002 5 Without mulching C - Harpalus pubescens 2003 b 4 Saw dust c 4.5 Saw dust Peat 3.5 Peat 4 Barley straw Barley straw 3.5 3 Black plastic Black plastic 3 2.5 b ab 2.5 2 2 a 1.5 ab 1.5 aa 1 a 1 a Average no. of individuals ± SE Average no. of individuals ± SE 0.5 0.5 0 0 26.6 2.7 11.7 17.7 24.7 31.7 24.6 30.6 7.7 14.7 Ripening time Ripening time

Figure 6. The effect of mulching treatments on Harpalus pubescens occurrence in different weeks in 2001, 2002 and 2003. Different letters in columns indicate significant differences between treatments (one-way ANOVA, PB0.05, nsnot significant).

91 226 L. Arus et al.

effective in controlling populations of herbivores in (Thiele, 1977). Harpalus pubescens is also reported to diverse systems than in simple ones (Russel, 1989). be a predator, a biocontrol agent for the larvae of the Average effect of 4 years showed that beds brassica pod midge, a pest of oilseed rape (Bu¨chs, mulched by barley straw were significantly preferred 2003). Their mixed diet (animal/plant) may explain to milled peat mulch beds. Carabids are more the similar abundance of H. pubescens in our different abundant in plantations with sufficient food and mulch treatments. suitable microclimatic conditions. Soil temperature, Pterostichus niger and P. vulgaris are the most humidity, food availability, organic matter and abundant species in agricultural landscapes and shelter may be influenced by husbandry practices their diet is composed of up to 90% animal matter such as providing ground cover with mulch materi- (Thiele, 1977). Pterostichus spp. has consumed winter als. Carabid species respond differently to different moth (Oteropthera brumata L.) pupae (Horgan & mulches as their ecological requirements are deter- Myers, 2004) and was considered to be an important mined by size, shape, food preferences, temperature, early season predator of larvae of Cydia pomonella humidity and season (Lo¨vei & Sunderland, 1996). In in apple orchards (Riddick & Mills, 1994). It has raspberry plantations, organic mulches could pro- been reported that P. niger, P. vulgaris, C. nemoralis vide proper shelter and better food resources for and even H. pubescens might be efficient predators of carabids, especially in dry weather. Mulches change the eggs and larval stage of Leptinotarsa decemlineata microclimatic conditions temperature and humi- (Thiele, 1977). The key pests of raspberry larvae dity. The mulch influence is more apparent in Byturus tomentosus could be among the other prey. extreme climatic conditions as in the extremely dry The abundance of dominant carabid species P. summer of 2006, when the straw mulch was niger, P. vulgaris, C. nemoralis and H. pubescens significantly preferred by all dominant species P. increased significantly when raspberry fruits were niger, P. vulgaris and C. nemoralis. Soil moisture is beginning to ripen. This is when mature raspberry apparently higher and soil temperature lower under beetle larvae fall to the soil for pupation and may the straw than in the other treatments. This could provide potential food items for P.niger, P.vulgaris, C. explain the significantly greater abundance of cara- nemoralis and H. pubescens. Further laboratory ex- bids in the straw mulch, especially at the ripening periments are required to confirm the role of these time of raspberry. Periods with high air temperature species in controlling the raspberry beetle. and low rainfall are very common in Estonia. Black plastic raises soil surface temperature. Therefore, Acknowledgements especially in cool and rainy summers, the abundance of carabids was higher in black plastic treatment. In This study was supported by target financed pro- not very hot and dry years the catches of carabids in jects, Estonia, SF0170057s09 and SF1092711s06. the no mulch control were probably higher because The authors thank Ingrid Williams for correcting the here they had additional food resources thanks to the English. presence of some weeds in raspberry rows. Seasonal activity of most common dominant carabid species adults was typical for autumn breed- References ing species, with peak catches in July and the Barone, M., & Frank, T. (2003). 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IV Arus, L., Kikas, A. and Luik, A. 2012. Carabidae AS NATURAL ENEMIES OF THE RASPBERRY BEETLE (Byturus tomentosus F.). Žemdirbystė/Agriculture 99(3): 327–332. ISSN 1392-3196 ŽEMDIRBYSTĖ=AGRICULTURE Vol. 99, No. 3 (2012) 327

ISSN 1392-3196 Žemdirbystė=Agriculture, vol. 99, No. 3 (2012), p. 327–332 UDK 634.711:634.75

Carabidae as natural enemies of the raspberry beetle (Byturus tomentosus F.)

Liina ARUS1, Ave KIKAS1, Anne LUIK2 1Estonian University of Life Sciences, Institute of Agricultural and Environmental Sciences, Polli Horticultural Research Centre Kreutzwaldi 1, 51014 Tartu, Estonia E-mail: [email protected] 2Estonian University of Life Sciences, Institute of Agricultural and Environmental Sciences Kreutzwaldi 1, 51014 Tartu, Estonia

Abstract The raspberry beetle (Byturus tomentosus F.) is a widespread pest of raspberry in Europe. Although it is being controlled chemically, alternative strategies should be developed, based on biological control by polyphagous predators. Laboratory feeding tests were used to investigate the role of raspberry beetle larvae in the diet of the carabid species, Pterostichus melanarius, P. niger, Carabus nemoralis and Harpalus rufipes. In no-choice and choice feeding tests with aphids or raspberry beetle larvae P. melanarius and P. niger preferred to consume raspberry beetle larvae. C. nemoralis quickly consumed both prey items. H. rufipes preferred to eat raspberry beetle larvae to Thlapsi arvense seeds. According to the consumed biomass of each food item, larvae of the raspberry beetle were preferred by each carabid species tested. Data reported here clearly indicate that large carabids − P. melanarius, P. niger, C. nemoralis and H. rufipes could play an important role in regulating raspberry pest populations.

Key words: biological control, Carabidae, aphid, Byturus tomentosus larvae, prey preference.

Introduction Carabids are the most common predatory insects of the crop. Due to their hidden lifestyle, raspberry beet- and important natural enemies of many pests on agricul- le larvae are safe from predatory arthropods during their tural crops (Thiele, 1977), including horticultural crops. development in raspberries. But, after feeding in the ber- Most species are generalist predators, consuming both ries, they drop to the soil for pupation and are then pos- animal and plant material: leaves, fruits, pollen, seeds sible targets for carabids and other ground living preda- and fungi (Toft, Bilde, 2002). Considering the predatory tors. Aphids are also important and a highly preferred polyphagous nutrition of carabids, they play a key role prey type for carabids in many crops (Ekbom et al., 1992; in agro-ecosystems as natural biological control agents Kielty et al., 1999) but in raspberry, they are less impor- (Kromp, 1999). tant pests in North European outdoor conditions (Gordon Several studies have shown that carabids, in et al., 1997). sufficient densities, can be efficient predators of aphids There have been few studies on interactions be- tween carabids and raspberry beetle larvae. Carabids are as well as the egg and larval stages of Coleopteran, common ground living predators in raspberry plantations Lepidopteran and Dipteran pests (Thiele, 1977; Sorokin, (Luik et al., 2000; Hanni, Luik, 2002) with the species 1981; Riddick, Mills, 1996; Kromp, 1999; Büchs, 2003; Pterostichus melanarius (Illiger), P. niger (Schaller), Horgan, Myers, 2004). A review of manipulative field Carabus nemoralis Mueller and Harpalus rufipes (De- studies showed that, in approximately 75% of cases, pest Geer) being common and most numerous in northern numbers were reduced significantly by these generalist Europe. The seasonal abundance of these species, in predators (Symondson et al., 2002). addition to the high number of individuals, is related In Northern Europe, the raspberry beetle (By- to the ripening time of raspberry fruits which coincides turus tomentosus F.) is the most serious pest attacking with the raspberry beetle larval stage (Arus et al., 2011). raspberries with yield losses up to 50% depending on P. melanarius, P. niger, C. nemoralis are mainly carnivo- cultivar (Tuovinen, 1997; Hanni, Luik, 2001). The dam- rous (Thiele, 1977; Pollet, Desender, 1985). H. rufipes age is mainly caused by larvae browsing on the drupes has previously been reported as a biocontrol agent of va- of young fruits, resulting in discoloured or contaminated rious pests (Kromp, 1999) and is an effective seed eater ripe fruits, which leads to the rejection or down-grading (Tooley et al., 1999).

97 328 Carabidae as natural enemies of the raspberry beetle (Byturus tomentosus F.)

The aim of the present study was to explore with fipes carabids were presented with either 10 raspberry laboratory feeding experiments the potential of these beetle larvae or 10 Thlapsi arvense seeds. carabid species for control of the raspberry beetle. Two In the choice feeding tests, P. melanarius, P. ni- types of feeding experiments were carried out: no-choice ger and C. nemoralis carabids were presented with 10 and choice tests. In no-choice tests the numbers of dif- raspberry beetle larvae together with 10 aphids while ferent prey items consumed by the carabids over certain H.rufipes carabids were presented with 10 raspberry time periods were measured. The choice feeding tests, beetle larvae together with 10 seeds. offering a mixture of food items, were carried out to es- A total of 135 carabids of each species were tested tablish carabid preferences for the different food items. in each type of feeding test. All tests were made in 9 rep- licates. Each carabid was tested only once; it was placed Materials and methods together with the prey items on moist filter paper in a Petri dish at room temperature (20ºC). Tests were conducted in The feeding experiment was carried out in the dark as carabids are night active and terminated after 2006. For feeding experiments, the carabid beetles (Pte- different periods of time: 1, 2, 3, 6 and 12 hours. After the rostichus melanarius, P. niger, Carabus nemoralis and specified time, dishes were taken into the light and the Harpalus rufipes) were caught with dry pitfall traps (cups number of prey items consumed was recorded. 9 cm in diameter and 12 cm deep) in a raspberry plan- The mean number of items consumed per de- tation at Polli Horticultural Research Centre, in South fined time unit and its standard error were calculated and Estonia (latitude 58°7′ N and 25°33′ E). The traps were the significance of data differences determined using the checked every 24 h; as the beetles are nocturnal this was Tukey-Kramer’s test. done early each morning to avoid the beetles being in the traps for too long. The captured beetles were kept in a laboratory for 24 hours without food before the ex- Results periments to standardize their hunger state. They were No-choice feeding tests. P. melanarius, P. niger then placed individually in small containers with water and C. nemoralis consumed most of the beetle larvae supplied on soaked cotton wool in the shade at room during the first hour of the experiment, whereas most of temperature (20ºC). The prey items, i.e. raspberry beet- the aphids were eaten two to three hours after the ex- le fourth instar larvae (with an average biomass of 4.46 periment started. H. rufipes at the same time interval had ± 0.171 mg), the large raspberry aphid Amphorophora eaten less food. idaei (Börner) (0.63 ± 0.029 mg) and dry seeds of Thlap- P. melanarius had consumed significantly more si arvense L. (1.1 ± 0.017 mg), were collected at the same beetle larvae than aphids after both the first and second locality as the beetles directly before each experiment. hours (Tukey-Kramer’s test, p < 0.001 and p = 0.01). Ac- Average raspberry beetle larvae biomass was determined cording to the biomass of the food, beetle larvae were by weighing 3 batches of 160 larvae, average aphids consumed significantly more (p < 0.001) than aphids at mass was determined by weighing 3 batches of 80 aphids every control point. and average seed mass was determined by weighing 4 P. niger, C. nemoralis and H. rufipes had con- batches of 400 seeds. sumed similar numbers of the two food items. According In the no-choice feeding tests, P. niger, P. mela- to the biomass of the food, beetle larvae were consumed narius, C. nemoralis carabids were presented with either significantly more than aphids at every control point 10 raspberry beetle larvae or 10 aphids while the H. ru- (Table 1). Table 1. Mean number and biomass (± standard error) of raspberry beetle larvae, aphids or seeds consumed by the carabids Pterostichus melanarius, P. niger, Carabus nemoralis and Harpalus rufipes when presented in no-choice tests for different lengths of time

Number of food items eaten Biomass (mg) of food items eaten Feeding Larvae of Larvae of Carabid species time Amphorophora Amphorophora Byturus p Byturus p h idaei idaei tomentosus tomentosus 1 2 3 4 5 6 8 9 10 11 Pterostichus melanarius n 10 10 44.6 6.0 1 9.2 ± 0.68 2.2 ± 1.4 0.0006 *** 40.9 ± 7.14 1.4 ± 1.25 <0.0001 *** 2 9.7 ± 0.72 4.7 ± 1.02 0.01 ** 43.1 ± 3.64 2.8 ± 0.92 <0.0001 *** 3 10.0 ± 1.13 7.7 ± 1.6 0.6427 ns 44.6 ± 0.00 4.6 ± 1.39 0.0004 *** 6 10.0 ± 1.04 9.3 ± 1.48 0.982 ns 44.6 ± 0.00 5.6 ± 0.35 <0.0001 *** 12 10.0 ± 1.01 10.0 ± 1.42 1.000 ns 44.6 ± 0.00 6.0 ± 0.00 <0.0001 *** P. niger n 10 10 44.6 6.0 1 8.8 ± 0.76 6.0 ± 0.88 0.1526 ns 39.0 ± 8.44 3.6 ± 1.04 0.0031 **

98 ISSN 1392-3196 ŽEMDIRBYSTĖ=AGRICULTURE Vol. 99, No. 3 (2012) 329

Table 1 continued 1 2 3 4 5 6 8 9 10 11 2 9.0 ± 1.22 7.7 ± 1.41 0.8896 ns 40.1 ± 8.92 4.6 ± 0.92 0.0038 ** 3 9.0 ± 0.89 8.3 ± 1.03 0.9596 ns 40.1 ± 8.92 5.0 ± 1.25 0.0037 ** 6 9.0 ± 0.59 10.0 ± 0.68 0.6963 ns 40.1 ± 8.92 6.0 ± 0.00 0.0046 ** 12 10.0 ± 1.01 10.0 ± 1.42 1.000 ns 44.6 ± 0.00 6.0 ± 0.00 <0.0001 *** Carabus nemoralis n 10 10 44.6 6.0 1 8.7 ± 1.27 5.0 ± 1.27 0.2349 ns 38.6 ± 2.57 3.0 ± 1.2 0.0003 *** 2 9.0 ± 1.64 9.7 ± 1.64 0.9912 ns 40.1 ± 4.46 5.8 ± 0.35 0.0053 ** 3 9.7 ± 0.64 10.0 ± 0.64 0.9822 ns 43.1 ± 2.57 6.0 ± 0.00 0.0016 ** 6 10.0 ± 0.72 10.0 ± 0.72 1.000 ns 44.6 ± 0.00 6.0 ± 0.00 <0.0001 *** Larvae of Larvae of Seeds of Seeds of Byturus Byturus Thlapsi arvense Thlapsi arvense tomentosus tomentosus Harpalus rufipes n 10 10 44.6 11.0 1 3.7 ± 0.91 0.3 ± 1.39 0.2284 ns 16.6±14.94 0.4 ± 0.64 0.029 * 2 4.7 ± 1.17 3.7 ± 1.79 0.9600 ns 21.0±15.38 4.0 ± 4.17 0.029 * 3 6.0 ± 1.24 4.7 ± 1.9 0.9341 ns 26.7±17.64 5.1 ± 4.17 0.018 * 6 7.0 ± 1.08 8.0 ± 1.64 0.9554 ns 31.2±16.84 8.8 ± 2.21 0.012 * 12 8.1 ± 0.91 10.0 ± 1.39 0.6859 ns 36.3±12.99 11.0 ± 0.00 0.021 * *, **, *** – significance level, ns – not significant, Tukey-Kramer’s test

Choice feeding tests. In the choice feeding tests, choice tests, there was no significant preference between the quantity of consumed food items was less than in the consumed food items. According to the biomass of the no-choice feeding tests. prey, a significant preference for beetle larvae occurred For P. melanarius and P. niger a significant pre- after three hours. ference for beetle larvae was seen in the choice feeding H. rufipes showed a clear significant preference tests after the 1st hour (p = 0.0248 and p = 0.0427). Later for beetle larvae in choice tests after three hours. Ac- such significant preferences for the larvae were lost. Ac- cording to the biomass of the larvae and seeds, the larvae cording to the biomass of the prey, larvae were preferred were consumed significantly more. to the aphids at every control point. Thus choice feeding tests gave clear evidence C. nemoralis was at first confused in choice that P. melanarius, P. niger, C. nemoralis and H. rufipes tests and consumed less food than in no-choice tests. In prefer to consume raspberry beetle larvae over aphids.

Table 2. Mean number and biomass (± standard error) of raspberry beetle larvae or aphids/seeds consumed by the carabids Pterostichus melanarius, P. niger, Carabus nemoralis and Harpalus rufipes in choice feeding tests after different time periods when offered a mixture of food items

Number of food items eaten Biomass (mg) of food items eaten Feeding Larvae of Larvae of Carabid species time Amphorophora Amphorophora Byturus p Byturus p h idaei idaei tomentosus tomentosus 1 2 3 4 5 6 7 8 9 10 Pterostichus melanarius n 10 10 44.6 6.0 1 3.0 ± 1.01 0.33 ± 0.96 0.0248 * 13.4 ± 4.46 0.2 ± 0.35 0.0355 * 2 4.7 ± 2.52 0.66 ± 1.02 0.055 ns 20.8 ± 11.22 0.4 ± 0.35 0.0346 * 3 6.3 ± 0.58 4.67 ± 1.6 0.6044 ns 28.2 ± 2.57 2.8 ± 2.84 0.0003 *** 6 9.7 ± 0.58 8.3 ± 1.48 0.2667 ns 43.1 ± 2.57 5.0 ± 0.92 0.0005 *** 12 10.0 ± 0.00 10.0 ± 1.42 0.9987 ns 44.6 ± 0.00 6.0 ± 0.00 <0.0001 *** P. niger n 10 10 44.6 6.0 1 7.0 ± 0.88 3.0 ± 0.88 0.0427 * 31.2 ± 4.46 1.8 ± 0.6 0.0068 ** 2 9.3 ± 1.41 6.7 ± 1.41 0.5665 ns 41.6 ± 5.14 4.0 ± 2.50 0.0017 ** 3 10.0 ± 1.03 8.0 ± 1.03 0.5447 ns 44.6 ± 0.00 4.8 ± 1.2 0.0003 *** 6 10.0 ± 0.68 9.7 ± 0.68 0.9851 ns 44.6 ± 0.00 5.8 ± 0.35 <0.0001 *** 12 10.0 ± 0.00 10.0 ± 0.00 1.000 ns 44.6 ± 0.00 6.0 ± 0.00 <0.0001 *** Carabus nemoralis n 10 10 44.6 6.0 1 1.3 ± 1.1 3.8 ± 1.1 0.4154 ns 5.6 ± 6.68 2.3 ± 1.98 0.4016 ns 2 4.5 ± 1.42 5.8 ± 1.42 0.9222 ns 22.6 ± 16.17 3.5 ± 2.42 0.0978 ns

99 330 Carabidae as natural enemies of the raspberry beetle (Byturus tomentosus F.)

Table 2 continued 1 2 3 4 5 6 7 8 9 10 3 7.3 ± 0.56 8.5 ± 0.56 0.4277 ns 32.3 ± 4.27 5.1 ± 1.04 0.0006 *** 6 8.3 ± 0.62 8.8 ± 0.62 0.9394 ns 36.8 ± 5.61 5.3 ± 1.14 0.0011 ** 12 9.3 ± 0.41 10.0 ± 0.41 0.5883 ns 41.2 ± 6.69 6.0 ± 0.00 0.0018 ** Larvae of Seeds of Larvae of Seeds of Byturus Thlapsi p Byturus Thlapsi p tomentosus arvense tomentosus arvense Harpalus rufipes n 10 10 44.6 11.0 1 5.3 ± 1.39 0.3 ± 1.39 0.1024 ns 23.8 ± 2.57 0.4 ± 0.64 0.0026 ** 2 7.3 ± 1.79 0.7 ± 1.79 0.0886 ns 32.7 ± 11.21 0.7 ± 1.28 0.037 * 3 8.7 ± 1.9 0.7 ± 1.9 0.0493 * 38.6 ± 6.81 0.7 ± 1.28 0.0088 ** 6 9.7 ± 1.64 1.3 ± 1.64 0.0171 * 43.1 ± 2.57 1.5 ± 1.28 0.00016 *** 12 10.0 ± 1.39 3.7 ± 1.39 0.0322 * 44.6 ± 0.00 4.4 ± 2.92 0.0018 ** *, **, *** – significance level, ns – not significant, Tukey-Kramer’s test Discussion Carabid species vary in their foraging prefe- In our feeding tests, C. nemoralis ate raspberry rences. Lindroth (1992) considered that the genus Pte- beetle larvae and aphids at an equivalent level and did not rostichus consumes chiefly animal food. It has been show a significant preference. reported that P. niger, P. melanarius, C. nemoralis, and The impact on raspberry beetle larvae is not even H. rufipes might be efficient predators of larval necessarily associated with a high preference for larvae. stage of Leptinotarsa decemlineata (Thiele, 1977; So- Fawki et al. (2005) reported that for P. melanarius and rokin, 1981). The activity of Pterostichus spp. beetles co- C. nemoralis insects are high-quality, earthworms are in- incided with the time interval in which fifth-instar Cydia termediate, and slugs and seeds are low quality food for pomonella larvae wander on the ground prior to pupation these species, whereas for C. nemoralis, earthworms are (Riddick, Mills, 1996), indicating their role in control of the preferred prey. But, it is important to note that pure Cydia pomonella. Pterostichus spp. also has consumed diets of all prey types are nutritionally incomplete and most predators can improve their fitness and fecundity winter moth (Oteropthera brumata L.) pupae (Horgan, by choosing a mixed diet (Toft, 1996; Saska, 2008). Dif- Myers, 2004). In our feeding experiments, P. melanarius ferent authors have studied carabid diet and aphid control and P. niger liked to eat raspberry beetle larvae. This ex- potential in the laboratory and field (Ekbom et al., 1992; plains their higher abundance in raspberry plantations Kielty et al., 1999). Even if aphids are important food during berry ripening time when raspberry beetle larvae for several polyphagous predators, a diet of aphids alone are available to them as prey items. provides a low-quality food for a wide range of generalist Species of the genus Harpalus are mostly gene- insectivores (Bilde, Toft, 1994; Jorgensen, Toft, 1997). ralists, accepting a wide range of species of seed (Honek Further, animal food in the diet of carabids could et al., 2007), preferring Viola and Cirsium seeds (Thiele, be dependent on season. For example, the intestines of 1977; Jorgensen, Toft, 1997; Honek et al., 2007), as well P. cupreus contained 67% plant material in spring but as insect prey. There are reports of H. rufipes as a pre- at the end of summer insect material dominated (80%) dator of cabbage root fly eggs and larvae (Coaker, Wil- (Thiele, 1977). That is apparently influenced by the liams, 1963) and Pieris rapae larvae (Dempster, 1967). greater availability of insects as a food source in summer. Büchs (2003) and Warner et al. (2000) reported H. ru- In raspberry plantations, aphids are available for a longer fipes as a biocontrol agent for the larvae of the brassica time in the vegetation period. The aggregation of H. ru- pod midge in oilseed rape. Holopainen and Helenius fipes, P. melanarius, P. niger and C. nemoralis during (1992) concluded that this carabid contributed to the berry ripening time when raspberry beetle larvae drop to suppression of Rhopalosiphum padi L. populations in the soil for pupation (Arus et al., 2011) suggests that they spring barley. Monzo et al. (2011) found that H. rufipes are concentrating at the available food source. Our feed- play an important role in regulating medfly populations ing experiments confirmed this. In choice feeding tests, in citrus orchards. In our choice feeding tests, H. rufipes H. rufipes, P. melanarius and P. niger significantly pre- significantly preferred raspberry beetle larvae to Thlapsi ferred raspberry beetle larvae to aphids. C. nemoralis had arvense seeds. This indicates that, if raspberry beetle lar- a tendency to consume more raspberry beetle larvae than aphids in no-choice tests. vae are available, as they are at raspberry ripening time in plantations, they could be preferably eaten by H. rufipes beetles. Probably some volatile signal compounds from Conclusion raspberry beetle larvae which drop to the soil during These carabid beetles (Pterostichus melanarius, raspberry ripening time attract migration of H. rufipes, P. niger, Carabus nemoralis and Harpalus rufipes) as a P. melanarius and P. niger to the raspberry plantation in- group of generalist predators, have, through their feed- dicating a good food source. ing preferences, the potential to make a significant con-

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Can polyphagous les // Physiological Entomology. – 2008, vol. 33, iss. 3, predators control the bird cherry-oat aphid, Rhopalosiphum p. 188–192 padi: in spring cereals // Entomologia Experimentalis et Sorokin N. S. Ground beetles (Col.: Carabidae) – natural ene- Applicata. – 1992, vol. 65, p. 215–223 mies of the Colorado potato beetle, Leptinotarsa decem- Fawki S., Smerup S., Toft S. Food preferences and food value lineata Say // Entomologicheskoje Obozreniye. – 1981, for the carabid beetles Pterostichus melanarius, P. ver- vol. 60, iss. 2, p. 282–289 sicolor and Carabus nemoralis // DIAS Report. – 2005, Symondson W. O. C., Sunderland K. D., Greenstone M. Can vol. 114, p. 99–109 generalist predators be effective biocontrol agents? // An- Gordon S. C., Woodford J. A. T., Birch A. N. E. Arthropod pests nual Review of Entomology. – 2002, vol. 47, p. 561–594 of Rubus in Europe: pests status, current and future control Thiele H. U. Carabid beetles in their environments. – Berlin, strategies: review article // Journal of Horticultural Sci- ence. – 1997, vol. 72, iss. 6, p. 831–862 Germany, 1977, 369 p. Hanni L., Luik A. Fruit damages caused by Byturus tomentosus Toft S. Indicators of prey quality for arthropod predators // Acta and Botryotinia fuckeliana depending on different rasp- Jutlandica. – 1996, vol. 71, iss. 2, p. 107–116 berry varieties // Transactions of the Estonian Agricultural Toft S., Bilde T. Carabid diets and food value // The agroeco- University. – 2001, vol. 213, p. 35–38 logy of ground beetles / Holland J. M. (ed.). – Andover, Hanni L., Luik A. Occurrence of spiders and carabids in rasp- UK, 2002, p. 81–110 berry plantation depending on different mulching / Pro- Tooley J. A., Froud-Williams R. J., Boatman N. D., Holland J. M. ceedings of the scientific international conference Plant Laboratory studies of weed seed predation by carabid beet- Protection in the Baltic Region in the Context of Integra- les / Proceedings of the 1999 Brighton Conference: Weeds. tion to EU. – Kaunas, Lithuania, 2002, p. 34–37 – Brighton, UK, 1999, p. 571–572 Holopainen J. K., Helenius J. Gut contents of ground beetles Tuovinen T. Hedelmä- ja marjakasvien tuhoeläimet. Kasvin- (Col., Carabidae) and activity of these and other epigeal suojeluseuran julkaisu No. 89. – Vaasa, Finland, 1997, predators during an outbreak of Rhapalosiphum padi 187 p. (in Finnish) (Hom., Aphidae) // Acta Agriculturae Scandinavica, Sec- Warner D. J., Allen-Williams L. J., Ferguson A. W., Williams tion B: Soil and Plant Science. – 1992, vol. 42, p. 57–61 I. H. Pest-predator spatial relationships in winter rape: im- Honek A., Martinkova Z., Saska P., Pekar S. 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101 332 Carabidae as natural enemies of the raspberry beetle (Byturus tomentosus F.)

ISSN 1392-3196 Žemdirbystė=Agriculture, vol. 99, No. 3 (2012), p. 327–332 UDK 634.711:634.75

Žygiai (Carabidae) – natūralūs paprastojo avietinuko (Byturus tomentosus F.) priešai

L. Arus1, A. Kikas1, A. Luik2 1Estijos gyvybės mokslų universiteto Žemės ūkio ir aplinkos mokslų instituto Polli sodininkystės ir daržininkystės tyrimų centras 2Estijos gyvybės mokslų universiteto Žemės ūkio ir aplinkos mokslų institutas

Santrauka Paprastasis avietinukas (Byturus tomentosus F.) yra Europoje plačiai paplitęs aviečių kenkėjas. Nors jo paplitimas kontroliuojamas cheminėmis priemonėmis, reikėtų kurti alternatyvias strategijas, paremtas biologine kontrole – polifaginiais plėšrūnais. Laboratorinių tyrimų metu siekta ištirti paprastojo avietinuko lervų reikšmę žygių rūšių Pterostichus melanarius, P. niger, Carabus nemoralis ir Harpalus rufipes mitybai. Tyrimų metu su ir be pasirinkimo pateikus amarus arba paprastojo avietinuko lervas, žygių P. melanarius bei P. niger rūšys teikė pirmenybę paprastojo avietinuko lervoms. C. nemoralis greitai suvartojo abi maisto rūšis. H. rufipes teikė pirmenybę paprastojo avietinuko lervoms, o ne Thlapsi arvense sėkloms. Pagal kiekvienos maisto rūšies suvartotą biomasę visos tirtos žygių rūšys teikė pirmenybę paprastojo avietinuko lervoms. Straipsnyje pateikti duomenys rodo, kad didieji žygiai − P. melanarius, P. niger, C. nemoralis ir H. rufipes – galėtų būti reikšmingi reguliuojant aviečių kenkėjų populiacijas.

Reikšminiai žodžiai: biologinė kontrolė, Carabidae, amaras, Byturus tomentosus lervos, pirmenybės teikimas maistui.

102 V Hanni, L. and Luik, A. 2006. PARASITISM OF RASPBERRY BEETLE (Byturus tomentosus F.) LARVAE IN DIFFERENT CROPPING TECHNIQUES OF RED RASPBERRY. Agronomy Research 4 (special issue): 187–190. Agronomy Research 4(Special issue), 187–190, 2006

Parasitism of raspberry beetle (Byturus tomentosus F.) larvae in different cropping techniques of red raspberry

L. Hanni1 and A. Luik2

1Polli Horticultural Research Centre, Institute of Agricultural and Environmental Sciences, Estonian University of Life Sciences, Viljandi county, Karksi–Nuia, Polli, 69104, Estonia; e-mail: [email protected] 2Institute of Agricultural and Environmental Sciences, Estonian University of Life Sciences, Kreutzwaldi St. 64, 51014, Tartu, Estonia

Abstract. Raspberry beetle (Byturus tomentosus F.) is the major pest in raspberry in Estonia and throughout Europe. The parasitism rate of raspberry beetle larvae was studied in different cropping systems and in wild raspberry. In the raspberry plantation two intercropping systems were used: intercropping with 7 herbs and with black currant. The control variant was monocropping. Larvae from wild raspberries were collected from a clear cut area in the neighbourhood of the plantation. In the monocropping area the larval parasitism rate was less than 5%. The intercropping of raspberries with herbs increased the larval parasitism rate (9.4%), while in the intercropping with black currant, it decreased (2.2%). Larvae from wild raspberry were the most parasitized (26.1%). Further investigation is needed to explain species composition of parasitoids in raspberry beetle larvae.

Key words: Byturus tomentosus, parasitoids, intercropping

INTRODUCTION

Raspberry beetle (Byturus tomentosus F.) is widely spread and major pest of cultivated raspberry throughout Europe (Gordon et al., 1997). Without special treatments, the yield loss may extend to 50% (Tuovinen, 1997). The beetles over- winter in the soil at the base of host plants and emerge in spring, usually before flower buds of raspberry have opened. On emerging from the soil young adult beetles frequently remain on the young foliage. They may feed extensively on the leaves of the growing tips resulting in extensive inter-veinal damage to the leaves. Later on, during flowering, the adults eat large holes in flower buds and pollen. Each adult female raspberry beetle can lay up to 120 eggs, usually as a single egg per flower. The most crucial damage is caused by larvae, which first gnaw the base of the receptacle and then dig galleries on the developing fruit. The result is discoloured or contaminated ripe fruit leading to rejection or down-grading of the crop. Due to their hidden lifestyle, the raspberry beetle larvae are safe from predatory and parasitoid arthropods. In some stadia, the larvae are directly threatened by natural enemies. Little is known about the parasitoids of raspberry pests. The research in Italy has focused on the natural enemies of strawberry blossom weevil (Anthonomus rubi Herbst.) in raspberry and bramble where the most efficient parasitoid was the

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105 Braconid, Triapsis aciculatus Ratz., causing up to 68.8% parasitism. Another Braconid, Bracon immutator Nees, was less effective and the Pteromalid, Spilomalus Quadrinota Walk. also emerged from infested strawberry blossom weevil larvae (Scanabissi & Arzone, 1992). Several species of Hymenopteran parasitoid have been isolated from galled canes (caused by Lasioptera rubi Heeger) in Italy but the role of these parasitic wasps in controlling L. rubi is unknown (Viggiani & Mazzone, 1978). Some Apophua species of ichneumonids attack strawberry leaf-rollers (Ancylis comtana Froelich) while they are hidden inside their leaves (below) (Henderson & Raworth, 1991). One of the factors which aggravates sustainability problems in agriculture is the use of monocultures, where every plant in a crop is genetically identical. Monocultures lead to vulnerability to stress, whether caused by pathogens, pests, or the weather, and hence to unstable yields. Intercropping with different cultures will provide a chance to reduce accumulation of pests and diseases, dispersing and disguising an odour of each other. On the other hand the intercropping with its diversity is attractive to beneficial organisms (Altieri & Nicholls, 2003). Intercropping has given good results in limiting a number of cabbage (Wiech, 1991) and carrot pests (Uvah & Coacer, 1984; Rämert, 1993). The aim of this work was to determine whether raspberry beetle larvae have parasitoids and whether raspberry growing in different intercropping systems might affect the extent of parasitism compared to wild raspberry.

MATERIALS AND METHODS

The raspberry plantation with different intercropping systems was established in spring 2002 in L. Hanni’s organic berry production farm in Viljandi County. The test variants were: I – control, raspberry monoculture, 15 x 15 m. II – raspberry rows alternately with rows of flowering plants, 15 x 10 m. (7 different herbs) III – raspberry rows alternately with rows of black currant, 15 x 15 m. IV – wild raspberry, from clear cut area in the neighbourhood of the plantation. Two raspberry varieties were used in every variant (‘Tomo’ and ‘Novokitaivska’) with three replications. The test variants were separated with a vegetable field (width 25 m). The flowering plants were Calendula (Calendula officinalis), Fennel (Foeniculum vulgare L.), Dill (Anethum graveolens L.), Borage (Borago officinalis), Chamomile (Matricaria chamomilla), Tansy (Tanaceum sect. Tanaceum) and Yarrow (Achillea millefolium). Dill and Fennel are potentially suitable floral hosts for two eulophid parasitoids, Edovum puttleri Grissel and Pediobius foveolatus Crawford (Patt et al., 1997). The plantation is surrounded with a 10 m width of thick grass, which was regularly cut down. Nearby the plantation there is a forest with clear cut area, natural grassland and a little body of water. Thick grass, consisting mostly of Gramineae and clover, and including some weeds like quackgrass (Elymus repens L.) and dandelion (Taraxacum officinale) was growing between rows.No chemical treatments or mineral fertilisation were used on the plantation. Weeds were mechanically controlled two times in the vegetation period. In spring, decayed manure was spread on the raspberry rows, about 5 kg per rowmeter, and cut grass was used as a mulch.

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106 To determine whether raspberry beetle larvae have parasitoids, and if raspberry growing in different intercropping systems and in the wild might affect the extent of pest parasitism, the raspberry beetle larvae were collected in 2005 during the ripening period of raspberry (July 11 – Aug. 17) in four different variants with three replications. The larvae were deep-frozen in distilled water. After thawing, the larvae were coloured and were dissected under a microscope at about 25 x magnification. The larvae of parasitoids appeared after the adipose tissue and haemolymph of pest larvae were coloured. The parasitism rate of raspberry beetle larvae was calculated and the results were elaborated; statistical analysis of variance and differences were compared using LSD test at P = 0.05.

RESULTS AND DISCUSSION

The total number of collected raspberry beetle larvae was 978: 243 larvae from raspberry monocropping variant, 440 larvae from intercropping variant with flowering plants, 180 larvae from intercropping variant with black currant and 115 larvae from wild raspberry. Inside one parasitized raspberry beetle larvae 1–6 parasitoid larvae were found. Larvae from wild raspberry were the most parasitized (26.1%) (Fig. 1). In the intercropping conditions the most parasitized were larvae from the variant with flowering plants (9.4%). The intercropping of raspberries with herbs increased the larval parasitism rate; it decreased (2.2%) in the intercropping with black currant. In the monocropping (control) conditions the parasitism rate was 4.4%. Raspberry growing in intercropping systems with herbs promoted the parasitism rate of the pest, and consequently also the presence of parasitoids. Wild flower strips have been sown as special field margins to promote beneficial insects, including pollinators, predators and parasitoids as well as soil organisms, all of which help by providing “ecological services” to crop plants. Intercropping with flowering herbaceous plants increases parasitoid survival, fecundity and retention and pest suppression in agro-ecosystems (Patt et al., 1997).

35 26.1 30 25 20 15 9.4 10 4.4 % of parazited larvae parazited % of 5 2.2 0 Monocropping Int.cropping with Int.cropping with Wild Rubus herbs b.currant

Fig 1. Parasitism rate of raspberry beetle larvae (%) in wild raspberry and its effect in different growing technologies (LSD05 = 4.5). 189

107 CONCLUSIONS

The results of present studies confirmed that raspberry beetle larvae have parasitoids. The parasitism rate was highest in wild raspberries, and higher in raspberries grown intercropping with flowering herbaceous plants than in monoculture or intercropping with black currants. Control of raspberry beetle especially in organic fields will benefit from the maintenance of useful entomofauna. Further investigation is needed to explain species composition of parasitoids in raspberry beetle larvae.

ACKNOWLEDGEMENTS. This research was supported by Estonian Science Foundation grant no. 5736.

REFERENCES

Altieri, M.A. & Nicholls, C.I. 2003. Biodiversity and Pest Management in Agroecosystems. Second edition. The Haworth Press, Inc. 236 p. Gordon, S.C., Woodford, J.A.T. & Birch, A.N.E. 1997. Arthropod pests of Rubus in Europe: Pests status, current and future control strategies. Review article. J. of Hort. Sc. 72(6) 831–862. Henderson, D.E. & Raworth, D.A. 1991. Beneficial insects and common pests on strawberry and raspberry crops, Canada, 34 pp. Patt, J.M., Hamilton, G.C. & Lashomb, J.H. 1997. Foraging success of parasitoid wasps on flowers: interplay of insect morphology, floral architecture and searching behaviour. Entom. Experim. Et Appl. 83(1), 21. Rämert, B. 1993. Mulching with grass and bark and intercropping with Mediago litoralis against (Psila rosae F. Biol. Agric. and Hortic. 9, 125–135. Scanabissi, G. & Arzone, A. 1992. Indagini epidemiologiche su Anthonomus rubi Herbst (Coleoptera, Curculionidae). Redia 75, 537–548 (in Italian). Tuovinen, T. 1997. Hedelmä- ja marjakasvien tuhoeläimet. Kasvinsuojeluseuran julkaisu n:o 89. Vaasa. 187 p. (in Finnish). Uvah, I. I. & Coacer, T. H. 1984. Effect of mixed cropping on some insect pests of carrots and onions. J. Entomol. Exp. Appl. 36, 159–167. Viggiani, G. & Mazzone, P. 1978. Infestazioni di Lasioptera rubi (Schrank) (Diptera, Cecidomyiidae) in lamponeti dell’Italia meridionale. Informatore Fitopatologico, 28, 3–4 (in Ilalian). Wiech, K. 1991. Effect of intercropping cabbage and white cover on some pests and beneficial insects. Materials of the 31st Research session of Institute for Plant Protection Panstwowe Wydawnictwo Rolniczne I Lesne, pp. 199–207.

190

108 CURRICULUM VITAE

First name: Liina Surname: Arus (Hanni until the year 2006) Date of birth: 14. 07. 1975 Children: Margus (21.10.1997) Kristjan (26.01.2004) Marten (30.12.2009)

Employment: Estonian University of Life Sciences, Kreutzwaldi 1, Tartu 51014, Institute of Agricultural and Environmental Sciences, Polli Horti- cultural Research Centre

Position: Researcher

Education: 2001-2013 Estonian University of Life Sciences, Institute of Agricultural and Environmental Sciences, PhD Study 1997-2001 Estonian Agricultural University (EAU), MSc Study 1993-1997 EAU, bachelor studies in horticulture 1990-1993 C.R. Jakobson Gymnasium

Scientifi c degree: MSc, entomology: “On damage resistance of the raspberry varieties in Southern Estonia”. Institution and year EAU, 2001 of issuing degree:

Career: 1999-2005 EAU, Polli Horticultural Institute, researcher 2005-2010 Estonian University of Life Sciences, Institute of Agricultural and Environmental Sciences, Polli Horticultural Research Centre, researcher

2011-… Estonian University of Life Sciences, Institute of Agricultural and Environmental Sciences, Polli Horticultural Research Centre, researcher

109 Administrative Estonian Academic Agricultural Society, activities: member Estonian Plant Protection Organization, member

Research interests: Raspberry cultivar investigation, breeding, agrotehnics, plant protection, entomo- phagous studies. Edible honeysuckle cultivar investigation

Participations in research projects: 2012-2013 Innove project no. 8-2/T12055PKPA: “Qualifi cation that meets the needs of local employers to the elderly people in the region of South-Viljandi – skilled mulk (traditional name of the inhabitant of South-Viljandimaa) is the king of the garden”, principal investigator. 2009-2014 Target fi nanced project No. SF0170057s09: “Plant protection for sustainable crop production”, PhD student 2009-2019 Ministry of the Agriculture of Estonia Project No. 8-2/T9014PKPA: “The small fruit breeding - breeding of black currant and raspberry cultivars”, principal investigator. 2007-2013 Ministry of the Agriculture of Estonia project No. 8-2/T9013PKPK: “Collection and maintenance of genetic resources of agricultural plants”, principal investigator. 2006-2011 Target fi nanced project No. SF1092711s06: “Improvement of assortment of fruit crops, maintenance of genetic diversity and development of environment-friendly culti- vating methods II”, principal investigator. 2004-2008 Target fi nanced project No. SF0172655s04: “Development of environmentally friendly plant protection II”, PhD student

110 2004-2007 Estonian Science Foundation No. 5736: “Occurrence of carabids and hyme-nopterous parasitoids in different crops depending on growing technologies and fi eld locations”, principal investigator. 2002-2006 Ministry of the Agriculture of Estonia project No. L003PAPA04: “Collection and maintenance of genetic resources of agri-cultural plants”, principal investigator. 2000-2007 Ministry of the Agriculture of Estonia Project No. 3.4-23/281: “Small fruit breeding and the research on the agro-technology of raspberry and black currant”, principal investigator. 2000-2003 Estonian Science Foundation No. 4109: „Taxonomical composition and abundance of the predator arthropods depending on crop, agrotechnology and fi eld location“, principal investigator. Professional training: 26.07-03.08. 2003 PhD course “Agricultural transformation in Germany and Europe”, 3 ECTS, Germany, Witzenhausen. 10.02-03.03. 2005 The course „Package of STATISTICA“, 0.5 ECTS, Estonia, Tartu. 08.01-30.04. 2007 The course „Using English in teaching at university level“, 4.5 ECTS, Estonia, Tartu. 13.08-16.08. 2012 The course „Package of STATISTICA for agricultural sciences“, 1.25 ECTS, Estonia, Tartu. 20.09-25.11. 2012 The course „Academic writing“, 3 ECTS, Estonia, Tartu.

111 ELULOOKIRJELDUS

Eesnimi: Liina Perekonnanimi: Arus (Hanni, kuni aastani 2006) Sünniaeg: 14. 07. 1975 Lapsed: Margus (21.10. 1997) Kristjan (26.01. 2004) Marten (30.12. 2009)

Töökoht: Eesti Maaülikool, Kreutzwaldi 1, Tartu 51014, Põllumajandus- ja keskkonnainstituut, Polli aiandusuuringute keskus

Ametikoht: Teadur

Haridustee: 2001-2013 Eesti Maaülikool (EMÜ), Põllumajandus- ja keskkonnainstituut, doktoriõpe 1997-2001 Eesti Põllumajandusülikool (EPMÜ), Agronoomiateaduskond, magistriõpe 1993-1997 EPMÜ, Agronoomiateaduskond, aianduse eriala, bakalaureuseõpe 1990-1993 C.R. Jakobsoni Gümnaasium

Teaduskraad: MSc entomoloogia erialal: „Aedvaarika-sortide kahjustuskindlusest Lõuna-Eesti tingimustes“.

Teaduskraadi välja EPMÜ, 2001 andnud asutus, aasta:

Teenistuskäik: 1999-2005 EPMÜ, Polli Aianduse Instituut, teadur 2005-2010 EMÜ, Põllumajandus- ja keskkonnainstituut (PKI), Polli aiandusuuringute keskus, teadur 2011-… EMÜ, PKI, Polli aiandusuuringute keskus, teadur

Teadusorganisat- siooniline tegevus: Akadeemilise põllumajanduse Seltsi ja Taimekaitse Seltsi liige

112 Teadustöö Aedvaarika sordiuurimine, aretamine, agro- põhisuunad: tehnika, taimekaitse, entomofauna. Kuslapuu sordiuurimine

Osalemine uurimisprojektides: 2012-2013 Elukestva Õppe Arendamise Sihtasutus Innove; Meede “Kvalifi tseeritud tööjõu pakkumise suurendamine”, Projekt nr. 8-2/ T12055PKPA: “Lõuna-Viljandimaa vanemaealistele piirkonna tööandjate vaja- dustele vastav kvalifi katsioon – osav mulk on aia kuningas”, põhitäitja. 2009-2014 Sihtfi nantseeritav teema nr. SF0170057s09: “Taimekaitse jätkusuutlikule taime- kasvatusele”, täitja 2009-2019 EV Põllumajandusministeeriumi grant nr. 8-2/ T9014PKPA: “Marjakultuuride sordi-aretus – musta sõstra ja vaarika aretus”, põhitäitja 2007-2013 Riiklik program nr. 8-2/T9013PKPK: “Põllumajanduskultuuride geneetiliste ressursside kogumine ja säilitamine”, põhitäitja 2006-2011 Sihtfi nantseeritav teema nr. SF1092711s06: “Aiakultuuride sortimendi parandamine, geneetilise mitmekesisuse säilitamine ja keskkonnasäästliku viljelustehnoloogia aren- damine II”, põhitäitja. 2004-2008 Sihtfi nantseeritav teema nr. SF0172655s04: “Keskkonnasäästliku taimekaitsetehnoloogia arendamine II”, täitja 2004-2007 Eesti Teadusfond grant nr. 5736: “Jooksiklaste ja kiletiivalistest parasitoidide esinemine erinevates kultuurides sõltuvalt kasvatustehnoloogiast ning põllu ääre-aladest”, põhitäitja. 2002-2006 Riiklik program nr. L003PAPA04: “Põllu- majanduskultuuride geneetiliste ressursside kogumine ja säilitamine aastateks 2002-2006”, alamprogramm “Puuvilja- ja marja-kultuuride ex situ säilitamine”, põhitäitja

113 2000-2007 EV Põllumajandusministeeriumi grant nr. 3.4- 23/281: “Marjakultuuride sordiaretus, vaarika ja musta sõstra agrotehnika uuring”, põhitäitja. 2000-2003 Eesti Teadusfond grant nr. 4109: „Rööv- lülijalgsete taksonoomiline koosseis ning ohtrus sõltuvalt kultuurist, agrotehnikast ning koosluse paigutusest“, põhitäitja.

Erialane enesetäiendamine: 26.07-03.08. 2003 Doktoriõppekursus “Põllumajanduse üm- berkorraldumine Saksamaal ja Euroopas”, 3 ECTS, Saksamaa, Witzenhausen. 10.02-03.03. 2005 Kursus „Statistikapakett STATISTICA kasutamine“, 0.5 ECTS, Estonia, Tartu. 08.01-30.04. 2007 Kursus „Inglise keele kasutamine õppetöö läbiviimisel“, 4.5 ECTS, Tartu. 13.08-16.08. 2012 Kursus „Põllumajandusstatistika“, 1.25 ECTS, Tartu. 20.09-25.11. 2012 Kursus „Akadeemiline kirjutamine“, 3 ECTS, Tartu.

114 LIST OF PUBLICATIONS

1.1. Articles indexed by the Thomson Reuters Web of Science

Arus, L., Kikas, A., Kaldmäe, H., Kahu, K. and Luik, A. 2013. Damage by raspberry beetle (Byturus tomentosus De Geer) in different raspberry cultivars. (Accepted by Biological Agriculture and Horticulture). Kaldmäe, H., Libek, A-V., Arus, L. and Kikas, A. 2013. Genotype and microclimate conditions infl uence ripening pattern and quality of blackcurrant (Ribes nigrum L.) fruit. Žemdirbystė/Agriculture 100(2): 167–174. Arus, L., Kikas, A. and Luik, A. 2012. Carabidae as natural enemies of the raspberry beetle (Byturus tomentosus F.). Žemdirbystė /Agriculture 99(3): 327–332. Arus, L., Luik, A., Monikainen, M. and Kikas, A. 2011. Does mulching infl uence potential predators of raspberry beetle? Acta Agriculturae Scandinavica, Section B - Plant Soil Science 61(3): 220–227.

1.2. Peer-reviewed articles in other International research journals with an ISSN code and International editorial board

Kaldmäe, H., Libek, A., Kikas, A. and Arus, L. 2010. Infl uence of Pollination Conditions on Fruit Set of Selected Blackcurrant Genotypes and Recently Released Cultivars. International Journal of Fruit Science 10(2): 187–194. Kask, K., Jänes, H., Libek, A., Arus, L., Kikas, A., Kaldmäe, H., Univer, N. and Univer, T. 2010. New cultivars and perspectives in professional fruit breeding in Estonia. Agronomy Research 8(3): 603–614. Kikas, A., Libek, A., Kaldmäe, H. and Hanni, L. 2007. Evaluation of strawberry cultivars in Estonia. Horticulture and Vegetable Growing 26: 131–137. Hanni, L. and Luik, A. 2006. Parasitism of raspberry beetle (Byturus tomentosus F.) larvae in different cropping techniques of red raspberry. Agronomy Research 4 (special issue): 187–190. Hanni, L. and Libek, A. 2003. Occurrence of some raspberry cane diseases depending on different mulching and varieties. Horticulture and Vegetable Growing 22(3): 382–388.

115 Libek, A. and Hanni, L. 2003. Winter hardiness of 23 raspberry cultivars at the Polli Horticultural Institute. Horticulture and Vegetable Growing 22(2): 57–64.

3.1. Articles in collections indexed by the Thomson Reuters ISI proceedings

Kikas, A., Kaldmäe, H., Arus, L. and Libek, A. 2012. Evaluation of blackcurrant cultivars for machine harvesting in Estonia. Acta Horticulturae 946: 143–147. Kikas, A., Libek, A., Kaldmäe, H. and Arus, L. 2009. Infl uence of spring frost and blossom weewil damage on strawberry yield formation. Acta Horticulturae 842: 347–350. Libek, A., Kikas, A., Kaldmäe, H. and Arus, L. 2008. Blackcurrant breeding in Estonia. Acta Horticulturae 777: 77–80. Kikas, A., Arus, L., Libek, A. and Kaldmäe, H. 2008. Evaluation of blackcurrant cultivars for machine harvesting in Estonia. Acta Horticulturae 777: 263–266. Arus, L., Kikas, A., Libek, A. and Kaldmäe, H. 2008. Testing fi ve raspberry cultivars of Estonian origin. Acta Horticulturae 777: 161–165. Hanni, L., Kask, K. and Kelt, K. 2005. Edible honeysucle: evaluation cultivars and selections at the Polli Horticultural Research Centre (Estonia). In: Proceedings of the International Scientifi c Conference „Environmentally Friendly Fruit Growing“ 222: 124–128. Libek, A., Kikas, A. and Hanni, L. 2005. The small fruit cultivars bred at Polli Horticultural Research Centre. In: Proceedings of the International Scientifi c Conference „Environmentally Friendly Fruit Growing“ 222: 98–102. Kikas, A., Libek, A. and Hanni, L. 2002. Evaluation of raspberry cultivars in Estonia. Acta Horticulturae 585: 203–207.

3.2. Articles published in books by Estonian or foreign publishers not listed in the ISI Web of Proceedings

Libek, A., Kikas, A. and Hanni, L. 2007. Small fruit cultivars bred at the Polli Horticultural Research Centre. Sovremennoje sostojanije kultur smorodiny i kryžovnika (Spornik nautchyh trudov), I.V. Mitchurin Research Institute: 116–119.

116 3.4. Articles published in the proceedings of International conferences

Arus, L., Luik, A., Libek, A. and Olep, K. 2008. The damage of the strawberry blossom weevil (Anthonomus rubi) depending on raspberry cultivars and mulching in Estonia. In: Dimza, I. et al. (eds.). Proceedings of the International Scientifi c Conference, Sustainable fruit growing: From plant to product; 2008 May 28-31; Jurmala–Dobele, Latvia. Latvia State Institute of Fruit- Growing: 244–249. Kikas, A., Kask, K., Jänes, H., Univer, T., Libek, A., Arus, L., Tiirmaa, K. and Kaldmäe, H. 2008. Fruit crop genetic resources in the Estonian University of Life Science. In: Dimza, I. et al. (eds.). Proceedings of the International Scientifi c Conference, Sustainable fruit growing: From plant to product; 2008 May 28-31; Jurmala–Dobele, Latvia. Latvia State Institute of Fruit- Growing: 149–157. Luik, A., Hanni, L., Merivee, E., Ploomi, A., Tarang, T. and Veromann, E. 2005. Studies in environmentally friendly plant protection in Estonia. NJF Report 1(1): 173–176. Luik, A., Tarang, T., Veroman, E., Kikas, A. and Hanni, L. 2002. Carabids in the Estonian crops. In Proceedings of the scientifi cs international conference „Plant protection in the Baltic region in the context of integration to EU“, Kaunas, Lithuania Sept. 26-27. 2002: 68–71. Hanni, L. and Luik, A. 2002. Occurence of spiders and carabids in raspberry plantation depending on different mulching. In Proceedings of the scientifi cs international conference „Plant protection in the Baltic region in the context of integration to EU“, Kaunas, Lithuania Sept. 26-27. 2002: 34–37.

3.5. Articles/presentations published in local conference proceedings

Luik, A., Eenpuu, R., Heidemaa, M., Arus, L., Tarang, T. and Vares, A. 2000. Carabids in different agrocoenosis of Estonia. In proceedings: „Development of environmentally friendly plant protection in the Baltic region“: International Conference; Tartu; 28.-29.09. 2000. Tartu: Estonian Agricultural University, 2000: 114–117.

117 6.3. Popular science articles (in Estonian):

Arus, L., Libek, A. 2013. Aedvaarika ja söödava kuslapuu sordid, nende kasvatus ja turustamise nõuded. Aiandusfoorum: 20–24. Arus, L., Luik, A. 2012. Vaarikamardika kahjustus sõltuvalt sordist ja õitsemise ajast. Teaduselt mahepõllumajandusele. Konverentsi toimetised: 9–11. Arus, L., Libek, A. and Kikas, A. 2008. Vaarikasortide võrdlev hindamine. Aiandusfoorum: 15. Libek, A., Hanni, L. and Kikas, A. 2004. Marja-aasta 2003 Pollis. Aiapidaja aastaraamat Aiatark: kalenderteatmik: 82–83. Arus, L. and Kask, K. 2007. Söödav kuslapuu sobib koduaeda. Maakodu 1: 72–74. Libek, A. and Arus, L. 2002. Väärtuslikud vaarikad. Aed (2002): 39–43.

6.4. Book (in Estonian)

Eskla, V., Libek, A., Hanni, L., Vool, E. and Niiberg, T. 2003. Vaarikas aias ja köögis. Tallinn: Maalehe Raamat

118

VIIS VIIMAST KAITSMIST

TEA TULLUS UNDERSTOREY VEGETATION AND FACTORS AFFECTING IT IN YOUNG DECIDUOUS FOREST PLANTATIONS ON FORMER AGRICULTURAL LAND ALUSTAIMESTIK JA SEDA MÕJUTAVAD TEGURID ENDISTEL PÕLLUMAJANDUSMAADEL KASVAVATES NOORTES LEHTPUUISTANDIKES Prof. Hardi Tullus, PhD Elle Roosaluste (Tartu Ülikool) 22. mai 2013

MIGUEL PORTILLO ESTRADA ON THE RELATIONSHIPS BETWEEN PLANT LITTER AND THE CARBON AND NITROGEN CYCLES IN EUROPEAN FOREST ECOSYSTEMS EUROOPA METSAÖKOSÜSTEEMIDE SÜSINIKU- JA LÄMMASTIKURINGE SEOSED TAIMSE VARISEGA Prof. Ülo Niinemets, teadur Steffen Manfred Noe 30. mai 2013

ZHIHONG SUN ISOPRENE EMISSION FROM ASPEN (Populus sp.) IN RELATION TO ENVIRONMENTAL DRIVERS KESKKONNATEGURITE MÕJU HAAVA (Populus sp.) ISOPREENI EMISSIOONILE Prof. Ülo Niinemets 5. juuni 2013

MIRJAM VALLAS GENETIC AND MODELLING ASPECTS OF MILK COAGULATION PROPERTIES IN DAIRY CATTLE PIIMA LAAPUMISOMADUSTE MODELLEERIMINE JA GENEETILINE DETERMINEERITUS Vanemteadur Elli Pärna, dots. Tanel Kaart, prof. Kalev Pärna (Tartu Ülikool) 27. juuni 2013

KARIN KALJUND GENETIC DIVERSITY, GENOTYPIC STRUCTURE AND VULNERABILITY OF NATIVE POPULATIONS OF SICKLE MEDIC (MEDICAGO SATIVA SSP. FALCATA) IN ESTONIA SIRPLUTSERNI (MEDICAGO SATIVA SSP. FALCATA) LOODUSLIKE POPULATSIOONIDE GENEETILINE MITMEKESISUS, GENOTÜÜPNE STRUKTUUR JA OHUSTATUS EESTIS Vanemteadur Malle Leht, vanemteadur Vello Jaaska 27. august 2013

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