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Resolving the Role of Jellyfish in Marine Food Webs

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Resolving the role of jellyfish in marine food webs Philip Lamb A thesis submitted for the degree of Doctor of Philosophy University of East Anglia School of Biological Sciences Submission Date: September 2018 This copy of the thesis has been supplied on condition that anyone who consults it is understood to recognise that its copyright rests with the author and that use of any information derived therefrom must be in accordance with current UK Copyright Law. In addition, any quotation or extract must include full attribution. Abstract Jellyfish populations in the Irish Sea have been increasing. This has caused a variety of economic problems, such as the destruction of aquaculture installations, and new opportunities, such as the establishment of a jellyfish fishery. However, interactions between jellyfish and other biota in the ecosystem is poorly characterised and ecological consequences of an increasing jellyfish population remains unknown. Molecular gut content analysis methodologies were developed to address this data gap. Cnidarian specific primers were developed and showed using more than 2500 stomachs that, during February and March, moon and mauve-stinger jellyfish were consumed by common fish species including herring, whiting, and lesser-spotted dogfish. Revisiting the ecosystem in October with 375 additional samples, the primers indicated jellyfish predation varied temporally: small jellyfish were still targeted by mackerel, however moon jellyfish adults were not preyed upon. To understand the context in which jellyfish consumption occurred a high throughput sequencing (HTS) approach using two universal primers was developed. A meta-analysis of HTS studies suggested results contained a quantitative signal, and the methodology could be used to move beyond a presence/absence approach. Using 188 samples from nine fish species, it was shown that jellyfish were consumed as part of a generalised diet during summer months. Finally, the approaches used to model jellyfish in the ecosystem model Ecopath with Ecosim (EwE) were reviewed. Jellyfish were included more frequently over time, however approaches remained relatively crude in the absence of high quality data in many ecosystems. Together, these approaches have gone some way towards addressing the data gap: jellyfish interactions with other biota have been recorded, and new approaches for studying these interactions have been developed. This has established a baseline for novel research opportunities such as mechanistic modelling of jellyfish, exploration of quantitative HTS approaches, and the generation of dietary time-series data to be conducted. 1 Acknowledgements I would first like to thank my primary supervisor Martin, and the rest of my supervisory team: Ewan, John, Richard, and Simon. I really appreciate the chance you took by taking me on as your PhD student, and the many hours you invested overseeing my research and my development as a scientist. I am also grateful for the cups of tea, or pints of beer, where you checked on my wellbeing in addition to the progress of the project. Next I would like to thank everyone at Cefas who has helped me during the course of this project. Whether that be providing technical guidance, attending my presentations, gathering samples, or assisting me while on board the Cefas Endeavour. I would like to thank Manuel Nicolaus for allowing me to participate on the CSEND research cruise. I would also like to thank Ciaran O’Donnell (Marine Institute), Ben Hatton, and Joanne Smith for gathering samples for me. Special thanks must go to Jeroen van der Kooij for his involvement in the project: granting me a berth on the research cruise, introducing me to colleagues to help source more samples, sharing data, proof reading manuscripts, and most importantly tolerating my incessant talk of rugby while at sea. I am also taking this opportunity to thank everyone at EnvEast, not only for funding my PhD but also helping me through the (surprisingly large amount) of paper work associated with the PhD. A big thank you must go to my family. You have always believed in my potential as a scientist, and although your support has been around long before the PhD (and hopefully long after!) I appreciate the opportunities and support you have given me over the years. Finally, thanks must go to Claire: I am so very grateful to you for listening to my woes when I was despairing over various aspects of the PhD, generally being a lovely human being, and making many loaves of delicious banana bread over the course of the PhD. 2 Author contributions Two chapters have been published, one chapter is currently under review. The remaining two chapters are in prep. Detailed below are author contributions. Chapter Two Lamb, P. D., Hunter, E., Pinnegar, J. K., Creer, S., Davies, R. G. & Taylor, M. I. 2017 Jellyfish on the menu: mtDNA assay reveals scyphozoan predation in the Irish Sea. Royal Society Open Science 4, 171421. (doi:10.1098/rsos.171421) M.I.T., E.H. and J.K.P. designed the study. E.H. participated in sample collection. P.D.L. conducted molecular lab work, data analysis, and wrote the manuscript. S.C., E.H., J.K.P., R.G.D. and M.I.T. contributed to writing and manuscript revision. Chapter Three Lamb, P. D., Hunter, E., Pinnegar, J. K., Creer, S., Davies, R. G. & Taylor, M. I. Under Review,Cryptic diets of forage fish: jellyfish consumption observed in the Celtic Sea and Western English Channel. Journal of Fish Biology. M.I.T., E.H. and J.K.P. originally generated the idea for the study. P.D.L., J.K.P. and J.V.D.K collected samples. P.D.L conducted wet and molecular lab work, analysis, and wrote the first draft. E.H., J.V.D.K., J.K.P. and M.I.T. contributed to manuscript revision. Chapter Four Lamb, P. D., Hunter, E., Pinnegar, J. K., Creer, S., Davies, R. G. & Taylor, M. I., 2018 (In press) How quantitative is metabarcoding: A meta-analytical approach, Molecular Ecology, 2018, (In press), (doi: 10.1111/mec.14920) 3 P.D.L conceived the study, conducted review and meta-analysis, and wrote the first draft of the manuscript. The supervisory team (S.C., E.H., J.K.P., R.G.D. and M.I.T.) critiqued and commented on the analyses and edited the manuscript. Chapter Five Lamb, P. D., Hunter, E., Pinnegar, J. K., Creer, S., Davies, R. G. & Taylor, M. I., In Prep, Putting jellyfish predation in perspective: jellyfishes’ importance in fish diets revealed by DNA metabarcoding. P.D.L, and the entire supervisory team contributed to the design of the study. Data collection was carried out by P.D.L, in addition to samples provided by Ciaran O’Donnell (Marine Institute), Ben Hatton (Cefas), and Joanne Smith (Cefas). Primer design, DNA extraction, 1st round PCR, and cleaning was conducted by P.D.L. 2nd round PCR and sequencing was conducted by Sheffield diagnostic genetics service. Bioinformatics, data analysis, and first draft of manuscript was written by P.D.L. The supervisory team contributed to manuscript revision. Chapter Five Lamb, P. D., Hunter, E., Pinnegar, J. K., Creer, S., Davies, R. G. & Taylor, M. I., In Prep, Tracking trends in the implementation of jellyfish in 30+ years of Ecopath with Ecosim models. P.D.L, J.K.P, and M.I.T. conceived the study. P.D.L collected data, conducted data analysis, and wrote the first manuscript. The supervisory team (S.C., E.H., J.K.P., R.G.D. and M.I.T.) critiqued and commented on the analyses and edited the manuscript. 4 Table of Contents Chapter 1: General introduction ................................................................................... 11 1.1 Our embattled seas ........................................................................................................ 11 1.2 Ecosystem approach to fisheries management ............................................................... 12 1.3 Jellyfish .......................................................................................................................... 13 1.3.1 Taxonomy & basic biology ............................................................................................. 13 1.3.2 Cnidarian jellyfish life history ........................................................................................ 15 1.3.3 Blooms & Jellyfish Population Increases ........................................................................ 16 1.3.4 Impacts of jellyfish ......................................................................................................... 18 1.3.5 Jellyfish as trophic dead-ends ........................................................................................ 18 1.4 Common dietary analysis methodologies ....................................................................... 19 1.4.1 Direct observation ......................................................................................................... 19 1.4.2 Morphological gut content analysis .............................................................................. 20 1.4.3 Fatty Acid analysis ......................................................................................................... 21 1.4.4 Stable Isotope Analysis .................................................................................................. 22 1.4.5 Antibody based approaches .......................................................................................... 23 1.4.6 DNA based approaches .................................................................................................. 24 1.5 Modelling approaches to fisheries management ............................................................
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