Ben-Gurion University of the Negev the Jacob Blaustein Institutes for Desert Research the Albert Katz International School for Desert Studies
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I Ben-Gurion University of the Negev The Jacob Blaustein Institutes for Desert Research The Albert Katz International School for Desert Studies The trophic niche of synanthropic insectivorous bats (Kuhl's pipistrelle, Pipistrellus kuhlii) and their potential contribution to arthropod pest suppression Thesis submitted in partial fulfillment of the requirements for the degree of "Master of Science" By Yuval Cohen March 2018 II Ben-Gurion University of the Negev The Jacob Blaustein Institutes for Desert Research The Albert Katz International School for Desert Studies The trophic niche of synanthropic insectivorous bats (Kuhl's pipistrelle, Pipistrellus kuhlii) and their potential contribution to arthropod pest suppression Thesis submitted in partial fulfillment of the requirements for the degree of "Master of Science" By Yuval Cohen Under the Supervision of Professors Carmi Korine and Shirli Bar David Mitrani Department of Desert Ecology Author's Signature ……………… … ……… Date 18/3/2018 Approved by the Supervisor … … .. Date 18/3/2018 Approved by the Supervisor ….. .… Date 18/3/2018 Approved by the Director of the School ……………… Date 18/3/2018 III The trophic niche of synanthropic insectivorous bats (Kuhl's pipistrelle, Pipistrellus kuhlii) and their potential contribution to arthropod pest suppression By Yuval Cohen Thesis submitted in partial fulfillment of the requirements for the degree of "Master of Science" Ben-Gurion University of the Negev The Jacob Blaustein Institutes for Desert Research The Albert Katz International School for Desert Studies 2018 ABSTRACT Conservation Biological Control (CBC) attempts to support the management of agricultural pests by identifying, preserving and enhancing the efficiency of natural enemies. Synanthropic insectivorous bats, are abundant in urban and agricultural ecosystems and can potentially suppress pest irruptions through opportunistic feeding. Yet, few studies described their trophic niche to high taxonomic resolution or related their diets to ecosystem services and their possible role in CBC. Pipistrellus kuhlii, a synanthropic generalist insectivorous bat, forages intensively over agricultural fields, including cotton fields in Israel. Hence, it has potential as a biological pest suppression agent. My working assumption is that synanthropic generalist insectivorous, such as P. kuhlii bats, regularly provide ecosystem services and are suitable natural enemies for CBC, particularly that P. kuhlii bats respond to pest irruptions with opportunistic feeding. I predicted the community of arthropods in the diet of P. kuhlii bats will vary in space and time. Furthermore, that the diet of the bats will comprise agricultural pest species. I expected that cotton pests will be found in the diet of the bats and will be positively correlated to their abundance in the cotton fields. Additionally, I anticipated that the bats dietary niche breadth will narrow as a function of increasing dominate pest species found in the diets. IV I located roosts of P. kuhlii bats near cotton fields in Emek-Hefer, Israel. I collected feces from the roosts throughout the cotton season (May - October 2016), and applied a molecular method, eDNA Metabarcoding, to process 133 fecal samples and identify taxa in the diet of P. kuhlii. I recovered 145 molecular operational taxonomic units (richness of prey) and 621 prey items (frequencies of prey) in the diet of P. kuhlii bats. I assigned 67% of the prey items to species or genus. The diet of the bats varied across the sampling season and showed disparities between sampling roosts. Lepidopterans and Dipterans emerged as dominate prey orders. Twenty-five agricultural pest species (32% of the total prey items), which target various agricultural crops, were found in the diet. Furthermore, potential disease vectors and nuisance arthropod pests were also identified in the diet. Yet, I found relatively low intraguild predation on arthropod natural enemies. Pink bollworm (Pectinophora gossypiella), a major cotton pest, showed the highest frequency occurrence of all prey taxa in the diet of P. kuhlii. It was found in diet at all sampling roosts, regardless of distance to cotton fields, and showed positive correlation with proxies of its abundances in cotton fields. This suggests that P. kuhlii consume Pink bollworms with opportunistic feeding. Additionally, the bats dietary niche breadth narrowed with the increasing frequency occurrences of Pink bollworms in the diet. My study emphasis the synanthropic trophic niche of P. kuhlii bats, highlights their ecosystem services and suggests that they function as holistic natural enemies of various deleterious arthropods in anthropogenic habitats. My findings especially demonstrate their potential for CBC programs to suppress cotton pests. The results possibly signify trophic interactions that occur across the wide-ranging distribution of P. kuhlii, with significant implications to economic concern that are still underappreciated. Further research directions should include quantifying the actual services of P. kuhlii, followed by attempts to preserve, enhance and communicate its contribution to pest suppression and sustainable agroecosystems. V ACKNOWLEDGMENTS I would like to express my sincere gratitude towards my supervisors Prof. Carmi Korine and Dr. Shirli Bar David, for giving me the opportunity to take part in this fascinating and fulfilling study. For always being supportive, patient and providing me the professional guidance I needed. For letting me express myself throughout the research, share my ideas freely and making my MSc experience one that I will remember positively. I want to express my appreciation to Prof. Thomas Gilbert from the University of Copenhagen (CGG: Center for GeoGenetics) for his willingness to collaborate. My extreme gratitude goes to Dr. Kristine Bohmann (CGG) for being a spectacular mentor, for her encouragement, guidance and professionality that had great contribution to my study. I am ever grateful to Martin Nielsen (CGG) for being supportive, coaching me in the laboratory and helping me complete the final steps of the molecular process. I thank Christina Lynggaard (CGG) for reassuring me during the lab work. I salute the farmers and cotton pest scouts for supporting the study in various ways. Practically, Haggai Medini from 'Israel Seeds' for his enthusiasm, commitment to the project and his innovate perspective on integrating bats in cotton pest management. Additionally, I want to thank Ariela Niv and Michael Axelrod from the Israel Cotton Board for their contribution to the study. I thank Giora Shoham and Nimord Shai and for sharing their insights and data on cotton pests and pesticide sprays with me. I am grateful to my dear friends Irene Stevens and Efrat Dener for always willing to help and give their advice. Additionally, I want to express thanks to Stav Livne for her valuable suggestions for the statistical analysis. I want to thank my lab members for being supportive and encouraging. I want to thank my friends that helped me with the bat roost surveys. My greatest gratitude goes to my family Pini, Tali, Dan and Ron Cohen and grandmother Nomi Levy for letting me follow me ambitions and being kind and encouraging throughout the way. Finally, I want to thank the bats for being such majestic and fascinating creatures that benefit us in tremendous ways. VI My research was funded by Israeli Ministry of Agriculture and Rural Development. My work was supported through a scholarship of the Albert Katz International School for Desert Studies Foundation. VII TABLE OF CONTENTS Abstract……………………………………………… ....... ………………..…………..……….II Acknowledgments……………………………………… ...... …….………………....…………V Table of Contents………………...……………………… ... …….…….………..………...…VII Table of Figures…………………………………… .......................................... …..………….IX Table of Tables…………………………………...………… .......... ….…….….……................X 1. Introduction……………………………………………… ...... ……….…………...…………1 1.1 Agroecology and Urban Ecology……………………………………………………..………1 1.2 Ecosystem Services and Biological Control……………………….…………..….………... .2 1.3 Conservation Biological Control……………………………..……...…………….…............2 1.4 The Diet of Insectivorous Bats………………………………….…………..….….…............4 1.5 Insectivorous Bats as Natural Enemies………………………….…………….…….………..9 2. Hypothesis and Predictions………………………………..………...……...….. ....…..…...12 3. Methods and Materials……………………………………….………... .... ….………….....13 3.1 Sampling Procedure……………………………………………………………...………… 13 3.2 Molecular Diet Analysis……………………………………………….………….....….…..16 3.3 Statistical Analysis and Data Visualization…………………………….…...……...……… 29 4. Results………………………………………...……………………….….………..….……. 34 4.1 Fecal Source…...……...……………………...……………………….….………..….……. 34 4.2 Efficiency of the Molecular Diet Analysis……....…………...……….….………..….……. 34 4.3 Spatio-temporal Variation in the Diet of P. kuhlii……......………...……………..….……. 37 4.4 Orders, Richness and Families of Arthropods in the Diet of P. kuhlii ……..……..….……. 41 4.5 Pest Species in the Diet of P. kuhlii…………..……………………………..……..….……. 45 4.6 Similarities in the Diet of P. kuhlii…..…………………………….…………………..……. 50 5. Disscusion………….…………………………………………………….………..…….…... 53 5.1 Metabarcoding the Diet of P. kuhlii……………………………………..…………..…..…..53 5.2 Spatial-temporal Trends in the Diet of P. kuhlii……………….….…………………...……..55 VIII 5.3 The Trophic Niche of P. kuhlii…………………………………………..........……......……58 5.4 Pipistrellus kuhlii in Conservation Biological Control…………….……...……….……..…60 6. Conclusions………..…………………………………………………….…………..……….66