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. © Radek Michalko, Masaryk University, 2017 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 18 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