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Ecological Consequences of Non-Native Parasites for Native UK Fishes

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Ecological Consequences of Non-Native Parasites for Native UK Fishes Ecological consequences of non-native parasites for native UK fishes Josephine Pegg This thesis has been submitted in partial fulfilment of the requirements of the degree of Doctor of Philosophy Bournemouth University October 2015 I This copy of the thesis has been supplied on condition that anyone who consults it is understood to recognise that its copyright rests with its author and due acknowledgement must always be made of the use of any material contained in, or derived from, this thesis. II Josephine Pegg Ecological consequences of non-native parasites for native UK fishes Abstract Introductions of non-native species can result in the release of their parasites. Although the majority of parasites are lost during the introduction process, those that do get released can spill over to native species and potentially result in pathological, physiological and ecological impacts. Whilst it is increasingly recognised that native parasites can play important ecological roles, the ecological consequences of non- native parasites remain unclear. Consequently, through study of three host-parasite models, this research investigated the ecological consequences of non-native parasites in UK freshwater fish communities through assessment of their effects on hosts (individuals to populations), and on food web structure. The three non-native parasite: host systems were Ergasilus briani and roach Rutilus rutilus and common bream Abramis brama, Bothriocephalus acheilognathi and common carp Cyprinus carpio, and Anguillicoides crassus and the European eel Anguilla anguilla. These parasites were chosen as they reflect a range of life cycle complexity in parasites. The pathology of each parasite was identified using histology, with E. briani having substantial effects on host gill structure, B. acheilognathi impacted the intestinal structure of their hosts, and A. crassus substantially altered the structure and functioning of the host swimbladder. Whilst infections of E. briani and A. crassus had minimal effects on the body size, growth and condition of their hosts, chronic infections of B. acheilognathi did impact the growth and condition of C. carpio when measured over a 12 month period. III Differences in the trophic ecology of the infected and uninfected components of the host populations were identified using stable isotope analysis and associated metrics, and revealed considerable differences in the trophic niche breadth of the infected and uninfected fish. In the component infected with E. briani, their trophic niche was constricted, indicating diet specialisation and a shift to feeding on less motile food items. For C. carpio infected with B. acheilognathi, their niche shifted away that of uninfected fish as they fed on higher proportions of planktonic prey resources. Whilst differences in the trophic ecology of infected and uninfected A. anguilla were apparent, this related to differences in their functional morphology that enabled the infected eels to prey upon greater proportions of fish paratenic hosts that resulted in their higher rates of infection. The wider ecological consequences of the introduced parasite were then investigated using topological and weighted food webs. The topological webs revealed that lifecycle and host specificity were important factors in how each parasite impacted the food web metrics, but in all cases the combined effects of including native parasites in food web structure exceeded that of adding the non-native parasite. However, weighting these food webs by using the dietary data outlined above revealed that these infections were predicted to have greater consequences than predicted topologically, and enabled scenarios of differing parasite prevalence and environmental change to be tested on food web metrics. These revealed that under increasing nutrient enrichment, infected individuals generally benefit via having access to greater food resources, a counter-intuitive resulting from increased algal biomass. IV Thus, this research revealed that introductions of non-native parasites have pathological and ecological consequences for their host populations that have measurable effects at the food web level. These outputs have important implications for the management of non-native parasites and their free-living hosts, and should be incorporated into risk-management and policy frameworks. V Table of Contents 1. Introduction .......................................................................................... 1 1.1 Introductions of non-native fish ..................................................................... 1 1.2 Arrival of parasites with introduced free-living species ................................ 3 1.3 How many non-native parasites arrive with free-living non-native hosts? ... 4 1.4 Infections by non-native parasites in their new range ................................... 6 1.5 Parasites in infectious food webs ................................................................... 7 1.6 Parasites affect ecosystem structure............................................................. 10 1.7 Parasites: consequences from individual hosts to ecosystems ..................... 11 1.8 Focal Parasites ............................................................................................. 12 1.9 Definitions of terminology ........................................................................... 18 1.10 Research aim and objectives ........................................................................ 20 1.11 Thesis structure ............................................................................................ 21 2. Consistent patterns of trophic niche specialisation in host populations infected with a non-native parasite .................................................... 23 2.1 Abstract ........................................................................................................ 23 2.2 Introduction .................................................................................................. 24 2.3 Materials and Methods ................................................................................. 26 2.3.1 Sample collection and initial data collection ............................................... 26 2.3.2 Histopathology ............................................................................................ 30 2.3.3 Data analyses ............................................................................................... 31 2.3.4 Statistical analyses ....................................................................................... 32 2.4 Results .......................................................................................................... 33 2.4.1 Parasite prevalence and abundance, and effect on fish length and weight .. 33 VI 2.4.2 Histopathology ............................................................................................ 36 2.4.3 Stable isotope metrics .................................................................................. 39 2.5 Discussion .................................................................................................... 45 3. Temporal changes in growth, condition and trophic niche in juvenile Cyprinus carpio infected with a non-native parasite .............................. 50 3.1 Abstract ........................................................................................................ 51 3.2 Introduction .................................................................................................. 51 3.3 Methods........................................................................................................ 54 3.3.1 Sample collection and initial data collection ............................................... 54 3.3.2 Histopathology ............................................................................................ 57 3.3.3 Data analyses ............................................................................................... 57 3.3.4 Statistical analyses ....................................................................................... 59 3.4 Results .......................................................................................................... 59 3.4.1 Parasite prevalence and abundance ............................................................. 59 3.4.2 Histopathology ............................................................................................ 62 3.4.3 Effect of infection on fish length and condition .......................................... 64 3.4.4 Stable isotope metrics .................................................................................. 66 3.5 Discussion .................................................................................................... 71 4. Head morphology and piscivory of European eels, Anguilla anguilla, predict their probability of infection by the invasive parasite parasitic nematode Anguillicoloides crassus .......................................................................... 75 4.1 Abstract ........................................................................................................ 76 4.2 Introduction .................................................................................................. 77 VII 4.3 Methods........................................................................................................ 80 4.3.1 Sample collection and initial data collection ............................................... 80 4.3.2 Data analysis ...............................................................................................
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