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Untangling Molecular Food Webs of Non-Native Invertebrates and Their Communities

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Untangling Molecular Food Webs of Non-Native Invertebrates and Their Communities Untangling molecular food webs of non-native invertebrates and their communities. Marco Benucci Department of Biological and Marine Sciences University of Hull A thesis submitted for the degree of Doctor of Philosophy January 2020 “So it isn’t the original building?” I had asked my Japanese guide. “But yes, of course it is.” he insisted, rather surprised at my question. “But it’s burnt down?” “Yes.” “Twice.” “Many times.” “And rebuilt.” “Of course. It is an important and historic building.” “With completely new materials.” “But of course. It was burnt down.” “So how can it be the same building?” “It is always the same building.” I had to admit to myself that this was in fact a perfectly rational point of view, it merely started from an unexpected premise. Douglas Adams - “Last Chance to See” (1990) i Abstract Invasive non-native species (INNS) are one of the main drivers of biodiversity loss globally, however to what extent INNS predators modify and utilise the invaded communities is still debated. This is particularly the case for arthropod INNS whose trophic interaction and predatory impact can be challenging to detect and describe. The application of DNA-based analysis, such as DNA metabarcoding, to the study of trophic interactions is often referred to as “MATI” (Molecular Analysis of Trophic Interactions). This approach has great potential in terms of increased sensitivity, higher resolution of prey identification and application to large-scale field studies, compared to previously established methods. This thesis focuses on describing trophic interactions in three non- native arthropod predators using this approach, with a key focus on intraguild predation (IGP), which has been shown to speed up invasion and facilitate establishment of invaders. In the first data chapter I focussed on the invasive amphipod, Dikerogammarus villosus, commonly known as “killer shrimp” to prove the concept that detection of prey DNA is possible in a controlled feeding experiment, and at a small field scale. From this proof of concept, I increased the scale of the field study by separately investigating the trophic interactions of three INNS: 1) D. villosus (Amphipoda: Gammaridae), 2) Harmonia axyridis (Coleoptera: Coccinellidae), and 3) the newly detected non-native Crangonyx floridanus (Amphipoda: Crangonyctidae). Data was collected for all species from UK sites across two seasons. The overarching goals were to investigate the broad trophic interactions of the target INNS across space and time, with a focus on detecting and understanding the importance of IGP in each target INNS. I predicted that high levels of IGP could be detected in all three target INNS. Firstly, I demonstrated that the method could detect prey species in both controlled and in field conditions, but detection success varied between prey taxa. I detected only low levels of IGP in D. villosus compared to a native amphipod, G. zaddachi, and found no evidence of IGP in H. axyridis, despite these species’ reputations as important IG predators. I relate this to the availability of IG prey in the wider community. By contrast I detected high levels of reciprocal IGP between the newly detected C. floridanus and the established, non-native C. pseudogracilis. Interestingly, IGP was asymmetric, in favour of the new invader, which could ii facilitate its establishment by eliminating competition. Together, these results demonstrate the applicability and also the challenges of DNA metabarcoding to molecular trophic interactions of INNS to understand the extent of their interactions in the invaded communities. I provide novel insight into the predatory dynamics of the three target species and their impact on the invaded communities. iii Candidate Declaration All the work submitted in this thesis is my own, except when otherwise stated. Several people have collaborated during this thesis. Drew Constable (DC), Katie Lee (KL), Alex Austin (AA), Lynsey Harper (LH), Rosetta Blackman (RB), Graham Sellers (GS), Lori Lawson-Handley (LLH), and Bernd Haenfling (BH). Lori Lawson-Handley (LLH) and Bernd Haenfling (BH) have been involved with all the work. Chapter 2: RB helped in the designing of the feeding arenas, KL helped on the fieldwork, RB and LH helped in the creation of the curated databases. Chapter 3: KL helped on fieldwork, morphological indentification of kick samples and on DNA amplification. RB and LH helped for the creation of databases Chapter 4: GS and AA helped on fieldwork Chapter 5: DC helped in providing extra samples, KL helped on fieldwork, GS helped in tissue extraction. RB and LH helped for the creation of databases. Marco Benucci, January 2020 iv Acknowledgements First of all I would like to thanks my suprevisors Dr. Lori Lawson-Handley and Dr. Bernd Haenfling for your support, contibrutions and suggestions during the whole project. A particular thank goes to Lori for your incredible help and support during these years, during both the positive and the negative times. Your enthusiasm, encouragements and open mind to networking have been a driving force throughout the whole PhD. A special thanks to Helen Roy, Peter Brown and Rachel Farrow for their help and suggestions on the Harmonia axyridis chapter. Thanks to Drew Constable for the help given in the identification of Crangonyx floridanus. A massive thanks to my ever-supporting family. Thanks for all your constant encouragement and kind words that you managed to transmit all the way from Italy. Thank you, I wouldn’t have made it without you. To my lab mates (past and present), thank you all. Rosetta Blackmann, Lynsey Harper, Graham Sellers, Alex Austin, Rob Donnelly, Jianlong Li, Cristina Di Muri, Helen Kimbell, Peter Shum, Nathan Griffith, and Rob Jaques; thank you all for sharing this time with me. Thanks for your help on fieldwork, for your recommendations in the lab and also for the unforgettable laughs we had. I found a group of friends inside this group of colleagues that made the time fly by and the heavier moments to feel lighter. Thanks to the whole EvoHull group, a place of discussion and improvement. The diverse knowledge contained in the group, and the routine sharing of those, made every lab chat a time of open discussion and debate. Thanks to my partner Barbara, your constant help during this last year of writing this thesis has been enormous. You allowed me to achieve this submission with your encouragements and with the Sundays spent hiking. To all my D&D friends I found outside of the university, thank you for all the laughs and all the memories created. Thank you all. v Table of Contents Abstract ............................................................................................................... ii Candidate Declaration ....................................................................................... iv Acknowledgements ............................................................................................. v Table of Contents .............................................................................................. vi Chapter 1 - Introduction ...................................................................................... 1 1.1 Ecological Communities. ........................................................................... 1 1.2 INNS within communities. .......................................................................... 1 1.3 INNS within networks ................................................................................ 3 1.4 DNA metabarcoding .................................................................................. 6 1.4.1 environmental DNA ................................................................................ 6 1.5 Molecular Analysis of Trophic Interactions (MATI) .................................... 7 1.6 Aims and objectives ................................................................................... 8 1.7 Target species ........................................................................................... 8 1.8 Ethics ....................................................................................................... 16 1.9 Rationale of the thesis ............................................................................. 16 Chapter 2 - Detecting molecular trophic interactions of Dikerogammarus villosus in feeding experiments and field samples in the UK. ........................................ 19 2.1 Introduction .............................................................................................. 21 2.2 Methods ................................................................................................... 26 2.3 Results..................................................................................................... 34 2.4 Discussion ............................................................................................... 40 2.5 Conclusions ............................................................................................. 44 Chapter 3 - DNA metabarcoding of gut contents of invasive Dikerogammarus villosus reveals low levels of intraguild predation compared to a native amphipod, Gammarus zaddachi in the UK. ...................................................... 45 3.1 Introduction .............................................................................................. 47 3.2 Methods ................................................................................................... 52 3.3 Results....................................................................................................
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