The ecology of Neoechinorhynchus rutili (Acanthocephala) in Scottish freshwater lochs

1. The ecology of Neoechinorhynchus rutili (Acanthocephala) has been investigated in a Scottish population of brown trout (Salmo trutta) inhabiting a small highland loch, in Central region. The results have been compared with data from other hosts and localities. In addition, a complementary study on the ecology of Echinorhynchus truttae in brown trout was carried out at a reservoir in Lothian Region. 2. A review of the knowledge of the classification, morphology of developmental stages, life cycle, ecology and distribution and biochemistry and physiology of Neoechinorhynchus rutili was undertaken. 3. Examination of 1189 fish (11 species) from 8 Scottish regions and collation of available records indicated that Neoechinorhynchus rutili infects 8 species of freshwater fish (Esox lucius, Gasterosteus aculeatus, Perca fluviatilis, Phoxinus phoxinus, Salmo gairdneri, Salmo salar, Salmo trutta and Salvelinus alpinus) at 41 sites in 6 Scottish regions. These sites encompass a wide spectrum of aquatic environments in terms of size, water quality and faunal community structure. This wide distribution of Neoechinorhynchus rutili is explained through the multifarious habits of the definitive host species and possibly interactions with human, avian or insect factors. There is evidence for temporal stability of the infection at some of these sites. 4. The main field site for the examination of the ecology of Neoechinorhynchus rutili was Loch Maragan (Grid ref. NN 402278), Central Region. This small loch (surface area 7.3 ha, maximum depth 10.2 m, volume 153943 m3) lies at 472 m above sea level and had slightly acid water conditions (p.H. 6.44, October 1986.) Three species of fish (Anguilla anguilla, Phoxinus phoxinus and Salmo trutta) were found to inhabit the loch. In August 1987 the brown trout population size was estimated, by a simple mark and recapture technique, as 2641 (1 to 3 years olds) (Maximum value). 5. Two benthic faunal surveys, carried out in November 1986 and May 1987 respectively, did not reveal the species of invertebrate which was acting as intermediate host for Neoechinorhynchus rutili at Loch Maragan. 6. A total of 226, between 1 and 5 years old were caught at Loch Maragan over a 25 month period between July 1986 and August 1988 and examined for visceral and gut macroparasites. Minnows (n = 207) and alder flies (Sialis lutaria) (larvae and adults) were also examined. Sialis lutaria larvae were infected with Neoechinorhynchus rutili and unidentified trematode metacercaria. The minnows harboured Neoechinorhynchus rutili, Ligula intestinalis and Crepidostomum spp. The brown trout harboured Capillaria salvelini, Crepidostomum spp., Diphyllobothrium ditremum and D.dendriticum and Neoechinorhynchus rutili. The distributions of these parasitic infections amongst their hosts are described. 7. The collection of 4992 Neoechinorhynchus rutili from 226 brown trout, revealed the overdispersed nature of the infection (k = 0.7893), individual fish harbouring between 1 and 324 worms. The overall prevalence and mean intensity of infection were 87.6% and 21.5 respectively. Monthly prevalence values (of samples) never fell below 50%. Trout age, but not sex, influenced the infection parameters. 8. Neoechinorhynchus rutili exhibited a definite seasonal cycle of intensity and maturation in brown trout at Loch Maragan. Although recruitment apparently occurred throughout the year, worm intensitites, particularly of gravid females, peaked in summer when water temperatures and host feeding rates were maximal. Acanthor production occurred between March and November. In summer 1987 the Neoechinorhynchus rutili metapopulation (in trout aged 1 to 3 years) was estimated to be 36154, of which 5566 were gravid females. These females were estimated to have produced 1.6 x 108 shelled acanthors which represents a reproductive success rate of 3.5 x 10-3 % i.e. 1 in 38030 shelled acanthors becoming a reproductively active female in the next parasite generation. No evidence for density dependent effects upon worm fecundity were found. Similar seasonal patterns were found at other Scottish locations. 9. Neoechinorhynchus rutili was typically found in the ileas and rectal regions of the trout gut, but the distribution was dynamic with respect to season, worm sex, state of maturity and infection intensity. 10. No adverse effect upon the condition factor of brown trout in Loch Maragan could be attributed to the presence of Neoechinorhynchus rutili. 11. The diet of brown trout at Loch Maragan was analysed and Sialis lutaria larvae formed an important element, especially in spring. Larger trout were found to be piscivorous. 12. Acanthocephalan specimens found in the haemocoel of Sialis lutaria larvae collected from 2 Scottish sites (Loch Maragan and Loch Monzievaird) were identified, on the basis of their morphology, as the eoacanthocephalan Neoechinorhynchus rutili. 13. Sialis lutaria larvae were found to be infected with Neoechinorhynchus rutili at Loch Maragan and 3 other Scottish sites where fish were also infected (Bridge of Weir fish farm, Drumore Loch and Loch Monzievaird). The distribution of infection was typically overdispersed (k values ranged from 0.27 to 1.25). Overall prevalence values ranged from 4.2 to 40.7%. Infection parameters varied with insect size and season. 14. Establishment of Neoechinorhynchus rutili in experimental infections of rainbow trout (Salmo gairdneri) via feeding upon infected Sialis lutaria larvae was up to 33% successful. Experiments to infect ostracods (Herpetocypris reptans) and Sialis lutaria larvae via feeding with shelled acanthors were unsuccessful. 15. Postcyclic transmission of Neoechinorhynchus rutili occurred in the laboratory when rainbow trout were exposed to worms established in the three-spined stickleback (Gasterosteus aculeatus) hosts. The re-establishment rate was estimated as 92.8%. There is circumstantial evidence to suggest that this form of transmission occurs in natural populations in Scotland. 16. In the complementary study at Gladhouse Reservoir, 4 visceral and gut parasites were identified in the brown trout: Cystidicola farionis, Eustrongylides sp. (Nematoda), Eubothrium crassum (Cestoda) and Echinorhynchus truttae (Acanthocephala). Both E.crassum and Echinorhynchus truttae were overdispersed in their hosts and the overall prevalences and intensities of infection were 61.9% and 92.9% and 1.48 and 156.4 respectively. Echinorhynchus truttae exhibited a seasonal pattern of maturation, females releasing shelled acanthors in the summer months. This study also considered the logistics of carrying out scientific research in collaboration with members of the public