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Investigating Trophic Interactions Between Parasites and Their Marine Fish Hosts Using Stable Isotope Analysis

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Investigating Trophic Interactions Between Parasites and Their Marine Fish Hosts Using Stable Isotope Analysis INVESTIGATING TROPHIC INTERACTIONS BETWEEN PARASITES AND THEIR MARINE FISH HOSTS USING STABLE ISOTOPE ANALYSIS Mark Jonathan Weston SUBMITTED TO THE UNIVERSITY OF CAPE TOWN In fulfillment of the requirements for the degree of MASTER OF SCIENCE in the Faculty of Science, Department of Biological Sciences University of Cape Town September 2017 Supervisors: Dr. Cecile C. Reed: Department of Biological Sciences, University of Cape Town Dr. Carl D. van der Lingen: Fisheries Research and Development, Branch Fisheries Management, Department of Agriculture, Forestry and Fisheries, Cape Town, South Africa Marine Research Institute and Department of Biological Sciences, University of Cape Town The copyright of this thesis vests in the author. No quotation from it or information derived from it is to be published without full acknowledgement of the source. The thesis is to be used for private study or non- commercial research purposes only. Published by the University of Cape Town (UCT) in terms of the non-exclusive license granted to UCT by the author. University of Cape Town The copyright of this dissertation vests in the author. No quotation from it or information derived from it is to be published without full acknowledgement of the source. This dissertation is to be used for private study or non-commercial research purposes only. Published by the University of Cape Town in terms of the non- exclusive license granted to the University of Cape Town by the author. ii Declaration I, Mark Jonathan Weston, hereby declare that the work on which this dissertation is based is my original work (except where acknowledgements indicate otherwise) and that neither the whole work nor any part of it has been, is being, or is to be submitted for another degree in this or any other university I empower the university to reproduce for the purpose of research either the whole or any portion of the contents in any manner whatsoever. Signature: Signature Removed Date: 4th September 2017 iii Abstract Parasitism is accepted as being an essential driver in the organization of biological communities. However, although there are estimated to be more parasitic than free-living organisms, parasites have been largely neglected from ecological studies and we have a relatively limited understanding of their trophic ecology. Hence, in order to incorporate parasites into food-web models and ecological studies, basic trophic interactions between parasites and their hosts need to be assessed. Here, I investigated host-parasite interactions using stable isotope analyses on a broad range of marine fish hosts and their associated copepod and monogenean gill parasites. The study also provides insight into the gill parasite diversity of a number of host species from South African marine waters. Seventeen species of fish hosts, ranging from lower to upper trophic levels, were collected from South African waters in 2015 and 2016 during surveys conducted by the Department of Agriculture, Forestry and Fisheries from South African waters. These host species were; Thunnus albacares, Thunnus maccoyii, Thunnus alalunga, Thunnus obesus, Isurus oxyrinchus, Prionace glauca, Xiphius gladius, Brama brama, Thyrsites atun, Seriola lalandi, Sarda sarda, Genypterus capensis, Merluccius paradoxus, Merluccius capensis, Lampanyctodes hectoris, Sardinops sagax and Trachurus capensis. The head region, gills and operculae from a total of 1513 fish were examined and any ectoparasites removed, identified down to the lowest taxonomic level possible, and counted. A total of 32 parasite taxa, comprising 20 copepods and 12 monogenean species, were recorded. Two new host records and 15 new geographic records for South Africa were catalogued. The new host records are Mazocraes sp. infecting T. atun, and Caligus dakari infecting T. capensis. The new locality records consist of Euryphorus brachypterus recovered from T. alalunga and T. obesus, Pseudocycnus appendiculatus recovered from T. albacares, T. alalunga and T. obesus, Hexostoma sp. recovered from T. albacares and T. obesus, Nasicola klawei recovered from T. albacares and T. obesus, Tristoma iv adcoccineum recovered from X. gladius, Eobrachiella elegans and two species from the genus Parabrachiella recovered from S. lalandi and Anthocotyle merlucci recovered from M. paradoxus and M. capensis. These new records have substantially contributed to the known parasite biodiversity within the South African marine environment. Host-parasite interactions between 15 species of fish host and their copepod and monogenean gill parasites were investigated by means of stable isotope analysis. Host white muscle tissue, host gill tissue and parasite samples were analysed for their carbon and nitrogen isotopic signatures. Results indicated that δ15N is tissue-specific, with host white muscle tissue showing significantly greater enrichment in 15N compared to host gill tissue (n =60; Z=5.66843; p<0.00001), and as gill tissue is what the parasites are presumably feeding on, host gill tissue was therefore selected as the most appropriate proxy. Comparisons of the δ15N of the parasites and their associated host gill indicated that gill parasites in general are significantly enriched in 15N compared to their associated host gill tissue (n=144; Z= 9.767249; p<0.00001), and that copepods show a significantly higher enrichment compared to monogeneans (U=987; ncopepods=117; nmonogeneans=28; p=0.001121). Further analysis of the effect of the diet and feeding mode on the trophic fractionation of δ15N within the monogeneans showed that tissue-scraping monopisthocotyleans are significantly more enriched in 15N compared to blood-feeding polyopisthocotyleans (U=22.00; nmonopisthocotyleans=5; npolyopisthocotyleans=23; p=0.035776). A lack of definitive knowledge about the feeding modes used by the various copepod gill parasites precluded similar analysis for this group. At a species specific level, 13 out of 22 host-parasite interactions examined showed an enrichment of 15N in the parasites compared to their associated host gill tissue with the majority of these comprising copepod-host interactions. A comparison between the δ15N of the parasites and the estimated δ15N of host blood resulted in 11 out of 18 host-parasite interactions showing significant enrichment in 15N, of which 10 were copepod-host interactions. Mathematical corrections of δ13C for samples with high C:N ratios appeared v successful for the majority of samples analysed. However some parasites showed very high C:N ratios, indicative of high lipid content, and the lack of lipid-extracted samples with which to compare the mathematically corrected samples prohibited any further biological inferences from being drawn and highlighting the necessity for the manual lipid extraction of such samples. The present study has indicated a general enrichment in 15N of parasites compared to their host gill and blood tissue. However there are variations in trophic fractionation according to parasite type, diet and feeding mode. Additionally, enrichment in 15N of parasites appeared to be linked to the relative trophic level of their host, being higher for lower trophic level hosts and lower for higher trophic level hosts. This supports the hypothesis that trophic fractionation if nitrogen isotopes in food-webs is not linearly related to trophic level. This study provides further insight into the trophic interactions between parasites and their hosts which lends itself toward a more comprehensive understanding of trophic interactions occurring within ecological communities. vi Table of Contents Declaration ..................................................................................................................................... iii Abstract .......................................................................................................................................... iv Table of Contents .......................................................................................................................... vii List of Tables .................................................................................................................................. x List of Figures ............................................................................................................................... xii Acknowledgements ...................................................................................................................... xvi Chapter 1: Introduction ................................................................................................................... 1 1.1- Food-webs ............................................................................................................................ 1 1.2- Parasitism ............................................................................................................................. 5 1.3- Incorporating Parasites into Food-Webs .............................................................................. 9 1.4- Methods for Understanding Trophic Interactions .............................................................. 15 1.4.1- Stable Isotope Analysis ............................................................................................... 16 1.4.2- Nitrogen Isotopes......................................................................................................... 17 1.4.3- Carbon Isotopes ........................................................................................................... 19 1.4.4- Using Stable
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