The occurrence and life history of Asymphylodora kubanicum (Platyhelminthes: Digenea: Monorchidae) in the Worcester-Birmingham canal, with special reference to the feeding habits of the definitive host, Rutilus rutilus

Two hundred roach and over 400 molluscs were examined over a one year period to investigate the occurrence and life history of Asymphylodora kubanicum in the Worcester-Birmingham canal. Larval stages, infective to the fish definitive host, were present in molluscs throughout the year but did not show a seasonal fluctuation in numbers. Parasites in the intestine of the roach showed a marked annual cycle of occurrence and maturation: low winter infection levels preceded a dramatic increase in infection during the spring and summer. Maturation of the parasite population was rapid during the spring and summer and in late summer and early autumn the parasites laid their eggs and subsequently died. The death of parasites after egg-laying resulted in the low winter infection level during which time little recruitment occurred.
Roach became infected mainly in their third year when molluscs become a dominant component of their diet. Thereafter the older fishes (<2+) are all equally susceptible to infection, but the larger (older) fishes become more heavily infected because of the greater consumption of molluscs per fish. The sex of the fish made no difference to infection with the parasite.     

The population biology of the acanthocephalan Pomphorhynchus laevis (Müller) in the River Avon

Regular samples of Gammarus pulex and dace Leuciscus leuciscus and occasional grayling Thymallus thymallus and chub L.cephalus were examined from the River Avon, Hampshire, for the presence of the acanthocephalan Pomphorhynchus leavis . The parasite only occurred in medium sized Gammarus due to lower probability of contact with small gammarids and stunted growth and selective mortality amongst older infected ones. No cycles in incidence or development of the parasite in G.pulex were observed. The parasite infected gammarids and grew in all months, and cystacanths were available throughout the year. Despite seasonal feeding activity and dietary preferences, fish fed on Gammarus and acquired infections in all months. Dispersion of P.laevis within the fish population was related to host feeding behaviour. No evidence of seasonal cycles in incidence or intensity of infection in fish was found, and observed monthly changes in the parasite population were related to changes in size structure of the host sample. In dace and grayling P.laevis grew little and matured only in summer, but in chub it grew and produced acanthors all year. The parasite population in fish appeared to be in a state of dynamic equilibrium and gain and loss of parasites took place throughout the year with the level of infection at any moment being determined primarily by the feeding behaviour of the host. This relationship between host diet, water temperature and parasite population size is discussed, and P.laevis in the R. Avon compared with other localities and other parasites.     

Host manipulation by Ligula intestinalis: a cause or consequence of parasite aggregation?

Previous investigations suggest that the infection of the cyprinid roach, Rutilus rutilus, with the larval plerocercoid forms of the cestode, Ligula intestinalis, creates behavioural and morphological changes in the fish host, potentially of adaptive significance to the parasite in promoting transmission to definitive avian hosts. Here we consider whether these behavioural changes are important in shaping the distribution of parasite individuals across the fish population. An examination of field data illustrates that fish infected with a single parasite were more scarce than expected under the negative binomial distribution, and in many months were more scarce than burdens of two, three or more, leading to a bimodal distribution of worm counts (peaks at 0 and >1). This scarcity of single-larval worm infections could be accounted for a priori by a predominance of multiple infection. However, experimental infections of roach gave no evidence for the establishment of multiple worms, even when the host was challenged with multiple intermediate crustacean hosts, each multiply infected. A second hypothesis assumes that host manipulation following an initial single infection leads to an increased probability of subsequent infection (thus creating a contagious distribution). If manipulated fish are more likely to encounter infected first-intermediate hosts (through microhabitat change, increased ingestion, or both), then host manipulation could act as a powerful cause of aggregation. A number of scenarios based on contagious distribution models of aggregation are explored, contrasted with alternative compound Poisson models, and compared with the empirical data on L. intestinalis aggregation in their roach intermediate hosts. Our results indicate that parasite-induced host manipulation in this system can function simultaneously as both a consequence and a cause of parasite aggregation. This mutual interaction between host manipulation and parasite aggregation points to a set of ecological interactions that are easily missed in most experimental studies of either phenomenon.     

The population biology of two species of eyefluke, Diplostomum gasterostei and Tylodelphys clavata, in perch

Incidence, intensity and frequency distributions of infections in perch, Perca fluviatilis , with the eyeflukes Tylodelphys clavata and Diplostomum gasterostei were studied in a lake at monthly intervals over a period of two years. T. clavata had appeared in the lake immediately prior to the study, and its levels of infection continued to rise throughout the period of investigation whereas those of D. gasterostei remained relatively steady. The main period of infection of fish by both species of parasites was late summer, but a second and minor infection took place in spring. In the first year after its introduction T. clavata exhibited a seasonal cycle in incidence and intensity of infection and disappeared from fish in summer, but in the second year this cycle was masked by increased variation in development times and lack of synchrony throughout the parasite population. It is concluded that T. clavata has a life span of one year or less and that the parasites die within the fish, mainly in summer. D. gasterostei in contrast has a life span of at least one year, and disappearance of the parasite from the population is probably due to death of some heavily infected fish, although it was not possible to determine if this was due directly to the presence of the parasite.     

The population biology of two species of eyefluke, Diplostomum spathaceum and Tylodelphys clavata, in roach and rudd

Infections of roach ( Rutilis rutilus ), and rudd ( Scardinius erythrophthalmus ), by the eyeflukes Diplostomun spathaceum and Tylodelphys clavata were studied in a lake over a three year period. T. clavata first appeared at the beginning of the study. Roach were heavily infected by both parasites, whereas the rudd contained very few specimens of either species. A small number of roach-rudd hybrids were also examined, and appeared to have a susceptibility intermediate between the parental types.
Levels of T. clavata in roach increased throughout the study. This parasite had a life span of a year or less in the fish, and was continuously lost from the population. This loss was balanced by a minor infection period in April/May and a major one extending from August until January. The fish continued to accumulate infections until they reached a size of about 130 mm, but thereafter intensity fluctuated about the level reached.
D. spathaceum infections similarly increased throughout the period of study, and there was a suggestion of a wave of infection in the spring. This parasite has a much longer life span, and levels of infection increased with fish size, only falling in the largest, and therefore oldest, hosts.
The major changes in the parasite populations in the roach were reflected, to a lesser extent, in the rudd. Both species were over-dispersed, but the data from roach was too heterogeneous to fit to any theoretical models, whereas that from the rudd was found to conform to a Negative Binomial distribution.     

Phenotypic modification of roach (Rutilus rutilus L.) infected with Ligula intestinalis L. (Cestoda: Pseudophyllidea).

In European freshwater, cyprinid fish may be heavily infected by plerocercoids of the pseudophyllidea cestode Ligula intestinalis (L.). During their development, these parasites grow rapidly to a large size in the fish's body cavity, characteristically distending the abdomen. In this study, the influence of this tapeworm on roach (Rutilus rutilus L.) morphology was analyzed. Forty-five infected and 45 uninfected roach were collected from the Lavernose-Lacasse gravel pit in Toulouse, south western France and examined for 40 morphological measurements to study phenotypic modification of the body and 14 bilateral characters for an analysis of asymmetry. Results indicate that the degree of bilateral asymmetry does not change between infected and uninfected roach, despite the strong host-morphological modifications such as deformation of the abdomen, fin displacements at the level of the tail, and sagging of the vertebral column. The intensity of abdominal distension and fish morphology changes depends on the total parasite biomass present. Differences were observed in morphology at different levels of infection, which relate to established effects of L. intestinalis on the physiology and behavior of intermediate hosts. These morphological changes induced by the parasite could increase trophic transmission to the definitive avian hosts.     

Changes in numbers and growth of Ligula intestinalis in the spottail shiner (Notropis hudsonius), and their roles in transmission

Eighteen species of fishes were collected during the open water (1985-1987) and winter seasons (1985-1986) from Dauphin Lake, Manitoba, Canada (51 degrees 17'N, 99 degrees 48'W) and examined for plerocercoids of Ligula intestinalis (L.). Plerocercoids were most prevalent (5.3%) in spottail shiners (Notropis hudsonius), the major fish host for Ligula in Dauphin Lake. Detailed analysis of the spottail shiner-Ligula host-parasite system revealed that the number of plerocercoids differed between years and among habitats but there was no statistically significant seasonal pattern; recruitment of new worms was highest in young fish and decreased with age, and infected spottails had reduced gonad development. Analysis of host and parasite growth revealed that the soma of male spottails infected with Ligula weighed more but had a reduced growth rate. Growth rate of females was unaffected by Ligula but somatic weight was slightly increased. This appears to be related to the greater metabolic stress on infected males. Based on increased mean somatic weight and skewness of the weight distribution for infected fish, we propose that infected spottails are subjected to size-selective mortality. Some of the contradictions in the literature may be attributed to underestimated prevalence due to increased numbers of spawning fish in the spring, mixed age-classes of Ligula in separate age-classes of fish, and differential effects on growth due to infection in male versus female hosts.     

Expression of gonadotropin subunits in roach (Rutilus rutilus, Cyprinidae) infected with plerocercoids of the tapeworm Ligula intestinalis (Cestoda)

Plerocercoids of the tapeworm Ligula intestinalis (Cestoda: Bothriocephalidea) have been reported to inhibit gametogenesis of their intermediate fish hosts. However, mechanistic studies are rare and the proximate cues leading to impaired reproduction still remain unknown. In the present study we investigated the effects of infection by L. intestinalis on reproductive parameters of roach (Rutilus rutilus, Cyprinidae), a common fish host of this parasite. Field studies on roach demonstrated that in both genders infection prevented gonad development. As revealed by quantitative PCR, infection was accompanied by essentially lower pituitary expression of follicle-stimulating hormone β-subunit (FSHβ) and luteinizing hormone β-subunit (LHβ) mRNA compared with uninfected roach, providing clear evidence for gonadotropin-insufficiency as the cause of arrested gametogenesis. Under controlled laboratory conditions infected roach showed lower mRNA levels of FSHβ but not of LHβ, despite histology revealing similar gonad stages as in uninfected conspecifics. These findings indicate the involvement of FSH rather than LH in mediating effects of infection early during gonad development in roach. Moreover, the impact of L. intestinalis on reproductive parameters of roach appeared to be independent of the parasite burden. Together, these data provide valuable information on the role of FSH and LH as mediators of parasite-induced sterilization in a vertebrate and implicate the selective inhibition of host reproduction by L. intestinalis as a natural source of endocrine disruption in fish.     

How parasitism and pollution affect the physiological homeostasis of aquatic hosts

Parasitism poses a serious threat to hosts under certain circumstances, while the well-being of organisms is also negatively affected by environmental pollution. Little information is available on the simultaneous effects of parasites and pollutants on the physiological homeostasis of organisms. The present paper demonstrates that parasites: (i) may influence the metabolism of pollutants in infected hosts, (ii) interact with pollution in synergistic or antagonistic ways, and (iii) may induce physiological reactions in hosts which were thought to be pollutant-induced. Experimental studies on the uptake and accumulation of metals by fish reveal that fish infected with acanthocephalans have lower metal levels than uninfected hosts; e.g. Pomphorhynchus laevis reduces lead levels in fish bile, thereby diminishing or impeding the hepatic intestinal cycling of lead, which may reduce the quantity of metals available for fish. Alterations in pollutant uptake and accumulation in different intermediate and final hosts due to parasites are thus very important in the field of ecotoxicology. In addition to such alterations, there is a close interaction between the effects of pollutants and parasites which seems to be mediated at least partly by the endocrine system, which itself is closely related to the immune system in fish. Laboratory studies on eels experimentally infected with the swimbladder nematode Anguillicola crassus reveal that toxic chemicals such as polychlorinated biphenyls produce immunosuppressive effects which facilitate parasite infection. Similarly, an increase in serum cortisol concentration in eels due to chemical exposure and infection is correlated with decreasing levels of anti-A. crassus antibodies. Furthermore, parasites are able to elicit physiological changes which are attributed to chemicals with endocrine disrupting activity, e.g. the cestode Ligula intestinalis is known to suppress gonad development in roach. The most thoroughly documented examples of endocrine disruption in wild fish are in roach, and it is conceivable that this disruption is not only due to chemical activity but also to parasites such as L. intestinalis or species of the phylum Microspora.     

The effects of a change in the growth rate of roach, Rutilus rutilus (L.), on the biology of the fish tapeworm Ligula intestinalis (L.)

Investigations into the biology of the roach and the pathogenic tapeworm Ligula intestinalis (L.) populations at Slapton Ley, Devon were carried out between October 1982 and December 1984. Data collected from the lake since 1977 have also been re-analysed to determine how the dramatic improvement in the individual growth rate of the roach over this period may have affected the growth, maturation and life-cycle of Ligula. Only the very young roach at this site become infected, so it was possible to follow cohorts of plerocercoids of similar age through each roach year class. Results for the 1978 and 1983 year classes are presented in detail. The roach grew extremely rapidly from May to August in each year, resulting in a pronounced cyclical pattern of changes in the condition of the roach, with the lowest condition occurring in late winter and spring. The yearly increase in the roach growth rate was accompanied by an increase in plerocercoid growth rate in the 0 + roach, but not in the 1 + roach. The growth rate of the plerocercoids was very high compared to that at other sites. It is usual for the parasite index (PI) of Ligula-infected fish to be high and to increase throughout their first few years of life. At Slapton, however, a lack of multiple infections has prevented high PIs from occurring, and in recent years the growth rate of the roach has been so high that the plerocercoids were unable to maintain a high weight relative to the fish, and the highest PIs occurred in the 0 + roach throughout late winter and spring. In recent year classes, therefore, the maximum PIs and highest pathogenicities coincided with the period of lowest condition in the 0+ roach. Observations of both caged and natural populations of 0+ roach over winter showed that a significant loss of roach containing the larger plerocercoids occurred from the population. In vitro cultivation of Ligula plerocercoids showed that they were capable of maturation at weights of 0.5 g, and only 6 months after having infected the roach. The increase of the growth rate of the plerocercoids in the 0+ roach has therefore resulted in a greater proportion of these plerocercoids being capable of infecting the definitive host. As a result of the increase in individual growth rate of the roach at Slapton, the potential for Ligula transmission, as measured in terms of both their pathogenicity and maturity, has shifted from the 1 + to the 0+ roach.     

The distribution and growth of coarse fish in gravel-pit lakes in south-east England

SUMMARY. Age and growth rates of the coarse fish of thirty-nine gravel-pit lakes in south-east England are compared. Species composition was very variable, the commonest species being roach ( Rutilus rutilus ), bream ( Abramis brama ), tench ( Tinca tinca ), perch ( Perca fluviatilis ) and pike ( Esox lucius ). Two main kinds of fish community were identifiable from the survey: (1) those consisting of a mixture of cyprinids, usually roach and bream; and (2) those in which cyprinids were rare or absent and the fish community was composed of perch and pike. The majority of the lakes fell into the first category. Comparison of growth curves derived by back-calculation showed that, in all species, variation occurred from lake to lake and from year to year. The majority of gravel-pit lake fishes had 'medium' growth rates when compared with published data by other workers on different waters. Seasonal growth of roach infected with plerocercoids of Ligula intestinalis was observed at monthly intervals. Annulus formation on the scales of these fish occurred at the onset of growth in May. The heavy Ligula burden in 89% of these fish had not caused the formation of any additional or false rings.     

Studies on Ligula intestinalis Some aspects of the pathology in the second intermediate host

A 3 year survey of a lake, in which 120 roach, Rutilus rutilus , were examined revealed the presence of the plerocercoids of Ligula intestinalis in more than 90 % of the fish. The average number of parasites per fish was 4.2 although fish exceeding 32 g were not ligulosed. Gudgeon, Gobio gobio , of all sizes were affected. Implants of the plerocercoids into small roach, gudgeon and goldfish, Carassius auratus , were successful but not in the case of Perca fluviatilis, Esox lucius and Leuciscus cephalus. The pathological effects of the plerocercoids on roach and gudgeon are described.     

Behaviour of roach (Rutilus rutilus L.) altered by Ligula intestinalis (Cestoda: Pseudophyllidea): a field demonstration

1. We studied the influence of a cestode parasite, the tapeworm Ligula intestinalis (L.) on roach ( Rutilus rutilus L.) spatial occupancy in a French reservoir (Lake Pareloup, South-west of France).
2. Fish host age, habitat use and parasite occurrence and abundance were determined during a 1 year cycle using monthly gill-net catches. Multivariate analysis [generalized linear models (GLIM)], revealed significant relationships ( P  < 0.05) between roach age, its spatial occupancy and parasite occurrence and abundance.
3. Three-year-old roach were found to be heavily parasitized and their location toward the bank was significantly linked to parasite occurrence and abundance. Parasitized fish, considering both parasite occurrence and abundance, tended to occur close to the bank between July and December. On the contrary, between January and June no significant relationship was found.
4. These behavioural changes induced by the parasite may increase piscivorous bird encounter rate and predation efficiency on parasitized roach and therefore facilitate completion of the parasite's life cycle.     

Overwinter body condition,mortality and parasite infection in two size classes of 0+ year juvenile European bitterling Rhodeus amarus

Body condition and parasite abundance were examined in two size classes of European bitterling Rhodeus amarus during the first overwintering period in two seasons (2007–2008 and 2009–2010). Body condition of large fish did not change during winter, and increased significantly in March. From November to February, small fish showed a decreasing trend in condition. Despite a significant increase in March condition of small fish only reached the same level as before winter. Total parasite abundance increased significantly in winter in both fish size classes, reflecting a seasonal increase in monogenean infection. Large fish were parasitized significantly more than small fish during winter, but only in small fish was a negative correlation between parasite infection and condition found and a significant decrease in parasite abundance recorded after wintering, indicating mortality of heavily infected individuals with low condition during the winter. A trend for higher overwinter mortality in small fish was found under semi‐experimental conditions. The decrease in condition during the winter period in small fish may reflect faster energy depletion generally expected in smaller individuals. The results indicate that parasite infection may contribute to the overwinter mortality of 0+ year R. amarus, with a stronger effect in smaller individuals.     

Host switch and infestation by Ligula intestinalis L. in a silver bream (Blicca bjoerkna L.) population

Sampling of the fish community was carried out for 20 years in the Mirgenbach reservoir, in North-Eastern France. The prevalence and the mean intensity of Ligula intestinalis (Cestoda) were analysed in roach (Rutilus rutilus) and silver bream (Blicca bjoerkna) populations, the main two infected species. The aim of this study was to investigate the host switch from roach to silver bream and the consequences of L. intestinalis infestation in silver bream, which is an unusual host for this parasite as Ligula parasitism in silver bream appears to be rare. We analysed in detail the relationships between parasitism index (PI), gonadosomatic index (GSI), perivisceral fat abundance (PFA) and condition index (CI) in the silver bream population. In 1998, prevalence of L. intestinalis highlighted a clear host switch from roach to silver bream. In the silver bream population, young fish were the most severely infected and the impact of plerocercoids appeared to be different depending on the host sex. In male silver bream, plerocercoids drew energy from fat reserves even if GSI was also slightly impacted. On the contrary, in females energy was diverted from gonad maturation rather than from perivisceral fat reserves. No significant difference was observed in terms of CI in either sex.     

Compared parasitic infection of Ligula intestinalis (Cestoda: Diphyllobothridae) in Cyprinidae species: Rutilus rubilio and Scardinius erythrophthalmus in two dam reserves in Tunisia

Monitoring quantitative parameters of parasitism by ligula intestinalis (Cestoda: Diphyllobothridae) was performed by examining 516 fish belonging to two introduced freshwater species: Rutilus rubilio (350 individuals) and Scardinius erythrophthalmus (166 individuals). These fish were collected in two dam reserves in Tunisia, Sidi Salem and Nebhana. The analysis of the aquatic bird's composition in these two reserves revealed the existence of piscivorous bird species that were previously reported as final host of Ligula. Monitoring the bird's composition highlighted higher relative abundance and frequency in Sidi Salem than in Nebhana dam reserve. The analyses of the prevalence, mean intensity and abundance of the parasite revealed the most important values in roach, Rutilus rubilio which seems to be the preferential second intermediate host of the parasite Ligula intestinalis in these environments. Comparative analysis of parasitism in both explored sites suggests that Ligula intestinalis presents two different strategies of infestation. In Sidi Salem reserve, which is larger than Nebhana and containing on important and diversified piscivorous species, the parasite infects a maximum of host individuals with low parasite mean intensity values. However, at Nebhana, which is a smaller reserve, the parasite infects fewer individuals than Sidi Salem but with higher mean intensity. The highest prevalence values were recorded in large size classes of roach species in Sidi Salem reserve.     

Studies on Ligula intestinalis (L.) effects on a roach population in a gravel pit

The effects of the plerocercoids of Ligula intestinalis were studied on a population of roach, Rutilus rutilus in a gravel pit. The incidence of the cestode fell from 92% in 0+ roach in April to 25 % in January of the succeeding year. The fall in the number of parasitized fish was due to predation, mainly by pike, Esox lucius. Observations indicated most of the parasitized fish failed to become sexually mature although the actual growth rate of the fish was not markedly reduced. The plerocercoids of L. intestinalis grew more rapidly during the summer. The author recommends roach of less than 9 months of age should not be introduced into confined water such as a gravel pit, since after this period they appear to be much less likely to be parasitized.     

Evidence for the co-existence of separate strains or species of Ligula in Lough Neagh,Northern Ireland

LIGULA (Cestoda: Pseudophyllidea) infections in gudgeon (Gobio gobio) and roach (Rutilus rutilus) differ markedly in the pathology that is observed in the host, particularly with respect to a tissue response and the extent of inhibition of gonadal development. The entire internal transcribed spacer (ITS) region (ITS-1, 5.8S and ITS-2) and the large subunit domains D1-D3 were sequenced and compared in parasites from these fish from Lough Neagh, Northern Ireland, together with a single specimen from minnow (Phoxinus phoxinus) from Wales. Sufficient differences were observed between parasites from R. rutilus and G. gobio to support the suggestion that they may represent different strains/species. In contrast, Ligula from P. phoxinus closely resembled those from R. rutilus. Ligula infections in G. gobio were recorded prior to the introduction of R. rutilus. The co-existence of separate strains or species of Ligula in Lough Neagh probably resulted from the introduction of R. rutilus to these waters, correlated with an increase in the number of great crested grebes (Podiceps cristatus).     

Infection of Salmincola edwardsii (Copepoda: Lernaeopodidae) in an age-structured population of Arctic charr—a long-term study

The parasite-host relationships between Salmincola edwardsii (Copepoda: Lernaeopodidae) and Arctic charr Salvelinus alpinus were studied in lake Takvatn, northern Norway, over an 8-year period. The infection levels were modest, with an overall prevalence of 16·1% and an abundance of 0·5 parasites fish⁻¹. Most of the infected fish (54·1%) had only one parasite attached, whilst only 4·3% had more than 10. In general, parasite infection increased with increasing age, and hence size of the fish. The increase was modest up to age 7, whereafter a steep increment in parasite burdens occurred. Within each age class there was little effect of either fish size, gender, maturation or choice of macrohabitat upon parasite abundance. There was also little year-to-year variation in infection of the different age classes, indicating a high degree of stability of the parasite-host interactions in this system. The infection levels exhibited seasonal changes, being lowest in early summer and highest during winter. The infection rates seemed to be related to seasonal and ontogenetic habitat shifts of the charr.     

The decline of a roach Rutilus rutilus (L.) population in Chew Valley Lake

A series of nettings for roach in Chew Valley Lake carried out by members of the Zoology Department, Bristol University, has revealed a marked decline in the population between 1965 and 1968. Fish from the main Lake were found to be heavily parasitized with Ligula intestinalis (L.) while those from the inflow pool (Herriott's Pool) were practically free from infection. It is considered that the decline of the roach can be linked to the incidence of Ligula , but that clean fish from the inflow pool may provide breeding stock and maintain the production of fry, which serve as food for the trout.