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.     

Ligula intestinalis infection as a potential source of bias in the bioindication of endocrine disruption in the European chub Leuciscus cephalus

European chub Leuciscus cephalus collected from five localities in the lowland and subalpine regions of Austria were analysed for oestrogenic effects of endocrine-disrupting chemicals and the presence of the plerocercoid of the tapeworm Ligula intestinalis. Of 1494 chub analysed, only seven (six males, one female) were found to be infected with single, but large plerocercoids up to 15 cm in length. Ligula-infected fish showed comparatively immature gonads, as demonstrated by the gonadosomatic index and gamete developmental stages. Plasma levels of the egg precursor protein vitellogenin also showed concentrations ranging below the detection limit. The present results indicate that chub infected with L. intestinalis and exposed to exogenous oestrogenic compounds can result in reduced gonadal maturation and produce false oestrogen-positive diagnoses in male fish. For plasma vitellogenin levels, L. intestinalis infections can result in false oestrogen-negative diagnoses in male and female 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.     

Distribution of the plerocercoid of Ligula intestinalis

The geographical distribution of the cestode Ligula intestinalis (Linnaeus 1758) is described with reference to the species of freshwater fish infected. Recent references indicate that the larval stage of this cestode is commonly reported from the Northern Hemisphere but less commonly from the Southern Hemisphere.
Cyprinid fish are infected in the Northern Hemisphere in the New and Old World, and where cyprinid fish are scarce, fish occupying a similar ecological position are infected. However, the infection of Yellow perch in North America and the absence of infected European perch may suggest that the form in the Yellow perch if not morphologically, may be physiologically, distinct.
In the Southern Hemisphere cyprinids have been reported as infected in Rhodesia and galaxids as infected in Australia. The infection of galaxids, some of which enter the sea to breed may indicate a possible method of distribution. It is suggested that transplantation of the larval cestode from the body cavity of one fish to another may yield more definite information as regards specificity.
The infection of fish, other than those listed, is reviewed with reference to those fish known to occur in habitats where fish infected with Ligula intestinalis also exist.     

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.     

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.     

The effects of Lepeophtheirus salmonis infections on the stress response and immunological status of Atlantic salmon (Salmo salar)

This study was conducted to determine the effects of a high level of infection of the parasitic copepod L. salmonis on the stress response and immunological status of Atlantic salmon. An initial low-level initial infection was carried out 14d prior to a second infection in which twice as many parasites were introduced. Plasma cortisol and prostaglandin E(2) (PGE(2)) levels were monitored concurrent to the expression of six immune-related genes over five sample times (9, 21, 26, 33 and 40days post initial infection, dpii). The mean lice counts on the infected fish increased significantly from the first infection (16.3+/-1.89 at 9dpii) to the second (142.8+/-12.8 at 26dpii). Plasma cortisol levels increased significantly at 26, 33 and 40dpii in infected fish compared to controls. Plasma PGE(2) levels were significantly higher in infected fish at 9, 33 and 40dpii, when compared to controls. At 9dpii, expression of interleukin-1beta (IL-1beta), tumour necrosis factor-alpha (TNFalpha)-like cytokine, major histocompatibility class II (MH II), transforming growth factor-beta (TGFbeta)-like cytokine and cyclooxygenase-2 genes were increased in infected fish compared to controls. The expression of most of these genes returned to control levels at 21dpii when the highest expression of the MH class I gene was observed in infected fish (significantly higher than controls). Major histocompatibility class I gene expression remained higher in infected fish at 26 and 33dpii compared to controls and this was observed for the TNFalpha-like gene. By 33dpii, MH class II and TGFbeta-like genes had higher expression in infected fish compared to controls. Interleukin-1beta and TNFalpha-like gene were the only genes that showed significantly higher expression in infected fish compared to controls at 40dpii, while MH class I gene expression was significantly depressed in infected fish at this time. The expression of nearly all immune-related genes studied here increased following initial infection with L. salmonis, however, immunological stimulation did not reduce parasite numbers or protect against re-infection.     

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.     

The establishment and subsequent history of a population of Ligula intestinalis in roach Rutilis rutilis (L.)

The introduction, establishment and subsequent history of a population of Ligula intestinalis in roach, Rutilus rutilus , of a small lake was studied over a period of seven years. The introduction is believed to be a natural, chance colonization achieved by the return of Great Crested Grebes as permanent residents. Within two years the parasite had infected 33% of the roach between 60–120 mm in size. It exhibited a pronounced seasonal cycle in infection. Fish were often infected when only a few months old in autumn, and young fish and parasites over-wintered together. Parasite growth resumed in the following summer, when some further infections occurred. The majority of infected fish died in or before their second winter, possibly as a result of selective predation, but a small proportion survived into a third year. Dispersion of the parasite was close to random for most of the time. Multiple infections and slight over-dispersion occurred only in summer months. Infections were scarcer in large fish, due partly to selective mortality of infected fish and partly to a change in the host diet. The pattern of seasonal infection compared favourably with other localities, but prevalence and intensity of infection were consistently lower, parasite dispersion closer to random and multiple infections much scarcer than elsewhere. Infection levels and parasite growth rates varied from year to year, but these annual fluctuations were irregular and showed no consistent pattern. The Ligula population exhibited both regulatory and destabilizing features and there was no definite evidence that it was stable. It is suggested that Ligula is an opportunist species. It is endemic in some sites but in others, especially small lakes, the populations are unregulated and unstable and so persist for short periods only in a non-equilibrium state.     

Induction time for resistance to microsporidial gill disease caused by Loma salmonae following vaccination of rainbow trout (Oncorhynchus mykiss) with a spore-based vaccine

Resistance to re-infection of rainbow trout to Loma salmonae, a microsporidian gill parasite has been previously documented and this study examined how rapidly this resistance develops. Naive rainbow trout were inoculated intraperitoneally (IP) with an inactivated spore-based vaccine and were then given an oral challenge with a high dose of L. salmonae spores at various weeks after being vaccinated. Non-vaccinated naive fish (exposed group) were challenged alongside of each group of vaccinated fish to ensure that the challenges were relatively standardised. In each group of fish, four weeks after the challenge, numbers of xenomas were counted on a gill arch for all fish. Vaccinated trout were completely resistant to a L. salmonae challenge six weeks after vaccination, although the onset of resistance began at approximately week 3, as observed with a reduction in the percent infected and xenoma intensity. The maximum percent infected for the vaccinated fish was 83% following a challenge two weeks following vaccination, whereas for the exposed group the maximum prevalence of 100% was reached several times. With continued research, a spore-based vaccine for L. salmonae has the potential to become the first commercially available parasite vaccine for fish.     

Severe, chronic proliferative kidney disease (PKD) induced in rainbow trout Oncorhynchus mykiss held at a constant 18 degrees C

Proliferative kidney disease (PKD), caused by the myxozoan parasite Tetracapsuloides bryosalmonae, is well documented as a seasonal disease of rainbow trout Oncorhynchus mykiss. Water temperatures influence the course of the infection both within the fish and the invertebrate host, the recovery of fish from the disease being accelerated with decreasing water temperatures. During this study, groups of rainbow trout were held at a constant temperature (18 degrees C) for a sustained period of time following initial exposure to T. bryosalmonae. While the majority of these fish had recovered from the clinical disease after 9 mo, 10% remained infected, showing clinical signs of disease. A histological study revealed that the majority exhibited very high parasite loads and unusually severe symptoms of PKD. This demonstrates that while most rainbow trout can recover from PKD independent of water temperature, there exists a sub-population that cannot.     

Ligula intestinalis--a tapeworm contraceptive

Human contraceptives are 'big business', but might the real breakthrough come out from the pharmaceutical industry but from a tapeworm? Ligula intestinalis can induce infertility in infected fish of the carp family - both males and females. If the mechanism for this can be discovered, this humble flatworm could drastically change contraceptive practices with one pill for all.     

Impact of Ligula intestinalis (L.1758) (Cestode), on the growth of Barbus setivimensis (Cyprinidae) in a lake system in Algeria

The Algerian freshwater fish fauna is mainly represented by the Cyprinidae family, in particular, the genus Barbus. This is represented only by natural populations of the subgenus Barbus. The systematic, based mainly on the methods of biometrics, is quite different from one author to another. However, two nominal species are usually cited: Barbus callensis (Valenciennes, 1842), which is limited to the region of El Kala (eastern Algeria) and Barbus setivimensis (Valenciennes, 1842) in other parts of the North. During the ecological study of this fauna, many individuals were found infested with the tapeworm Ligula intestinalis (Linné, 1758), which led us to study the effect of this parasite on B. setivimensis using the ecological parasites' index (prevalence, abundance and parasite intensity) and to focus on the impact of the parasite on the growth of fish. Tapeworm L. intestinalis presents a wide geographical distribution and a complex lifecycle to multiple hosts: the cycle starts in the body of birds. The life expectancy in the major host is a maximum of 5 days, but in this time, they will lay a multitude of eggs. These eggs are passed into water via the faeces of the bird. Once in the aquatic medium, they hatch and are eaten by a wide range of copepod zooplankton (first intermediate host). The cycle continues when fish (second intermediate host) ingests the copepod. The worm then burrows through the gut wall and continues to develop in the fish's body cavity. The cycle is then complete when the bird (final host) eats the tapeworm-hosting fish. We studied the effects of diet, the hosting period, the habitat on the prevalence, abundance and intensity of the parasitic larvae plerocercoid L. intestinalis and the parasiting effect on the Cyprinids fishs of the genus Barbus in the Keddara dam (Boumerdes, Algeria) during one year. Although L. intestinalis was recorded in several host fish, the available data on the parameters of parasitism are limited and no studies are reported on B. setivimensis. In this study, a total of 613 individuals were sampled and checked on the presence of L. intestinalis plerocercoid stages. Only 64 were infested. The value of the prevalence was 10.44% and the average intensity was 1.89 parasites (average two parasites per infested fish). The infection rate is high during the autumn and low during the spring season. The latter corresponds with the breeding period.     

Experimental infection of several fish species with the causative agent of Kuchijirosho (snout ulcer disease) derived from the tiger puffer Takifugu rubripes.

Kuchijirosho (snout ulcer disease) is a fatal epidemic disease which affects the tiger puffer, Takifugu rubripes, a commercial fish species in Japan and Korea. To assess the possibility that non-tiger puffer fish can serve as reservoirs of infection, 5 fish species were challenged by infection with the extracts of Kuchijirosho-affected brains from cultured tiger puffer: grass puffer T. niphobles, fine-patterned puffer T. poecilonotus, panther puffer T. pardalis, red sea bream Pagrus major, and black rockfish Sebastes schlegeli. When slightly irritated, all these species, especially the puffer fish, exhibited typical signs of Kuchijirosho, i.e., erratic swimming, biting together and bellying out (swelling of belly), as generally observed in tiger puffers affected by Kuchijirosho. Although the mortalities of the 2 non-puffer species were lower, injection of the extracts prepared from the brains of both inoculated fish into tiger puffer resulted in death, indicating that the inoculated fish used in this experiment have the potential to be infected with the Kuchijirosho agent. Condensations of nuclei or chromatin in the large nerve cells, which is a major characteristic of Kuchijirosho, were histopathologically observed to some extent in the brains of all kinds of puffer fish species infected. These findings suggest that the virus can spread horizontally among wild and cultured puffers and even among fishes belonging to different orders.     

Estimates of daily mortality from a neascus trematode in age-0 shortnose sucker (Chasmistes brevirostris) and the potential impact of avian predation

Parasites may be an important component of early life mortality in fishes, but assigning part of total mortality to parasites is difficult. The Chapman-Robson mortality estimator is a robust and potentially valuable way to quantify the added mortality of parasites when age data are available. We used daily age data and the Chapman-Robson catch-curve procedure to estimate daily mortality for 15 years in juvenile age-0 shortnose suckers (Chasmistes brevirostris), and for 6 years, the daily mortality of fish with and without black spot infection, a trematode whose final host is a piscivorous bird. Infected fish always had higher mortality rates than uninfected fish, and for 3 years when those differences were significant, the added daily mortality for infected fish was 3.6–3.7 %. Based on the proportion infected each year, and for durations of 15–50 d, juvenile populations were 18.3–38.6 % lower than they would have been without black spot infections. There were no significant differences in growth between infected and uninfected fish in most years and little indication of a direct metabolic impact of infections. Thus, this added mortality, primarily in July and August, seemed unlikely to be an indirect result of infection and was most likely due to predation. The source of that predation is unknown but the parasite’s final hosts, piscivorous birds, seemed the most obvious candidate for this added mortality.     

Some aspects of the infection of bib, Trisopterus luscus (L.), by the parasitic copepod Lernaeocera lusci (Basset-Smith, 1896) in Portuguese waters

Winter samples totalling 2308 specimens of Trisopterus luscus (total length range: 13–36 cm) caught in northern Portugal were examined for infections with Lernaeocera lusci. Infection prevalence was of 42%, and infection intensity was 1.7 copepods per infected fish. Individual infection varied between 1 and 9 copepods per infected specimen; 30.6% of the fish had bilateral parasitosis. There was a significant correlation (P<0.01) between fish length and prevalence. Length-weight relationships of uninfected and infected fish were not significantly different (P > 0.05) and thus provide evidence that L. lusci has no effect on the condition of T. luscus in all the examined 1–cm size classes.     

Effects of Ligula intestinalis on habitat use, predation risk and catchability in European minnows

The frequency of infection with Ligula intestinalis (Cestoda) in European minnow Phoxinus phoxinus , in a subalpine lake in Eastern Norway, did not differ between vegetated shoreline, exposed shoreline and non-vegetated localities >50 m from the shoreline. There was no difference in the vertical distribution of infected and uninfected individuals. The frequency of infection was higher among minnows in brown trout Salmo trutta stomachs than among those obtained by gillnets and minnow traps, suggesting that brown trout selectively preyed on infected minnows. Prevalence of infection decreased with increasing fish size, probably due to selective mortality among parasitized individuals. Within a given length-class, minnows captured by different sections of multi-mesh gillnets showed a significant increase in the frequency of infection with increasing mesh-size. Apparently, parasitized individuals had a higher catchability in gillnets due to increased girth caused by the plerocercoid in the body cavity. This may partly explain why the observed prevalence of infection was several times higher among minnows captured by gillnets than by minnow traps.     

Dynamics of Anguillicola crassus larval infections in a paratenic host,the ruffe (Gymnocephalus cernuus) from the Oder River on the border of Germany and Poland

The course of infection of 2-year-old ruffe (Gymnocephalus cernuus L.) from the Oder River (Germany/Poland) with third-stage larvae (L3) of Anguillicola crassus (Nematoda: Anguillicolidae) was investigated at monthly intervals between March 1994 and March 1995. Of 230 fish examined, 152 (66%) harboured viable L3. Monthly prevalences fluctuated between 12 and 96%; mean intensities ranged from 1.0 to 5.6 L3 per infected fish. Temperature-dependent differences in infection were noted with the prevalence and mean intensity of infection being significantly higher (Chi-Square test and Mann-Whitney-U-test, respectively; ) at water temperatures less than 10 degrees C (cold period) than at those above (warm period). These differences remained significant even after the division of fish samples into two size classes (8.5-10.5 cm, 11-13 cm). Although the paratenic hosts may acquire infections year round, the results suggest that ruffe become infected mainly during the cold season and that the host's feeding ecology determines the final course of infection.     

Transmission routes maintaining a viral pathogen of steelhead trout within a complex multi‐host assemblage

This is the first comprehensive region wide, spatially explicit epidemiologic analysis of surveillance data of the aquatic viral pathogen infectious hematopoietic necrosis virus (IHNV) infecting native salmonid fish. The pathogen has been documented in the freshwater ecosystem of the Pacific Northwest of North America since the 1950s, and the current report describes the disease ecology of IHNV during 2000–2012. Prevalence of IHNV infection in monitored salmonid host cohorts ranged from 8% to 30%, with the highest levels observed in juvenile steelhead trout. The spatial distribution of all IHNV‐infected cohorts was concentrated in two sub‐regions of the study area, where historic burden of the viral disease has been high. During the study period, prevalence levels fluctuated with a temporal peak in 2002. Virologic and genetic surveillance data were analyzed for evidence of three separate but not mutually exclusive transmission routes hypothesized to be maintaining IHNV in the freshwater ecosystem. Transmission between year classes of juvenile fish at individual sites (route 1) was supported at varying levels of certainty in 10%–55% of candidate cases, transmission between neighboring juvenile cohorts (route 2) was supported in 31%–78% of candidate cases, and transmission from adult fish returning to the same site as an infected juvenile cohort was supported in 26%–74% of candidate cases. The results of this study indicate that multiple specific transmission routes are acting to maintain IHNV in juvenile fish, providing concrete evidence that can be used to improve resource management. Furthermore, these results demonstrate that more sophisticated analysis of available spatio‐temporal and genetic data is likely to yield greater insight in future studies.