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MASARYK UNIVERSITY

Faculty of Science

Department of Botany and Zoology

Radek MICHALKO

Spiders as bioagens of pome orchard pests

Ph.D. Dissertation

Supervisor: prof. Mgr. Stanislav Pekár, Ph.D. Brno, 2017

Bibliographic Entry

Author: MSc. Radek Michalko

Faculty of Science, Masaryk University,

Department of Botany and Zoology

Title of Dissertation: Spiders as bioagens of pome orchard pests

Degree Programme: Biology

Field of Study: Ecology

Supervisor: prof. Mgr. Stanislav Pekár, Ph.D.

Academic Year: 2017 / 2018

Number of Pages 148

Keywords Araneae, Biological control, Cacopsylla pyri,

Generalist predator, Food-web, Intraguild

predation, Predation, Trophic niche

Bibliografický záznam

Autor: Mgr. Radek Michalko

Přírodovědecká fakulta, Masarykova univerzita,

Ústav botaniky a zoologie

Název práce: Pavouci v biologickém boji proti škůdcům

v ovocných sadech

Studijní program: Biologie

Studijní obor: Ekologie

Vedoucí práce: prof. Mgr. Stanislav Pekár, Ph.D.

Akademický rok: 2016 / 2017

Počet stránek 148

Klíčová slova Araneae, Biologický boj, Cacopsylla pyri,

Generalistický predátor, Potravní síť,

Intraguildová predace, Predace, Trofická nika

ABSTRACT

Spiders are among the most abundant natural enemies in many agroecosystems. However, their role in biological control is still questionable because, as generalist predators, they may not only reduce pest populations but may also disrupt the biocontrol exerted by other natural enemies. This thesis focuses of improvement of spiders’ biocontrol potential in pome fruit orchards. A special focus was devoted to the system occurring in the pear orchards during winter, involving the winter-active spiders Philodromus spp. (Philodromidae) and Anyphaena accentuata (Anyphaenidae) and a psyllid pest Cacopsylla pyri, which belongs to the most serious pest of pears in Europe.

This dissertation thesis consists of six studies. The first study investigates the efficiency of various hunting strategies of spiders capturing different prey types. In general, spiders effectively capture prey like hemipterans and dipterans, but the different hunting strategies differ in their efficiency with respect to capturing specific prey type. The rest of the studies focus on trophic niches of philodromids and Anyphaena, intraguild predation (IGP) among the spiders, and the spiders’ ability to suppress psylla during winter and early spring. Winter- active spiders mostly prefer preying on pests in orchards and significantly reduce the population of C. pyri during winter and early spring. However, their efficiency is reduced by

IGP. IGP can be reduced by installation of corrugated cardboard bands around pear trees that provide refuges for small spiders. The efficiency of psylla suppression highly depends on the behavioral composition of the philodromid populations and the ratio between abundances of philodromids and the Dictyna sp. spiders. Aggressive philodromids kill more pests, are non-choosy, and do not prefer either psylla or Dictyna. Timid philodromids kill fewer pests, are choosy, and prefer psylla to Dictyna. The aggressive/non-choosy philodromids are more effective in psylla suppression when the Philodromus to Dictyna abundance ratio is high, while the timid/choosy philodromids are more effective when the ratio is low. The results of this thesis show that communities of the winter-active spiders can serve as highly efficient biocontrol agents in orchards.

ABSTRAKT

Pavouci patří mezi dominantní skupinu přirozených nepřátel škůdců v nejrůznějších agroekosystémech. Nicméně jejich přínos v biologickém boji proti škůdcům je dosud nejasný. Pavouci, jakožto generalističtí predátoři, mohou nejen snižovat abundance škůdců, ale i narušovat funkci ostatních přirozených nepřátel. Tato disertační práce se zabývá možnostmi, jak zvýšit efektivitu pavouků v biologickém boji proti škůdcům v ovocných sadech. Zvláštní pozornost je věnována pavoukům, kteří jsou aktivní v zimním období, listovníkům (Philodromus spp.) a šplhalce keřové (Anyphaena accentuata). Byla zkoumána jejich schopnost potlačovat meru hrušňovou (Cacopsylla pyri), která patří k nejzávažnějším

škůdcům v hrušňových sadech s vysokou resistencí vůči pesticidům.

Disertační práce se skládá ze šesti publikací. První publikace zkoumá, jakou kořist pavouci loví v závislosti na jejich lovecké strategii. Celkově pavouci loví převážně hmyz ze skupin

Hemiptera a Diptera, ale frekvence, s jakou pavouci s různými loveckými strategiemi loví různé typy škůdců, se liší. Ostatní studie se zabývají trofickou nikou listovníků a šplhalky, intragildovou predací a schopností pavouků potlačovat meru skvrnitou během zimy. Bylo zjištěno, že listovníci a šplhalka loví a zároveň preferují převážně typy hmyzu představující

škůdce ovocných sadů. Zároveň tito pavouci výrazně redukují populaci mery v průběhu zimy a začátkem jara. Jejich efektivita je ale snižována vzájemnou intragildovou predaci. Tu lze ovšem zmírnit instalací kartonových pásů kolem větví a kmene hrušní, které poskytnou úkryt pro malé pavouky. Efektivita potlačování mery je závislá na kombinaci behaviorálního složení populace listovníků a poměru abundancí listovníka a pavouka cedivečky Dictyna sp.

To je dáno tím, že agresivní listovníci sice zabijí více kořisti, ale nerozlišují mezi merou a cedivečkou. Naopak neagresivní listovníci zabijí méně kořisti, ale preferují meru před cedivečkou. Agresivní listovníci jsou efektivnější v případě, že poměr abundancí listovníků a cediveček je vysoký, zatímco neagresivní listovníci jsou efektivnější, pokud je tento poměr nízký. Výsledky disertační práce ukazují, že podpora výskytu pavouků aktivních v zimě, může výrazně přispět k potlačování škůdců ovocných sadů.

ACKNOWLEDGEMENT

The largest thanks go to my supervisor Prof. Stano Pekár for sharing his rich knowledge and experience, for patiently teaching me the ways of scientific thinking, and for his generous financial support. I am very grateful that he let me a lot of free will to do the research of my own interest but was still willing and able to provide me with numerous ideas and advices. I am also very grateful for his benevolence with my complete inability to keep the 9-17 attendance. Also, I really appreciate that he enabled me to visit all the international arachnological and other congresses in places I would hardly get to otherwise.

Special thanks go to Ondřej Košulič for the co-operation on many research projects and for the beers and shots in “Babka” and in various places around the world. Special thanks also go to Lenka Sentenská for her friendship, support, funny times, and the role of a confidant ear.

I would also like to thank my great friends and colleagues Radek Visner, Radomil Řežucha,

Milan Vrtílek, Pavel Šebek, and Jiří Šmejkal for their friendship, support, advices, for drawing my interest to their fields of study, and for the times around the grill. I am also very thankful to

Luboš Purchart for giving me the opportunity to work in his team, for support, and for creating the environment where I was able to combine my studies and work. I would like to thank also to many friends and/or colleagues from the Terrestrial Invertebrates Research Group at the

Masaryk University and from the Mendel University for their help, advices, support, and co- operations.

I am very grateful to my parents for their enormous support during the whole decade of my studies and for respecting my choice to catch spiders instead of drilling someone’s teeth.

Many thanks go also to all the reviewers for their comments that significantly improved the manuscripts.

TABLE OF CONTENTS

I. PREFACE……………………………………………………………... 19

II. INTRODUCTION……………………………………………………… 20

1. Current pest control………………………………………….. 20

2. Spider as biocontrol agents………..……………………….. 21

3. Trophic ecology of spiders in agroecosystems…..……….. 23

3.1. The determinants of spider trophic niches……….. 24

Hunting strategy………………………………... 25

Relative prey size………………………………. 25

Prey nutritional composition…………………... 25

Trophic niche dynamics…….…………………. 26

3.2. Predatory responses of spiders to pests…………. 27

Functional response…………………………… 28

Numerical response……………………………. 30

3.3. Non-consumptive effects………………………….... 31

4. The effects of multiple predators……………..…………….. 34

4.1. Antagonistic effects..………………………………... 34

Intraguild predation…………………………….. 34

Interference competition.……………………… 36

4.2. Additive and synergistic effects.…………………... 37

5. Pest suppression during winter…………………………….. 39

III. AIMS OF THE THESIS………………………………………………. 42

IV. CONCLUSION………………………………………………………... 44

V. REFERENCES……………………………………………………….. 46

VI. SUPPLEMENT……………………………………………………….. 63

1. Publications related to the thesis………………………….. 64

Study A………………………………………….. 66

Study B………………………………………….. 78

Study C………………………………………….. 88

Study D………………………………………….. 102

Study E………………………………………….. 112

Study F………………………………………….. 124

2. Author’s contribution………………………………………… 134

3. List of publications…………………………………………… 136

4. Review activity……………………………………………….. 141

5. Conference contribution…………………………………….. 142

6. Curriculum vitae……………………………………………… 148

I. PREFACE

This thesis deals with the role of spiders in conservation biological control in pome fruit orchards. It is based on six studies published in peer-reviewed journals. I am the first author of four studies and the second author of two studies. The data published in one study were obtained during my master studies. All other data were obtained during the doctoral studies.

The first study investigates the efficiency of various hunting strategies of spiders during capturing of different prey types. The rest of studies explore trophic niches of the spiders

Philodromus spp. and Anyphaena accentuata, intraguild predation among spiders, and the spiders’ abilities to suppress psylla during winter and early spring.

II. INTRODUCTION

1. Current insect pest control

The chemical control still represents the main way to control the insect pests despite its negative impact on the non-target organisms, such as pollinators, natural enemies, and even humans (Desneux et al. 2007; Pekár 2012; Shelton et al. 2014). It has been known for long that the overuse of chemical pesticides can (1) speed up evolution of resistance in pests, (2) lead to the ecological release and outbreak of primary or secondary pests (Dittrich et al.

1985; Furlong et al. 2004; Zhao et al. 2006; Pekár 2012). Yields of the crops treated by pesticides can be consequently similar or even lower than the yields of the untreated crops

(Furlong et al. 2004; Bommarco et al. 2011). The awareness of the negative impacts on the environment and often reduced efficiency of the chemical control have resulted in shift from conventional to more environmentally-friendly practices such as integrated pest management

(IPM) or organic farming.

IPM aims to combine use of the selective pesticides with other measures of pest control including mechanical, cultural, and biological practices (Vandermeer 2011).

Unfortunately, many “selective” pesticides are not selective enough and still negatively impact the arthropod natural enemies and pollinators. It is caused either by the active ingredients and / or the adjuvants (e.g. Řezáč et al. 2010; Biondi et al. 2012; Michalko &

Košulič 2016; Niedobová et al. 2016). It is, therefore, necessary to investigate how to improve other measures of pest control than the chemical one in order to minimize the environmental burden while keeping high yield and meeting growing demand for food

(Bommarco et al. 2013).

The most environmentally-friendly to control the pests seems to be the utilization of ecosystem services provided by a community of natural enemies, which is already present in an agroecosystem and its surrounding. In other words, it is better to prevent a pest outbreak than deal with the pest after its outbreak as postulated already by Riechert & Lockley (1984).

Indeed, several studies have demonstrated the irreplaceability of natural enemies in pest suppression and outbreak prevention in various perennial as well as annual agroecosystems

(reviewed, e.g., in Symondson et al. 2002). Given the enormous complexity of food webs and mechanisms driving the ecological dynamics, however, it remains a large challenge to find a way how to increase the efficiency of natural enemies so they would keep the pests under the economic thresholds steadily.

Spiders belong to the most abundant predators in many agroecosystems, either annual such as wheat (Schmidt et al. 2003; Traugott et al. 2012), rice (Bambaradeniya &

Edirisinghe 2008), or perennial such as vineyards (Costello & Daane 1999; Thomson &

Hoffmann 2010), and orchards (Miliczky & Horton 2005; Horton et al. 2012). At the same time, spiders are the most diversified generalist predators (WSC 2017), using very diverse hunting strategies (Cardoso et al. 2011), occupying various spatial niches from litter to tree canopies in the agroecosystems (Marc et al. 1999), distributed across several trophic levels

(Mestre et al. 2013; Sanders et al. 2015). Alike other natural enemies spiders have been observed to disrupt the pest control (Lang 2003). All this makes spiders an ideal model group to study the effect of generalist predators on the biological control.

The thesis’s introduction will focus on the several scales, from individuals to communities, that can affect spiders’ influence on the pest populations. At the individual and population scales, it will review the determinants and dynamics of spider trophic niches, like hunting strategy, size, life stage, nutritional target, and personality. The introduction will also review the predatory response and the non-consumptive effects of spiders to pest and factors that influence them. At the spider community scale, it will review the multiple-predator effect, i.e. antagonistic, additive, and synergistic effect. The last chapter is devoted to the pest suppression during winter and early spring.

2. Spiders as biocontrol agents

Spiders possess many exceptional traits for biocontrol. Spiders have high capture rate in comparison to other natural enemies and consume large number of prey (Wise 1993;

Nyffeler & Birkhofer 2017). They are well adapted to long periods of starvation, which enables them to maintain high abundances during periods when the pest is absent in the agroecosystem (Riechert & Harp 1987). Consequently, spiders can evince high predation pressure on the pest when it starts to invade an agroecosystem (Riechert & Lockley 1984;

Symondson et al. 2002). Therefore, spiders possess certain potential as the biocontrol agens. Spiders have been shown to reduce, e.g., aphids in wheat (Schmidt et al. 2004;

Birkhofer et al. 2008a), moths and aphids in apple orchards (Isaia et al. 2010; Lefebvre et al.

2016), dipteran pest in olive orchards (Picchi et al. 2016), and psyllids in pear orchards

(Pekár et al. 2015; Michalko et al. 2017).

However, spiders also lack several characteristics needed for a successful biocontrol.

Spiders have slow reproductive response as well as slow among-fields aggregative response so they cannot evince the density-dependent tracking of pest population growth (Symondson et al. 2002). Spiders, as generalist predators, can prey also on natural enemies and disrupt their biocontrol function (Traugott et al. 2012). Spiders have been observed to enhance, for example, thrips in wheat as they preyed on their natural enemies (Lang 2003).

Generalist predators, such as spiders, were traditionally considered as ineffective for biocontrol because the predation on non-target prey disrupts the pest control (Riechert &

Lockley 1984; Symondson et al. 2002). Nevertheless, this topic is largely unresolved as several studies show that the presence of alternative prey reduces, has no effect, or actually enhances the pest suppression (Birkhofer et al. 2008b; Knop et al. 2014; Welch et al. 2016).

To improve spiders’ pest control efficiency, it is necessary to investigate not only the factors that influence abundance and diversity of spiders in the agroecosystems (reviewed, e.g., in

Birkhofer et al. 2013; Baba & Tanaka 2016), but also connect it with their trophic ecology, which lags behind the diversity studies. The necessity to combine both approaches arises from the fact that the increased abundances and / or diversity of spiders do not always

translate in enhanced pest suppression (Hanna et al. 2003; Markó & Keresztes 2014;

Tscharntke et al. 2016). The mechanistic approach of trophic ecology can help to explain the reasons and it can help to decide how to manipulate the composition, diversity, and abundances of spiders in the agroecosystems to improve their biocontrol services.

3. Trophic ecology of spiders in agroecosystems

When studying biocontrol potential of spiders in the agroecosystems, one needs to consider the interplay among bottom-up, top-down, and intraguild interactions among spiders, their prey, and other natural enemies (Schmitz 2010; Hanley & Pierre 2015). Most spiders are generalist predators (Pekár et al. 2012), which can have various top-down effects on their prey but, from the biocontrol perspective, it is important that the generalist predators can significantly reduce prey population (e.g., Isaia et al. 2010), keep prey in low abundances

(e.g., Sinclair et al. 1998), or cause local extinction of prey (e.g., Cronin et al. 2004).

However, in the case of spiders in the agroecosystems, the prey may be pest, indifferent or beneficial.

From the bottom-up point of view, many pests are of sub-optimal quality as a prey for spiders, which negatively impacts their condition and fitness (e.g. Toft 2005; Bressendorf &

Toft 2011). Nutritionally complementary prey to pest can enhance fitness of spiders, maintain their high abundances in an agroecosystem, and keep high predation pressure on pests

(Oelbermann & Scheu 2009; Toft 2013; Tsutsui et al. 2016).

The investigation of spider trophic niches and their determinants helps to elucidate to a large extent the top-down and bottom-up interactions between spiders and their prey in agroecosystems. From the top-down point of view, the investigation of spider trophic niches and their determinants can help to evaluate the potential of spiders to supress certain pests or to disturb biocontrol of particular natural enemies. While from the bottom-up point of view, it can help to identify such prey, which would sustain abundant spider populations and maintained their high capture rates. Nonetheless, it is necessary to consider also other

effects than the diet composition that can affect the pest suppression. For example, some spider species with low preferences for a pest but high capture rate can reduce the pest more than other spiders with high preferences for the pest but with low capture rate

(Michalko & Pekár 2017). Alternatively, some spider species can evince strong non- consumptive effect causing lower fecundity, higher mortality or higher emigration rate of the pest. Such non-consumptive effects can overcome the consumptive effect (Werner & Peacor

2003; Schmitz 2010). The efficiency of spiders in pest suppression depends also on their interactions with other natural enemies. For example, the interference among predators can reduce the per capita prey capture (Schmidt et al. 2014; Michalko et al. 2017). Because of the low capture rate, the increased densities of spiders may not able to enhance the overall predation pressure on pest (Michalko et al. 2017).

3.1. The determinants of spider trophic niches

Most spiders are generalist predators that prey mostly on arthropods, especially insects and other spiders (Pekár et al. 2012; Michalko & Pekár 2016). The highest proportions in generalist spiders’ diet make Diptera, Hemiptera, Hymenoptera, and Coleoptera (Michalko &

Pekár 2016). Spiders were traditionally considered as highly opportunistic utilizing their prey proportionally to its availability (Riechert & Lockley 1984). However, recent research clearly indicates that despite being generalists, many spiders, if not most, show some degree of prey selectivity leading to a disproportional predation to prey availability (e.g. Nyffeler &

Sterling 1994; Agustí et al. 2003; Harwood et al. 2004; 2005; 2007; Kuusk & Ekbom 2010,

2012; Kobayashi et al. 2011; Chapman et al. 2012; Schmidt et al. 2012a; Michalko & Pekár

2015). The trophic niche of spiders depends on the interplay between traits of spiders (e.g., hunting strategy, size), of their prey (e.g., sclerotization, size, movement, dangerousness, nutritional content), and the environment (e.g., temperature, microhabitat structure, local selection pressures, prey community composition) (Riechert 1991; Kruse et al. 2008;

Richardson & Hanks 2009; Schmidt et al. 2012b; Sanders et al. 2015; Michalko & Pekár

2015). Given this, the realized niches of generalist spiders can evince a high spatio-temporal dynamics.

Hunting strategy.—Spiders employ a wide variety of hunting strategies (Cardoso et al. 2011), which differ in their efficiency to capture various prey types (Michalko & Pekár

2016). For example, spiders with a pursuing hunting mode are more effective in capturing a sedentary prey while spiders using a sit-and-wait hunting mode are more effective in capturing a highly mobile prey (e.g. Kuusk & Ekbom 2012; Sweeney et al. 2013).

Consequently, generalist spider predators with different hunting strategies utilize similar prey types but in different proportions (Michalko & Pekár 2016). Spiders with different hunting strategies can, therefore, differ in their efficiency to reduce various pests. For example, the cursorial ground hunting spider Pardosa littoralis Banks (Lycosidae) is highly effective in reducing abundances of two leafhopper species while the sheet-web weaving spider

Grammonota trivitatta Banks (Linyphidae) is ineffective (Denno et al. 2004). Similarly, Liu et al. (2015) found a negative relationship between cursorial spiders and leafhopper pest in the tea plantations, while no relationship between web spiders and the pest.

Relative prey size.—Generalist spiders seem to be specialized to certain prey size range (Nentwig & Wissel 1986; Yamanoi & Miyashita 2005; Okuyama 2007; Michalko &

Pekár 2014; 2015). Relatively small and large prey is often ignored by spiders because it is unprofitable (Stephens et al. 2007; Nentwig & Wissel 1986; Okuyama 2007). A particular spider species can be effective in suppression of several pests that fall within its size range.

On the other hand, a spider species may be limited to certain size cohorts of a pest with distinctively sized population, such as caterpillars.

Prey nutritional composition.—Spiders need to optimize their nutritional intake while minimizing the intake of toxins to maximize their fitness (Toft 2013). Different prey species are of different quality for spiders which are able to select prey according to its nutritional and toxin content (Toft 1999; Toft & Wise 1999a; Mayntz et al. 2005; Schmidt et al. 2012b). The trophic niche of spiders can be, therefore, determined by the nutritional content of pests and

other potential prey in the agroecosystem. Many pests seem to be of sub-optimal quality for spiders (e.g. Toft 2005). Spiders can have aversion and completely ignore a low quality prey

(Toft & Wise 1999a). However, due to generalized searching image (e.g., Pekár et al. 2013), the generalist spiders can keep attacking and killing low quality pests but exploiting it only shortly if high quality prey is present (Toft & Wise 1999a). Some prey of low quality can be ingested as it may contain essential nutrients (Toft 1995). Spiders will remain catching such prey though at lower frequency.

Trophic niche dynamics.—The dynamic of spider trophic niche is spatio-temporal. It depends on the state of an individual such as ontogenetic stage (Bartos 2011; Pekár et al. 2011), size

(Sanders et al. 2015), feeding history (hunger, nutritional state [Riechert 1991; Schmidt et al.

2012a,b]), environmental factors, such as temperature (Kruse et al. 2008), and on the presence of natural enemies and competitors (Michalko & Pekár 2014). Juvenile spiders can occupy distinct trophic niche than adults because of the size differences (Richardson &

Hanks 2009; Michalko & Pekár 2015; Sanders et al. 2015) and/or because of different nutritional requirements (Toft 2013). Spiders before overwintering can prefer lipid-rich prey to improve their energy state but after overwintering they can shift to more protein-rich prey to enhance their growth and development (Bressendorff & Toft 2011).

Actual temperature can affect the trophic niches of spiders because it influences movement of spiders and their prey, spiders’ catching ability, and escape ability of spiders’ prey (Kruse et al. 2008). Spiders can switch from sit-and-wait to more active hunting mode with increasing temperature or because temperature affects the silk properties (Yang et al.

2005; Kruse et al. 2008). Given the allometric species responses to the changing temperature, the trophic niche of spiders can differ between seasons, years, or regions

(Kruse et al. 2008; Dell et al. 2014).

The prey preference of a generalist predator can be also determined by the relative abundances of alternative prey. In other words, the rank of a pest species can change with its relative availability (Ryabov et al. 2015). For example, Schmidt et al. (2012a) found that

the wolf spider Pardosa milvina (Hentz) utilizes dipterans more frequently than expected, when they are scarce, but less frequently than expected, when they are overabundant. This is because spiders select prey to balance their nutritional targets (Schmidt et al. 2012b).

Similarly, Pardosa pseudoannulata (Boesenberg & Strand) preferred a planthopper over a mirid bug at low planthopper frequency, but mirid bugs at high plantohpopper frequency

(Heong et al. 1991).

The spider populations can be exposed to different selection pressures, which can select for certain behavioral phenotype, i.e. behavioral type. The selection pressures that produce different behavioral types can include, for example, prey availability, level of predation, and pesticide application (Riechert & Hedrick 1993; Royauté et al. 2014). The function of spiders in an agroecosystem can then largely depend on these local selection pressures (Royauté & Pruitt 2015). The aggressive individuals have higher capture rate than the timid individuals. The behavioral types can occupy distinct trophic niches (position, width)

(Riechert 1991; Michalko & Pekár 2014, 2017). The aggressive individuals then can have wider trophic niche than the timid individuals because they are less prey selective (Riechert

1991; Michalko & Pekár 2014; 2017). Individuals can also differ in level of their activity and, according to locomotor cross-over hypothesis (Huey & Pianka 1981), more active individuals will more likely catch the sedentary pest, while less active individuals will more likely catch the mobile pest (Sweeney et al. 2013). The distribution (mean, variance) of behavioral types within a spider population can have therefore profound effect on the abundances and pest community composition and suppression in an agroecosystem (Bolnick et al. 2011; Royauté

& Pruitt 2015; Michalko & Pekár 2017).

3.2. Predatory responses of spiders to pests

The total response of a predator to prey is a product of functional and numerical response

(Solomon 1949). The functional response expresses a relationship between prey density and mean number of prey killed by a single predator (Holling 1965), while numerical response

describes change in the numbers of predators through aggregation and reproduction

(Solomon 1949).

Functional response.— There are three basic types, I-III, although additional types have been described, such as the dome-shaped or roller-coaster type; all were documented in generalist spiders (Holling 1965; Riechert & Lockley 1984; Breene et al. 1990; Mansour &

Heimbach 1993; Jeschke & Tollrian 2005; Vucic-Pestic et al. 2010; Bressendorff & Toft 2011;

Schmidt et al. 2012a; Michalko & Košulič 2016).

The type I is characterized by a linear increase with prey density to some threshold above which the number of killed prey remain constant (Jeschke et al. 2004). A predator with functional response of type I kills constant proportion of prey with changing prey densities

(Jeschke et al. 2004). The type I functional response was observed in web spiders (e.g.

Mansour & Heimbach 1993) but also in hunting spiders affected by pesticides that kill but do not consume the prey so the handling and digesting times are reduced to a minimum

(Michalko & Košulič 2016).

Spiders have been considered to have mainly the hyperbolic type II (Riechert &

Lockley 1984; Wise 1993). The properties of type II functional response imply that predation pressure on pest is most intense at pest’s low densities (Sinclair et al. 1998). The abundant population/community of spider predators can, therefore, evince very intense predation pressure on the pest in the beginning of season when the pest begins to reproduce. This may lead to the local exclusion of a pest, it can keep the pest at very low densities, or it can significantly retard the pest’s population growth (Sinclair et al. 1998). So spiders, as generalist predators with type II, can prevent the population outbreak of pest. This has been supported empirically, e.g., in lycosid and thomisid spiders that retarded the growth of aphid pest at the beginning of season (Birkhofer et al. 2008a).

The type III is characterized by a sigmoid shape with a slow initial capture rate followed by a rapid increase that consequently slows down and converges to an asymptote

(Křivan 2008). The type III arises due to learning and/or prey switching (Sinclair et al. 1998).

The type III is the only functional response, which can per se stabilize the predator-prey system and the predator can keep the pest under control (Sinclair 1998). However, this is only possible if the density of pest falls within the area of densities where the killing rate increases more than proportionally to pest’s density and the pest does not exceed the release threshold (Křivan 2008). Although the type III was observed in spiders too, it has been traditionally considered rare (Riechert & Lockley 1984; Wise 1993). However, the presence of the type III functional response is probably largely underestimated due to the experimental settings. The functional responses of spiders have been investigated mostly with only single prey type or in homogenous environment which do not meet conditions needed for the type III to occur (Křivan 2008). The disproportional predation on various prey types than their availability (e.g. Nyffeler & Sterling 1994; Schmidt et al. 2012a) indicates the presence of prey switching in spiders. Spiders are also able to learn and avoid some noxious prey (Toft 1999). Prey switching has been observed, for example, in Tigrosa helluo

(Walckenaer) (Lycosidae), which prefers such prey that she consumed most recently

(Persons & Rypstra 2000).

In fact, the functional response in spiders, as generalist predators, is likely transitional between the type II and type III depending on the prey community composition (Morozov &

Petrovskii 2013; Ryabov et al. 2015). This arises from the imperfect prey selectivity, which means that prey are delimited with their traits such as size, movement, shape, etc. According to the similarity in these traits, predators may or may not be able to distinguish between prey types (Morozov & Petrovskii 2013; Ryabov et al. 2015). The switching will be likely present only in cases where predators are able to distinguish between preys before they kill. Spiders are able to distinguish between some prey species prior to the attack, while in other cases they need to kill it and taste it or they do not distinguish between the prey species at all. For example, the cursorial Philodromus spiders distinguished between a psylla pest and Dictyna spiders before they initiated an attack (Petráková et al. 2016). The cursorial Pardosa spiders

needed to taste aphids before they can distinguish between toxic and palatable aphid species (Toft & Wise 1999a).

Regardless the type of functional response, spiders have high asymptote of their capture frequency in comparison to other predators (Wise 1993). The high killing frequency results from partial feeding, and overkilling (Riechert & Harp 1987; Samu 1993; Samu & Bíró

1993). The high killing rate predestines spiders to impose high predation pressure on a pest.

The type IV functional response is dome-shaped, which means that the capture rate increases with prey density but above a threshold it sinks. In spiders, the dome-shaped capture rate can be caused, for example, by a nutritional imbalance induced by overconsumption of prey of low nutritional quality (Bressendorff & Toft 2011; Schmidt et al.

2012b). The absence of high quality prey or prey with complementary nutritional content

(alternative, pest) reduces conditions of spiders and consequently it can reduce their killing frequency. Therefore, the alternative prey can act as a nutritional balancer that would keep a high killing rate of the pest (Oelbermann & Scheu 2009; von Berg et al. 2009).

The fact that the alternative prey can either reduce, increase or have no effect on capture rate of pests by spiders is also mirrored in experimental studies investigating the pest suppression (Madsen et al. 2004; Birkhofer et al. 2008b; Gavish-Regev et al. 2008;

Oelbermann & Scheu 2009; Kuusk & Ekbom 2010, 2012; Kobayashi et al. 2011; Samu et al.

2013; Knop et al. 2014; Welch et al. 2016). Whether alternative prey disrupts the pest suppression seems to depend on the combination of several factors, such as nutritional and energetic values of pest and alternative prey as well as on the ratio of pest to alternative prey

(Madsen et al. 2004; Oelbermann & Scheu 2009).

Numerical response.— Although spiders have the outstanding dispersal ability, ballooning, it is a passive dispersal and so highly random (Decae 1987). In addition, the ballooning ability is limited to the relatively short life period in many spider species (Decae

1987). The aggregative response of spiders among crop fields is therefore ineffective in comparison to insect natural enemies with active flight, inasmuch as the random dispersal

imposes very long lags in the aggregative response (Riechert & Lockley 1984). Contrary to the slow long distance aggregative response, the within field response can be rather fast in cursorial species as some spiders can be relatively mobile within a crop field and its adjacent habitats (Samu et al. 1999). Indeed, spiders can aggregate in patches with high abundances of their preferred prey (Harwood et al. 2003; Schmidt & Rypstra 2010).

Given the fact that most spiders reproduce once per year while many pest species can have several generations per year, the tracking of pest density is impossible for spiders

(Riechert & Lockley 1984). Reproductive response of generalist predators, such as spiders, is not coupled with one prey species but rather it is connected to several prey species

(Murdoch et al. 2002). In addition, spiders are well adapted to the periods of famine (Riechert

& Harp 1987). All this enables spiders to maintain high population densities in the agroecosystems throughout the season when the pest is absent.

The clear drawback of spiders is that they are highly territorial with strong cannibalistic tendencies, which limits their numerical response (Wagner & Wise 1996; Wise 2006;

Schmidt & Rypstra 2010; Gan et al. 2015; Lesne et al. 2016).

3.3. Non-consumptive effects

Spiders, similarly to other predators, do not influence their prey by direct consumption, but also through the non-consumptive effects (Schmitz 2005; Bucher et al. 2014a). For a short period, the pest suppression can be larger due to the non-consumptive effect of spiders than due to consumptive effect (Cronin et al. 2004; Beleznai et al. 2017). Spiders can dislodge pests, such as caterpillars or aphids, which lead to increased mortality as the pests are more vulnerable to other predators or exposed to the stressful environmental conditions, or they are not able to find a way back and consequently starve (Sunderland 1999). Other non- consumptive effects include behavioural or physiological changes in pests as a response to a predation risk (Werner & Peacor 2003). The pests can reduce their movement and foraging activity to lower their detectability by spiders (Rypstra & Buddle 2013; Bucher et al. 2014a;

Beleznai et al. 2015) or can increase their mobility to flee away from acute danger and emigrate with consequent habitat shift (Schmitz et al. 1997; Binz et al. 2014; Bucher et al.

2015a). However, pests can also increase their foraging to satisfy the increased metabolism due to chronic stress and constant predator vigilance, which can lead to the increased herbivory and crop damage (Hawlena & Schmitz 2010a,b; Bucher et al. 2014b; Rendon et al.

2016). The behavioural / physiological changes are associated with the fitness costs - slower development, lower fecundity, and shorter longevity. All this then retards the pest population growth rate (Preisser & Bolnick 2008; Hawlena & Schmitz 2010b).

The type and intensity of the pest’s behavioural response to predation risk depends on the interplay between the traits of pest and predator and can change over the pest’s lifetime (Schmitz 2005). It depends on, for example, foraging mode of spiders and pests and their habitat domains (Miller et al. 2014), and the risk, which the predator represents for the pest (Binz et al. 2014). Schmitz (2005) provide a framework for the adaptive anti-predator response based on the combination of habitat domains and foraging modes. When the pest has a broad habitat domain (i.e. a pest individual roams widely) while the predator has narrow habitat domain, the adaptive anti-predator response is a habitat shift. If pest has narrow habitat domain, the anti-predator response should be activity reduction. This is conditioned by foraging mode of predators. If both, pest and predator, have broad domain and the predator use sit-and-move foraging mode, then the response should be either habitat shift or activity reduction. If the predator uses active hunting mode then the response should be flee-away from immediate danger. The pest can also respond only to predators that represent high risk. Binz et al. (2014) found that crickets responded by reduced or increased movement only to the chemo-tactile cues produced by large and common spiders. Rare and

/ or small spiders did not elicit any anti-predator response in the crickets.

As the pests’ response to predation risk is context-dependent, the way and strength how the non-consumptive effects of spiders cascade down on the crops is also context- dependent. The consumptive and non-consumptive effects interact and they can act

complementary or antagonistically (Schmitz 2005). In the former case, reduced feeding of pest and its mortality reduce crop damage or pathogen transmission. Increased pest foraging acts antagonistically, at least at short term. The net effect of a spider predator on a crop would then depend on the relative strength of the consumptive and non-consumptive effects and the fitness costs caused by the non-consumptive effect (Werner & Peacor 2003;

Hawlena & Schmitz 2010a). Enhanced per capita feeding of pests might buffer or even exceed the consumptive effect which can then result in no trophic cascade or even in negative effect on crops. For example, Rendon et al. (2016) found that spiders decreased number of a pest caterpillars on cotton by direct consumption but, at the same time, increased their herbivory by increased per capita foraging activity, which led to the reduced cotton yield. On the other hand, the stress elicited by the risk of predation may impose high pest mortality or low fecundity (Hawlena & Schmitz 2010b). The effects of high mortality and low fecundity of pest may exceed the enhanced per capita feeding rate of the pest. Thus, the population level herbivory can increase at short time but decrease at longer term. As the studies investigating the non-consumptive effects of spiders on pests are mostly short-term and conducted at the individual level, this question remains to be explored.

If the pest response to predation risk is emigration from spider-risk to the spider-free patches the result will be scale-dependent because the pest will cause less damage in the risky patches but more damage in the safe patches where it may aggregate (Schmitz et al. 1997;

Bucher et al. 2015b). The overall damage would then depend on the ratio, juxtaposition, and configuration between risky and safe patches and also on the quality of the safe patches

(Laundré et al. 2014). For example, in an agroecosystem with high risk: safe patches ratio, the indirect effect of spiders on crop would be positive. The positive effect of spiders on an agroecosystem would increase with the increasing ratio risk: safe patches faster the lower the quality of the safe patches for the pest would be, because of the increased pest mortality and reduced fecundity.

4. The effects of multiple predators

Spiders occur in an agroecosystem in a community with other natural enemies and the top- down control from this community strongly depends on the interactions among the natural enemies. The effect of predators can be additive (i.e. sum of the per capita effects of each predator species in a single population equals to that in the diverse predator community), synergistic (i.e. sum of the per capita effects of each predator species in a single population is lower than that in the diverse predator community), and antagonistic sum of the per capita effects of each predator species in a single population is higher than in the diverse predator community [Sih et al. 1998; Schmitz 2007]). The additive and synergistic predation enhances pest mortality while the antagonistic predation reduces pest mortality (Sih et al. 1998). Here, I will focus on the interactions among spiders for simplicity and space limitation, although spiders interact with many other natural enemies (Traugott et al. 2012; Sitvarin & Rypstra

2014).

4.1. Antagonistic effects

Intraguild predation (IGP).—IGP, i.e. predation among potential competitors, is inevitable in generalist predators (Polis et al. 1989). Spiders prey not only on other natural enemies like parasitoids and predaceous heteropterans (Whitehouse et al. 2011; Traugott et al. 2012) but also on spiders (Wise 1993). On the other hand, they are themselves exposed to predation from the predatory beetles, ants, birds, etc. (Wise 1993). Spiders represent a substantial portion mainly in the diet of cursorial spiders (Michalko & Pekár 2016). The IG prey, however, can be both cursorial and web spiders (Denno et al. 2004; Michalko & Pekár 2015).

IGP among spiders is size-dependent (Rypstra & Samu 2005; Okuyama 2007;

Korenko & Pekár 2010; Michalko & Pekár 2015). The probability of a mesopredator being killed rapidly decreases with decreasing top predator to mesopredator size ratio in comparison with other prey types (Rypstra & Samu 2005; Michalko & Pekár 2015). This is because spiders are dangerous prey and a mesopredator can seriously harm or even kill a

top predator (Foelix 2011; Michalko & Pekár 2017). Furthermore, generalist spider species lack specialized adaptations to overcome such prey (Pekár & Toft 2015). Other spiders, therefore, represent a low-rank diet item for generalist spiders and the intensity of IGP decreases with the availability of alternative palatable prey (Rickers et al. 2006; Oelbermann et al. 2008; Michalko & Pekár 2015; Petráková et al. 2016). However, if the top predator to mesopredator size ratio is sufficiently large, the IGP increases rapidly and very small spiders can become more preferable prey for the large spiders than pests (Michalko, unpubl.).

The general nutritional value of a mesopredator for a top predator is still not well known as ambiguous results were observed (Toft & Wise 1999b; Oelbermann & Scheu 2002;

Mayntz & Toft 2006). Mayntz & Toft (2006) concluded that IGP is highly profitable for spiders and the negative effect in other studies (Toft & Wise 1999b; Oelbermann & Scheu 2002) were caused by the reluctance to prey on the dangerous spiders. In addition, various trophic levels systematically differ in their macronutrient composition (Fagan & Denno 2004; Lease &

Wolf 2011). Preying on multiple trophic levels can help spiders to optimize their nutritional demand and IGP can act as a nutritional balancer (Matsumura et al. 2004; Mayntz & Toft

2006; Wilder et al. 2013). In addition, IGP can help to overcome the periods of alternative prey shortage, prevent starvation and maintain high abundances of spider top predators in the agroecosystem (Toft & Wise 1999b; Mayntz & Toft 2006).

The classical perspective is that IGP reduces the pest suppression due the consumptive and non-consumptive effects of a top predator on a mesopredator (Rosenheim et al. 1995; Müller & Brodeur 2002; Schmidt-Entling & Siegenthaler 2009). The non- consumptive effects are similar as in herbivores described above (see chap. 2.3.). The mesopredator can reduce its foraging (Walker & Rypstra 2003; Schmidt-Entling &

Siegenthaler 2009), emigrate (Mestre et al. 2014), change microhabitat (Folz et al. 2006), etc. IGP does not reduce predation pressure on pest only by the mesopredator, but the predation on mesopredator reduces the capture rate of pest also in the top predator (Pekár et al. 2015; Michalko & Pekár 2017).

Although, the consumptive as well as non-consumptive effects of IGP can lead to the ecological release of a pest (e.g. Finke & Denno 2004; Schmidt-Entling & Siegenthaler

2009), several interacting factors determine the extent to which IGP affects pest suppression.

It depends, for example, on the relative pest suppression efficiency of the predators, the top predator’s prey preferences, and mesopredator’s immigration rate (Rosenheim & Harmon

2006; Michalko & Pekár 2017). With respect to the suppression efficiency, if the top predator is more efficient in pest suppression than the mesopredator, then IGP will not have severe consequences for the biocontrol. If the mesopredator is highly effective against the pest, then

IGP can cause the ecological release of pest (Rosenheim & Harmon 2006; Michalko & Pekár

2017). However, regardless the differences in suppression efficiency between the predators, if the mesopredator’s mortality is buffered by immigration, the effect of IGP on pest suppression would be probably minimal.

Under some circumstances, IGP might, theoretically, have a synergistic effect instead of antagonistic. High consumption of pest can cause a nutritional imbalance in a top predator which reduces its per capita capture rate and fecundity (Toft 2005; Bressendorf & Toft 2011).

As the mesopredator can act as a nutritional balancer, IGP may maintain high capture rate and fecundity of the top predator (Mayntz & Toft 2006; Bressendorf & Toft 2011). The system with a nutritionally balanced top predator might be more efficient than the joint predation of the nutritionally imbalanced top predator and mesopredators. Nevertheless, this hypothesis needs to be tested experimentally and / or by simulation models.

Interference competition.—Non-consumptive interference among spiders of a similar size can also reduce their per capita capture rate (Schmidt & Rypstra 2010; Schmidt et al. 2014;

Michalko et al. 2017). Lower per capita capture rate can arise due to lost time in direct confrontations, reduced prey acceptance and/or reduced search efficiency due to reduced activity (Schmidt et al. 2014; Michalko et al. 2017). The per capita capture rate decreases with increasing spider density (Schmidt et al. 2014; Michalko et al. 2017). The interference can be so strong, that the enhanced densities of the predators may not be able to

compensate for lower capture rate, which can consequently reduce overall predation pressure on the pest. For example, Michalko et al. (2017) found that the overall predation pressure on a psyllid pest by Philodromus spiders increased only asymptotically with the spider densities. This clearly indicates that simply increasing abundances of spiders does not necessarily leads to increased predation pressure on pest. The non-consumptive interference can also lead to emigration due to reduced consumption that can further reduce the predation pressure on a pest (Schmidt & Rypstra 2010; Schmidt et al. 2014).

4.2. Additive and synergistic effects

In the synergistic predation, the pest changes its behaviour to avoid one predator but, at the same time, it makes itself more vulnerable to other predators. In additive predation, the vulnerability of the pest does not depend on the presence of the second predator (Losey &

Denno 1999). Nevertheless, in both cases the pest’s mortality increases. The additive and synergistic effects generally arise with some type of niche complementarity among the natural enemies (Schmitz 2007). The niche complementarity reduces the enemy-free space for the pest, minimizes IGP and interference among spiders. In addition, the utilization of alternative resources reduces exploitative competition and enables to build up larger populations of natural enemies and so enhances predation pressure on the pest by means of numerical responses. The niche complementarity works at intra-specific level (personality differences of individual specialization [Bolnick et al. 2011; Royauté & Pruitt 2015; Pruitt et al.

2016]) as well as inter-specific level (Losey & Denno 1999; Finke & Snyder 2008; Knop et al.

2014; Royauté & Pruitt 2015; Pruitt et al. 2016). Spiders can be complementary with regards to prey, space, time, and behavior.

Trophic niche complementarity arises when spiders utilize different prey types and/or sizes.

Except reducing the exploitation, the utilization of different prey type can also ensure that spiders aggregate in different prey patches (e.g., Harwood et al. 2003), which may, theoretically, reduce the number of safe patches for the pest (Laundré et al. 2014). With

respect to prey size, spiders can prey on different size cohorts of pests (Nentwig & Wissel

1986), which reduces the size-mediated enemy free space for the pest.

The spatial complementarity arises with horizontal and vertical stratification on various scales from habitats to microhabitats. For example, Takada et al. (2013) observed a synergistic predation on a mirid pest in the paddy fields evinced by tetragnathid and wolf spiders, which occupy distinct habitat domains. The mirids shifted from the rice canopy to lower plants’ parts to avoid predation, but instead they fell prey to wolf spiders (Takada et al.

2013).

The temporal complementarity includes distinct diurnal activity and distinct phenology among predators. For example, Picchi et al. (2016) found that the abundances of a dipteran pest in olive orchards was negatively correlated with philodromid spiders at the beginning of season while negatively correlated with linyphiids later in the season.

The spatio-temporal complementarity among spiders may also contain the conditions- dependent efficiency in pest suppression. For example, various spider species can switch in their pest suppression efficiency with a fluctuating temperature. Two syntopic cursorial spider species, Anyphaena accentuata (Walckenaer) (Anyphaenidae) and Philodromus cespitum

(Walckenaer), that occupy similar trophic niche, differ in their prey capture efficiency at various temperatures (Korenko et al. 2010; Petráková et al. 2016). Anyphaena is more efficient in capturing fruit flies at 15 °C while Philodromus is more efficient at temperatures above 20 °C (Korenko et al. 2010).

Spiders can be complementary also by means of hunting modes (Schmitz 2005). The adaptive response of pest to a sit-and-wait spider is reduced activity but this makes the pest more vulnerable to active spiders that search for an inactive prey (Schmitz 2005; Sweeney et al. 2013; Miller et al. 2014). Similarly, the adaptive response of pests to actively hunting spiders is enhanced activity as it tries to flee from immediate danger and / or emigrate but this makes the pest more vulnerable to the sit-and-wait predators (Schmitz 2005; Sweeney et al. 2013; Miller et al. 2014). Another behavioral complementarity may, theoretically, arise if a

highly size-structured pest, like caterpillars, reduces feeding activity due to anti-predator response (Schmitz 2005) and the retarded growth of pest may prevent to reach the size- mediated refuge from small predators.

5. Pest suppression during winter

In the temperate zone, most arthropods go through reproductive diapause, and mostly even through hibernation, during winter and early spring (Kirchner, 1987; Alford,

1999). However, a few arthropods remain active in the agroecosystems, including some spiders (Korenko et al. 2010; Boreau de Roincé et al. 2013; Pekár et al. 2015; Petráková et al. 2016; Michalko et al. 2017). The predation on pest by generalist spider predators during this period is probably crucial because it might determine the trajectory of pest’s population growth (Athey et al. 2016).

During winter and early spring, the winter-active spiders can be especially successful in pest suppression because the pest’s mortality is not compensated by its natality. In addition, the capture rate of the winter-active spiders remains high even at low temperature and it is not diluted among several prey because alternative prey are scarce

(Pekár et al. 2015). Indeed, generalist winter-active spiders have been shown to significantly reduce densities of aphids and psyllids already during winter (Boreau de Roincé et al. 2013;

Pekár et al. 2015; Petráková et al. 2016; Michalko et al. 2017).

The paucity of alternative prey in winter intensifies not only the predation on pest but also IGP among the winter-active spiders, which limits their predation pressure on a pest

(Gunnarsson 1985; Pekár et al. 2015; Petráková et al. 2016; Černecká et al. 2017).

However, IGP among the winter-active spiders decreases in heterogeneous environment that provides enemy-free shelters, like bark crevices, for the smaller spiders (Korenko &

Pekár 2010; Černecká et al. 2017). Providing artificial shelters during winter reducing IGP

(e.g., corrugated cardboard bands wrapped around the fruit trees) represents a promising environmentally-friendly management practice that enhances pest suppression by the winter-

active spiders (Michalko et al. 2017). On the other hand, the artificial shelters can also provide a refuge to the pest and enhance its abundance if the winter-active spiders are scarce (Michalko et al. 2017). Ideally, this within-field practice should be combined with the measures at the landscape scale that enhance the abundances of the winter active spiders in the agroecosystem (Lefebvre et al. 2016).

III. AIMS OF THE THESIS

1] Investigation of the natural prey of selected spider species using various methods, with special focus on the winter active spiders in fruit orchards [studies A-F].

2] Assessment of the environmental conditions under which the winter active spiders prey, of their ontogenesis, and of the prey consumption [Studies D-F].

3] Quantification of the predation pressure on the pest population and other spiders [C-F].

The spiders’ trophic niches were investigated by literature search and meta-analysis. Further research focused on trophic niches of winter active spiders, namely Philodromus cespitum,

P. aureolus, P. albidus, P. buchari, and Anyphaena accentuata by the direct field observations, molecular gut-content analysis, and prey acceptance experiments.

The environmental conditions influencing predatory activity were investigated a] by the series of experiments studying functional responses along the temperature gradient and b] by tracking the predation events throughout winter and early spring using molecular gut- content analysis. The ontogeny of winter active spiders during winter was assessed by a] rearing the spiders in laboratory and b] by size comparison between autumn and spring in the following year.

The predation pressure on pest and other spiders was quantified by a] model simulations using parameters obtained from the laboratory experiments and the field observations; b] manipulative experiments in the field; c] correlative relationships between abundances of the interacting species.

IV. CONCLUSION

Spiders are among the most abundant natural enemies of pest in various agroecosystems.

However, their role in biological control remains controversial because they not only suppress pest but also disrupt the biocontrol function provided by other natural enemies. In this thesis, I investigated the biocontrol potential of spiders in the pome fruit orchards. The potential of spiders as bioagents in the fruit orchards was evaluated by means of spiders’ trophic niches and their ability to supress pests. The model system represented the winter active spiders, Philodromus spp. and A. accentuata, and the pest Cacopsylla pyri

(Hemiptera, Psyllidae), one of the most serious pest in the pear orchards.

Overall, the largest proportions in the diet of generalist spiders are represented by

Diptera and Hemiptera. However, various hunting strategies employed by spiders differ in their efficiency to capture certain prey types. The relative frequency of hunting strategies in the spider assemblage can therefore have a large influence on the overall composition of herbivore community in fruit orchards. It is possible to employ management practices that enhance the abundances of particular hunting strategies that are the most effective in reducing a certain pest.

The winter active spiders, Anyphaena accentuata and Philodromus spp., have similar trophic niches. They prey on and prefer mostly the prey types that are considered pests in the fruit orchards, such as hemipterans, brachycerans, and lepidopterans (both adults and caterpillars). Therefore, they possess a certain biocontrol potential. However, they highly prey also on an alternative prey, like collembolans and nematocerans. The effect of these alternative prey taxa on biocontrol potential of the winter active spiders is not clear yet as they may disrupt, enhance, or have no effect at all on the pest suppression. Although the winter active spiders avoid other similarly sized spiders, small spiders, including some winter- active spiders, represent a substantial portion in their diet. IGP may therefore reduce their biocontrol potential.

Although philodromids are euryphagous, individuals within the population have distinct prey preferences, which are associated with their foraging aggressiveness.

Individuals that are more aggressive kill more pest and have wider trophic niches because they do not distinguish between the pest C. pyri and Dictyna spiders. The timid individuals kill less pest but are choosy and prefer the psylla to dictynids. These differences in trophic traits influence the dynamics of IGP at least in a short term period. During the short-term pest suppression, the system with aggressive individuals is more effective when the Dictyna to

Philodromus abundance ratio is low, whereas the system with timid individuals is more effective when the ratio is high. In addition, a system with both predators limits the prey more when dictynids are abundant. This suggests that the timid/choosy behavioral type of philodromids might limit the population of the psylla more in habitats where both spider species are relatively abundant.

During winter and early spring, the winter active spiders prey on the pest C. pyri, but

Anyphaena also preys heavily on philodromids. Despite the strong IGP, the community of winter active spiders significantly reduces the psylla’s densities during this period. The IGP among winter active spiders can be reduced by wrapping the pear trees by corrugated cardboard bands that provide enemy-free shelters for smaller philodromids. This consequently improves the psylla suppression by the winter active spiders.

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Sweeney, K., Cusack, B., Armagost, F., O’Brien, T., Keiser, C. N. & Pruitt, J. N. (2013).

Predator and prey activity levels jointly influence the outcome of long-term foraging bouts.

Behavioral Ecology, 24(5), 1205-1210.

Symondson, W. O. C., Sunderland, K. D., Greenstone, M. H. (2002). Can generalist

predators be effective biocontrol agents? Annual Review of Entomology, 47: 561-594.

Takada, M. B., Kobayashi, T., Yoshioka, A., Takagi, S. & Washitani, I. (2013). Facilitation of

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spiders in organic paddy fields. Journal of Arachnology, 41(1), 31-35.

Tscharntke, T., Karp, D. S., Chaplin-Kramer R. et al. (2016). When natural habitat fails to

enhance biological pest control–Five hypotheses. Biological Conservation, 204, 449-458.

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importance of local vegetation. Biological Control, 52(2), 160-166.

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Applied Ecology, 32(3), 552-560.

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Toft, S. (2005). The quality of aphids as food for generalist predators: implications for natural

control of aphids. European Journal of Entomology, 102(3), 371.

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generalist predators (Tetragnatha spider) in environmentally friendly paddy fields. Applied

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spiders to cotton: behaviourally mediated predator effects over four trophic levels. Austral

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895-902.

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Plutellidae) resistance to spinosad, indoxacarb, and emamectin benzoate. Journal of

Economic Entomology, 99(1), 176-181.

VI. SUPPLEMENT

1. Publications related to the thesis

2. Author’s contribution

3. List of publications

4. Review activity

5. Conference contribution

6. Curriculum vitae

1. Publications related to the thesis

Study A. Michalko, R. & Pekár, S. (2016) Different hunting strategies of generalist predators result in functional differences. Oecologia, 181, 1187–1197.

Study B. Michalko, R. & Pekár, S. (2015). The biocontrol potential of Philodromus

(Araneae, Philodromidae) spiders for the suppression of pome fruit orchard pests. Biological

Control, 82, 13–20.

Study C. Michalko, R. & Pekár, S. (2017). The behavioral type of a top predator drives the short-term dynamic of intraguild predation. American Naturalist, 189, 242–253.

Study D. Petráková, L., Michalko, R., Loverre, P., Sentenská, L., Korenko, S. & Pekár, S.

(2016) Intraguild predation among spiders and their effect on the pear psylla during winter.

Agriculture Ecosystems & Environment, 233, 67–74.

Study E. Pekár, S., Michalko, R., P., Loverre, P., Líznarová, E. & Černecká, Ľ. (2015)

Biological control in winter: novel evidence for the importance of generalist predators. Journal of Applied Ecology, 52, 270–279.

Study F. Michalko, R., Petráková, L., Sentenská, L., Pekár, S. (2017) The effect of habitat complexity and density-dependent non-consumptive interference on pest suppression by winter-active spiders. Agriculture Ecosystems & Environment, 242, 26–33.

Study A Different hunting strategies of generalist predators result in

functional differences.

Michalko, R. & Pekár, S. (2016) Oecologia, 181, 1187–1197.

Study B The biocontrol potential of Philodromus (Araneae,

Philodromidae) spiders for the suppression of pome fruit

orchard pests.

Michalko, R. & Pekár, S. (2015) Biological Control, 82, 13–20.

Study C The behavioral type of a top predator drives the short-term

dynamic of intraguild predation.

Michalko, R. & Pekár, S. (2017) American Naturalist, 189, 242–253.

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Study D Intraguild predation among spiders and their effect on the pear

psylla during winter

Petráková, L., Michalko, R., Loverre, P., Sentenská, L., Korenko, S. & Pekár, S. (2016).

Agriculture Ecosystems & Environment, 233, 67–74.

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Study E Biological control in winter: novel evidence for the importance of

generalist predators.

Pekár, S., Michalko, R., P., Loverre, P., Líznarová, E. & Černecká, Ľ. (2015) Journal of

Applied Ecology, 52, 270–279.

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Study F The effect of habitat complexity and density-dependent non- consumptive interference on pest suppression by winter-active

spiders.

Michalko, R., Petráková, L., Sentenská, L., Pekár, S. (2017). Agriculture Ecosystems &

Environment, 242, 26–33.

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Authors’ contribution

Study A.

Michalko, R. & Pekár, S. (2016) Different hunting strategies of generalist predators result in functional differences. Oecologia, 181:1187–1197. IF2016 = 3.130

RM conceived the idea and designed the study; searched the literature and collected the data; performed the statistical analyses. RM and SP wrote the manuscript. Contribution of

RM was 90%.

Study B.

Michalko, R. & Pekár, S. (2015) The biocontrol potential of Philodromus (Araneae,

Philodromidae) spiders for the suppression of pome fruit orchard pests. Biological Control,

82:13–20. IF2015 = 2.012

RM conceived the idea; performed the experiments and the statistical analyses. RM and

SP designed the experiments. and wrote the article. Contribution of RM was 80%.

Study C.

Michalko, R. & Pekár, S. (2017) The behavioral type of a top predator drives the short-term dynamic of intraguild predation. American Naturalist, 189:242–253. IF2016 = 4.167

RM conceived the idea and designed the experiments; performed the experiments, simulations, and the statistical analyses. RM and SP developed the model and wrote the manuscript. Contribution of RM was 80%.

Study D.

Petráková, L., Michalko, R., Loverre, P., Sentenská, L., Korenko, S. & Pekár, S. (2016)

Intraguild predation among spiders and their effect on the pear psylla during winter.

Agriculture Ecosystem & Environment, 233:67–74. IF2016 = 4.099

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SP conceived the idea. SP and RM designed the experiments. RM, LP, PL, LS, and SK performed the experiments. LP and PL designed the DNA primers. SP and RM performed the statistical analyses. SP, LP, and RM wrote the manuscript. Contribution of RM was 20%.

Study E.

Pekár, S., Michalko, R., P., Loverre, P., Líznarová, E. & Černecká, Ľ. (2015) Biological control in winter: novel evidence for the importance of generalist predators. Journal of

Applied Ecology, 52:270–279. IF2015 = 5.196

SP conceived the idea. SP and RM designed the experiments. RM, PL, EL, ĽČ performed the experiments. SP developed the model and performed the simulations. SP and

RM performed the statistical analyses. SP wrote the manuscript. Contribution of RM was

30%.

Study F.

Michalko, R., Petráková, L., Sentenská, L., Pekár, S. (2017) The effect of habitat complexity and density-dependent non-consumptive interference on pest suppression by winter-active spiders. Agriculture Ecosystem & Environment, 242:26–33. IF2016 = 4.099

RM and SP conceived the idea. RM and SP designed the experiments. RM, LP, and LS performed the experiments. RM performed the statistical analyses. RM, LP, and SP wrote the manuscript. Contribution of RM was 60%.

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2. List of publications

3.1. Publications with IF

Michalko R. & Pekár S. (2017) The behavioral type of a top-predator drives the short-term dynamic of intraguild predation. American Naturalist, 189, 242–253. IF2016 = 4.167

Michalko R., Košulič O. & Řežucha R. (2017) Link between aggressiveness and shyness in the spider Philodromus albidus (Araneae, Philodromidae): state dependency over stability.

Journal of Insect Behavior, 30, 48–59. IF2016 = 0.970

Černecká L’., Michalko, R. & Krištín A. (2017) Abiotic factors and biotic interactions jointly drive spider assemblages in nest-boxes in mixed forests. Journal of Arachnology, 45, 213-

222. IF2016 = 0.988

Havlová L., Hula V., Niedobová J. & Michalko, R. (accepted). Effect of adjacent steppe-like habitats on spider diversity in vineyards. BioControl. IF2016 = 1.918

Michalko, R. & Košulič, O. (2016) Temperature-dependent effect of two neurotoxic insecticides on predatory potential of Philodromus spiders. Journal of Pest Science, 89, 517–

527. IF2016 = 3.728

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Michalko R., Košulič O., Hula V. & Surovcová K. (2016) Niche differentiation of two sibling wolf spider species, Pardosa lugubris and Pardosa alacris, along a canopy openness gradient. Journal of Arachnology, 44, 46–51. IF2015 = 0.988

Michalko, R. & Pekár, S. (2016) Different hunting strategies of generalist predators result in functional differences. Oecologia, 181,1187–1197. IF2015 = 3.130

Korenko, S., Niedobová, J., Kolářová, M., Hamouzová, K., Kyslíková, K. & Michalko, R.

(2016) The effect of eight common herbicides on predatory activity of agrobiont spider

Pardosa agrestis. BioControl, 61, 507–517. IF2016 = 1.918

Košulič O., Michalko R. & Hula V. (2016) Impact of canopy openness on spider communities: Implications for conservation management of formerly coppiced oak forests in

Central Europe. PloS ONE, 11, e0148585. IF2016 = 2.806

Niedobová, J., Hula, V. & Michalko, R. (2016) Sublethal effect of agronomical surfactants on spider Pardosa agrestis. Environmental Pollution, 213, 84–89. IF2016 = 5.009

Petráková, L., Michalko, R., Loverre, P., Sentenská, L., Korenko, S. & Pekár, S. (2016)

Intraguild predation among spiders and their effect on the pear psylla during winter.

Agriculture Ecosystem & Environment, 233, 67–74. IF2015 = 4.099

Michalko, R. & Pekár, S. (2015) The biocontrol potential of Philodromus (Araneae,

Philodromidae) spiders for the suppression of pome fruit orchard pests. Biological Control,

82, 13–20. IF2015 = 2.012

Michalko R. & Pekár S. (2015) Niche partitioning and niche filtering jointly mediate the

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coexistence of three closely related spider species (Araneae, Philodromidae). Ecological

Entomology, 40, 22–33. IF2015 = 1.687

Pekár S., Michalko R., Loverre P., Líznarová E. & Černecká L. (2015) Biological control in winter! Novel evidence for importance of generalist predators. Journal of Applied Ecology,

52, 270–279. IF2015 = 5.196

Michalko R. & Pekár S. (2014) Is different degree of individual specialization in three spider species caused by distinct selection pressures? Basic and Applied Ecology, 15, 496–506.

IF2014 = 1.942

Košulič O., Michalko R. & Hula, V. (2014) Recent artificial vineyard terraces as a refuge for rare and endangered spiders in a modern agricultural landscape. Ecological Engeneering,

68, 133-142. IF2014 = 2.580

Pekár, S., Michalko R., Korenko S., Šedo O., Líznarová E., Sentenská L. & Zdráhal Z.

(2013) Phenotypic integration in a series of trophic traits: tracing the evolution of myrmecophagy in spiders (Araneae). Zoology, 116, 27–35. IF2013 = 1.596

Kehlmaier C., Michalko R. & Korenko S. (2012) Ogcodes fumatus (Diptera: Acroceridae) reared from Philodromus cespitum (Araneae: Philodromidae), and first evidence of

Wolbachia Alphaproteobacteria in Acroceridae. Annales Zoologici, 62, 281–286. IF2012 =

0.660

3.2. Submitted manuscripts:

Michalko R. & Košulič O. (under review) Management type in fruit orchards alters the

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functional community structure of arthropod predators. International Journal of Pest

Management.

Michalko R., Košulič O., Pung T. & Vichitbandha P.T. (submitted) Predictability in a lynx spider is interactively influenced by behavioral type, prey density, and an insecticide. Current

Zoology.

Michalko R., Kula E. & Košulič O. (submitted) Temperature and liming alter body size distribution in a community of epigeic spiders. Annals of Forest Science.

Michalko, R., Pekár, S. & Entling, M.H. (submitted). The role of generalist predators in biological control – an updated perspective using spiders. Advances in Agronomy

Michalko, R. & Řežucha, R. (in revision) Top predator's aggressiveness and mesopredator's shyness additively determine probability of predation during predator-predator interaction.

Behavioral Ecology & Sociobiology

Michalko R., Košulič O, Wongprom P. (in revision) Latitudinal gradient of spider diversity in dry dipterocarp forests of Thailand. Ecological Research.

Cardoso J.C.F., Michalko R., Gonzaga M.O. (under review) Coexistence mechanisms and parasite-mediated indirect effect on niche occupation of two closely related spider species.

Oecologia

Heroldová M., Michalko R., Suchomel J. & Zejda J. (under review). Influence of field ploughing method on common vole (Microtus arvalis) abundance. Pest Management

Science.

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Košulič O., Pung T., Vichitbandha, P. & Michalko, R. (in revision). The effects of plant extracts from Embelia ribes and two commercial biopesticides on a generalist predator.

Journal of Applied Entomology

2.3. Publications aimed at wider public:

Falta, V., Bagar, M., Bagarová, K., Holý K.,, Hortová B., Chaloupka M.,, Kloutovrová, J.,

Kocourek, F., Loskot, R., Michalko, R., Navrátil, M., Pekár S., Psota, V., Suchá J. & Vávra,

R. (2016) Ochrana jádrovin v ekologické produkci.

Michalko, R. (2015) Utváření a význam pavoučích osobností v ekologické dynamice. Živa

5/2015.

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4. Review activity

Agriculture Ecosystems & Environment

Animal Biodiversity and Conservation

Annales Zoologici Fennici

Arachnology

Ecography

Ecological Entomology

Journal of Arachnology

Journal of Insect Behavior

Polish Journal of Ecology

Thailand Natural History Museum Journal

Tropical Ecology

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5. Conference contribution

5.1. International:

Michalko R., Košulič O., Pung T. & Vichitbandha P.T. (2017): The predictability in predatory activity of the spider Oxyopes lineatipes is interactively influenced by behavioral type, prey density, and neem application. 4th Conference of the Asian Society of Arachnology,

Chongqing, China.

Michalko R. & Pekár S. (2017): The behavioral type of a top-predator drives the short-term dynamic of intraguild predation. 5th International Symposium on Biological Control of

Arthropods. Langkawi, Malaysia. (poster)

Michalko R., Košulič O., Pung T. & Vichitbandha P.T. (2017): Neem application alters the relationship between predatory activity and behavioural predictability along a prey-density gradient in the spider Oxyopes lineatipes. 30th European Congress of Arachnology,

Nottingham, UK. (oral presentation).

Petcharad, B., Košulič, O., Bumrungsri, S., Michalko, R. (2017): Alteration of predatory behavior of a generalist predator by exposure to two insecticides. 5th International

Symposium on Biological Control of Arthropods. Langkawi, Malaysia. (poster)

Michalko, R., Kula, E., Košulič, O. (2016): The effect of liming on epigeic hunting spiders differs between birch wood stands and grass clearings. 17th International Congress of Soil

Zoology. Nara, Japan. (oral presentation).

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Michalko, R., Petraková, L., Sentenská L., Pekár S. (2016): Effect of increased habitat complexity on pest supression by winter-active spiders. 20th International Congress of

Arachnology. Golden, USA. (oral presentation)

Košulič, O., Michalko R., Purchart, L., Larionova, M., Surovcová, K. (2016) Ground dwelling arthropod assemblages during succesion stages of a commercial lowland forest. 17th

International Congress of Soil Zoology. Nara, Japan. (poster)

Košulič, O., Michalko, R., Surovcová, K., Hula, V. (2016) Impact of canopy openness on epigeal spider communities with implications on conservation management of forest biodiversity. 17th International Congress of Soil Zoology. Nara, Japan. (poster)

Petcharad, B., Košulič, O., Bumrungsri, S., Michalko, R. (2016) Alteration of predatory behavior of a generalist predator by exposure to two insecticides. 20th International

Congress of Arachnology. Golden, USA. (poster)

Michalko, R., Košulič, O. & Hula, V. (2015) The relationship between niche properties and composition of spider communities in vineyard terraces. 29th European Congress of

Arachnology. Brno, Czech Republic. (oral presentation)

Michalko, R. & Pekár, S. (2015) Increased habitat complexity improves the suppression of pest Cacopsylla pyri by winter-active spiders. 29th European Congress of Arachnology.

Brno, Czech Republic. (poster)

Dudová, P., Michalko R., Klečka, J. & Pekár, S. (2015) Individual behavioural differences in a specialized ant-eating spider Zodarion rubidum. 29th European Congress of Arachnology.

Brno, Czech Republic. (poster)

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Havlová, L., Hula, V., Niedobová, J. & Michalko, R. (2015) Araneofauna of grapevines under different management regimes - increasing diversity and abundance of spiders in agroecosystem. 29th European Congress of Arachnology. Brno, Czech Republic.

Košulič, O., Michalko, R., Surovcová, K. & Hula, V. (2015) Effect of canopy openness on distribution of epigeal spider communities in former coppiced oak forest stands with implications on forest management. 29th European Congress of Arachnology. Brno, Czech

Republic (oral presentation).

Košulič, O., Michalko, R., Pung, T. & Vichitbandha, P. (2015) Toxicity effect of a crude extract of Embelia ribes and two commercial pesticides on mortality and foraging behaviour of a potential biocontrol agent Oxyopes lineatipes. 29th European Congress of Arachnology.

Brno, Czech Republic. (poster)

Niedobová, J., Hula, V. & Michalko, R. (2015) Sublethal effect of agronomical surfactants on spider Pardosa agrestis. 29th European Congress of Arachnology. Brno, Czech Republic.

(poster)

Pekár, S., Michalko R., Loverre, P., Líznarová, E. & Černecká, L. (2015) Biological control in winter! Novel evidence for importance of generalist predators. 29th European Congress of

Arachnology. Brno, Czech Republic (oral presentation).

Michalko, R. & Pekár, S. (2014) Implications of behavioral traits of an intra-guild predator for biological control. In 28th European Congress of Arachnology, Torino, Italy. (oral presentation)

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Michalko, R., Košulič, O. & Hula, V. (2014) Changes in coexistence mechanisms with spatial scale and management type in the spider communities from vineyard terraces. In 28th

European Congress of Arachnology. Torino, Italy. (poster)

Michalko, R. (2014) Are distinct hunting strategies of euryphagous spiders linked to their trophic functional distinction? 28th European Congress of Arachnology. Torino, Italy. (poster)

Košulič, O., Michalko, R. & Hula, V. (2014) Vineyard terraces as a refuge for rare and endangered spiders in a modern agriculture landscape. 28th European Congress of

Arachnology. Torino, Italy. (oral presentation)

Košulič O., Michalko R., Hula V. & Surovcová, K. (2014) Effect of canopy openness on distribution of sibling species from Pardosa lugubris-group (Araneae, Lycosidae). 28th

European Congress of Arachnology. Torino, Italy.

Michalko, R. & Pekár, S. (2013) Different degree of individual specialisation in three

Philodromus species (Araneae: Philodromidae) is caused by influence of different selection pressures. 19th International Congress of Arachnology. Kenting National Park, Taiwan

Košulič, O., Michalko, R. & Hula, V. (2013) Do vineyard terraces act as a refuge for xerothermic spiders in high-pressure agriculture landscape? 19th International Congress of

Arachnology. Kenting National Park, Taiwan.

Michalko, R. & Pekár, S. (2012) Coexistence among three Philodromus species (Araneae,

Phildromidae). 27th. European Congress of Arachnology. Ljubljana, Slovenia.

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5.2. Domestic:

Michalko, R., Košulič, O. & Hula, V. (2016) Vztah mezi vlastnostmi niky a složením společenstva pavouků na viničních terasách. Zoologické dny 2016. České Budějovice.

Michalko, R. & Košulič, O. (2015) Teplotně specifický účinek pesticidů na predační potenciál listovníků (Araneae, Philodromidae). Zoologické dny 2015, Brno. (poster)

Havlová L., Hula V., Niedobová J. & Michalko R. (2015) Differences in species diversity of spiders on grape vine on terraced and conventional vineyards depending on the type of management. Zoologické dny 2015. Brno. (poster)

Košulič, O., Michalko R., Hula, V. & Surovcová, K. (2015) Effect of canopy openness on distribution of sibling species from Pardosa lugubris-group (Araneae, Lycosidae). Zoologické dny 2015. Brno

Michalko, R. (2014) Lovecká strategie jako "měkký" funkční znak euryfágních pavouků.

Zoologické Dny 2014. Ostrava. (oral presentation)

Havlová, L.., Hula, V., Niedobová, J. & Michalko, R. (2014) Differences in spider species diversity on grapevine plants on terraced and plain vineyards depending on the type of management. MendelNet, Brno. (oral presentation)

Košulič, O., Michalko, R. & Hula, V. (2014) Importance of recent artificial vineyard terraces for xerothermophilic spiders in high-pressure agriculture landscape. Zoologické Dny 2014.

Ostrava. (oral presentation)

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Michalko, R. & Pekár, S. (2013) Individuální specializace pavouků rodu Philodromus.

Zoologické dny 2013. Brno. (oral presentation)

Michalko, R. 2013. Lze různé lovecké strategie euryfágních pavouků použít jako proxy pro jejich funkční odlišnost? Ekologie. Brno. (poster)

Košulič, O., Michalko, R. & Hula, V. (2013) Význam vyničních teras pro vzácné a ohrožené druhy xerotermních pavouků. Ekologie. Brno.

Michalko, R. & Pekár, S. (2012) Eko-evoluční dynamika niky umožňuje koexistenci mezi třemi blízce příbuznými druhy pavouků rodu Philodromus. Kostelecké Inspirování. Praha.

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7. Curriculum vitae

Name: Mgr. Radek Michalko

Education

2009-2012: Mgr., Systematic Biology and Ecology, Coexistence and niche partitioning in spiders of the genus Philodromus. Faculty of Science, Masaryk University.

2006-2009: Bc., Systematic Biology and Ecology, Ecophysiological adaptation of Selamia spiders to myrmecophagy. Faculty of Science, Masaryk University

Employment history

4/2015-present Department of Forest Ecology, Faculty of Forestry and Wood Technology, Mendel University in Brno. Researcher.

4/2012- 12/2016 Department of Botany and Zoology, Faculty of Science, Masaryk University. Researcher.

Awards

4/2017 Masaryk University Rector’s Award for Outstanding PhD Student

2017-10-04, Brno, Czech Republic

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