Ecological consequences of indigenous and non-indigenous freshwater fish parasites.

Abstract

Parasites can have considerable consequences for their freshwater fish hosts, irrespective of whether they are intermediate or final hosts. The ecological consequences of infection arise from processes including parasite manipulation, where the parasite manipulates the host to increase their chance of transmission to the next host in the lifecycle, and parasite-mediated competition, where a consequence of infection is an alteration in the symmetry of competition between hosts and their uninfected conspecifics, or with other species. Whilst there is a great deal of existing knowledge on some of these consequences, there also remain some considerable knowledge gaps. This research covered the role of parasite exposure and water temperature on infection consequences, the foraging responses of fishes to intermediate hosts of the fish parasite Pomphorhynchus laevis that has an indigenous and non-indigenous range in Great Britain, the ecological consequences of this parasite for some freshwater fishes across these ranges, the issue of ‘enemy release’ and ‘parasite acquisition’ in introduced freshwater fishes, and the ecological consequences of infection by some native parasites for native freshwater fish. When the freshwater fish chub (Squalius cephalus) was exposed to different levels of intermediate hosts (Gammarus pulex) of P. laevis under two water temperature treatments, ambient and warmed, it revealed this interaction had considerable consequences for both parasite prevalence and the infection parameters. Whilst parasite prevalence was substantially higher at the elevated temperature, where infections did develop at lower temperatures, they were associated with fewer but larger parasites resulting in significantly higher parasite burdens, indicating complex consequences for host-parasite relationships under conditions of warming. Studies into parasite manipulation have frequently used the P. laevis: G. pulex parasite-intermediate host system for investigating how infections can result in behavioural modifications to the host that then results in their elevated risk of being predated by a fish. Here, comparative behavioural functional response experiments were used to test differences in the consumption rates of three fishes exposed to either uninfected or infected G. pulex, testing the hypothesis that the consumption rate of infected G. pulex would be significantly higher. The Type II functional response curves indicated that the results of the experiments were contrary to this hypothesis, with subsequent behavioural and foraging experiments also supporting these results. These counter-intuitive outcomes were also contrary to most other studies that suggested a parasite would manipulate its intermediate host in a way that promotes its transmission to a final host and facilitating the continuation of its life cycle. The reasons for these outputs were discussed as likely to relate to different selection pressures in this host-parasite system, given this is a generalist parasite with a wide range of potential fish final hosts. This was revealed by studies on this parasite from four fish species from five rivers that demonstrated high parasite prevalence in all species studied and suggested that small-bodied fishes, such as bullhead Cottus gobio, might play important roles in the P. laevis lifecycle. These prevalences, and the pathological consequences of the P. laevis infections, were also consistent across their indigenous and non-indigenous range, suggesting parasite origin had minimal consequences on their virulence and on the susceptibility of hosts to infection. That parasite origin often has minimal ecological consequences for their ecological impacts was reinforced by work on the ‘enemy release hypothesis’ in non-native fish in England and Wales. This revealed very few non-native parasites had been introduced with their non-native fish hosts. Those that had been introduced tended to be specialist parasites with direct lifecycles that had little opportunity to be transmitted to native fishes. Instead, the acquisition of native parasites by the non-native fishes was frequently observed, leading to potential concerns these fish would act as reservoir hosts and spill-back the parasites to the native fishes. Given the low probability of parasite introduction, the ecological consequences of three native parasites with complex lifecycles were then tested on three native fishes, and revealed consistent patterns of trophic niche divergence between infected and uninfected population sub-groups. Whilst the actual mechanism underpinning this, such as parasite-mediated competition, could not be tested, these results did reveal that the consequences of infection can be far-reaching for hosts and can be measured through a variety of methodologies. In summary, the research provided some comprehensive insights into many aspects of the pathological and ecological consequences of infection for some freshwater fishes from native/ non-native and indigenous/ non-indigenous parasites. In doing so, it has raised a series of new questions and hypotheses for further investigation, with the host-parasite systems used here capable of answering these.