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.     

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.     

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 (L.) (Cestoda: Pseudophyllidea): plerocercoid-induced changes in the spleen and pronephros of roach, Rutilus rutilus (L.), and gudgeon, Gobio gobio (L.)

The effects of the plerocercoid of Ligula intestinalis (L.) (Cestoda: Pseudophyllidea) on the major lymphoid organs, the spleen and pronephros, of roach, Rutilus rutilus (L.), and gudgeon, Gobio gobio (L.), are described. The spleen of ligulosed roach showed a significant decrease in weight. Differential cell counts suggested this was due to a reduction in erythrocytes, despite significant increases in macrophages and vacuolated granulocytes. The spleen of gudgeon, which consisted almost entirely of erythrocytes, showed a slight reduction in weight in ligulosed fish. In both roach and gudgeon this decrease was independent of parasite burden. Differential cell counts of the pronephros from ligulosed roach revealed a significant decrease in neutrophils and increase in vacuolated granulocytes. In the pronephros of gudgeon, however, cell counts were unaffected by ligulosis. Ultrastructural observations included an apparent disintegration of vacuolated granulocytes and increased pinocytic activity in specialized endothelial cells in the spleens of ligulosed roach. Also, melano-macrophage centres and melano-macrophages increased in the spleen of ligulosed roach and gudgeon, respectively. The marked changes in spleen weight and differential cell counts in ligulosed roach and lack of such changes in ligulosed gudgeon correlate with the differential response to the parasite by these two fish species.     

Observations on a tissue response within the body cavity of fish infected with the plerocercoid larvae of Ligula intestinalis (L.) (Cestoda: Pseudophyllidea)

Infection of certain species of cyprinid fish with the plerocercoid larva of the cestode Ligula intestinalis is accompanied by a host tissue response.
The tissue reaction is evident in roach Rutilus rutilus as young as three months. An initial cellular infiltration is followed by the laying down of sheets of connective tissue. A case of calcification is described in a single infected rudd Scardinius erythrophthalmus .     

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.     

Parasite community and mortality of overwintering young-of-the-year roach (Rutilus rutilus)

The composition and development of the parasite community of overwintering young-of-the-year (YOY) roach (Rutilus rutilus) was studied in outdoor artificial ponds. Cumulative mortality of the roach from November until May was about 20%. The prevalences of the epizoic ciliates Trichodina sp. and Apiosoma sp., and of the monogeneans Dactylogyrus suecicus, Dactylogyrus nanus, and Gyrodactylus sp. in general tended to peak in the beginning of April at a water temperature of about 8 C. However, mean parasite intensity remained constant over this interval. Prevalence of metacercariae of the digeneans Diplostomum cf. spathaceum and Tylodelphys clavata remained constant with values around 60% and 10%, respectively. Larvae of the nematode Philometra obturans and the cestode Ligula intestinalis and females of the copepod Neoergasilus japonicus were found sporadically. A concept of 2 thresholds, a critical condition factor (attained by a temperature-induced energy deficiency), and a condition-dependent critical infection intensity, which determine winter mortality of YOY, is suggested.     

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.     

Inhibition of gametogenesis by the cestode Ligula intestinalis in roach (Rutilus rutilus) is attenuated under laboratory conditions

Reproductive parameters of Ligula intestinalis-infected roach (Rutilus rutilus) which were held under long-tem laboratory conditions with unlimited food supply were investigated. Although uninfected and infected roach showed no difference in condition factor and both groups deposited perivisceral fat, the gonadosomatic-index was significantly lower in infected female and male roach. Quantitative histological analysis revealed that gonad development was retarded upon parasitization in both genders. In contrast to the phenotype described in the field, infected females were able to recruit follicles into secondary growth, but a high percentage of secondary growth follicles underwent atresia. In both genders, the histological data corresponded well with reduced expression of pituitary gonadotropins and lowered plasma concentrations of sex steroids, as revealed by real-time RT-PCR and ELISA, respectively. Furthermore, a reduction of vitellogenin mRNA and modulated expression of sex steroid receptors in the liver was demonstrated. Like in the field, there was a significant adverse impact of L. intestinalis on host reproductive physiology which could not be related to parasite burden. Our results show, for the first time, that maintenance under laboratory conditions can not abolish the deleterious effect of L. intestinalis on gametogenesis in roach, and indicate a specific inhibition of host reproduction by endocrine disruption.     

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.     

Encounter rate between local populations shapes host selection in complex parasite life cycle

The present study aimed to understand how a parasite with a complex life cycle selects a given host succession when several potential hosts are present. Ligula intestinalis (Cestoda, Pseudophyllidea) was considered, which presents a life cycle with three hosts: copepod, fish, and piscivorous bird. Encounter probability between each pair of hosts was calculated for Lavernose-Lacasse gravel pit (France) using a sum of the product of the host abundances over time. Among four potential copepod hosts, two potential fish hosts, and six potential bird hosts, the results demonstrate that the copepod Eudiaptomus gracilis , the roach ( Rutilus rutilus ), and the great crested grebe ( Podiceps cristatus ) had a maximal encounter probability due to their abundance, but also due to the similarities of the temporal dynamics of their life cycles. These results agree with previous experiments and field work identifying a high specificity of L. intestinalis to E. gracilis , R. rutilus , and P. cristatus in the study site. This suggests that the abundance of potential hosts and the temporal dynamics of their life cycles act together to determine encounter rates between hosts and parasites, and thus could constitute a crucial determinant in local host selection by parasites with a complex life cycle.  © 2006 The Linnean Society of London, Biological Journal of the Linnean Society , 2006, 89 , 99–106.     

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.     

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.     

Parameters of the blood and immune system of Rutilus rutilus lacustris (Cypriniformes: Cyprinidae) during an invasion with pleurocercoids of Ligula intestinalis (Pseudophyllidae: Ligulidae)

The morphological composition of blood and the reaction of the immune system in a Siberian roach Rutilus rutilus lacustris (Baikal, Chivyrkuiskii Bay) both infested and not infested with pleurocercoids of Ligula intestinalis is investigated. An infestation with L. intestinalis renders a negative effect on the morphological and immunological parameters of blood supporting the immunological homeostasis of its host. In comparison with individuals not infested, the following changes are recorded in the infested individuals: a decrease in the count of erythrocytes and leukocytes (due to a decrease in lymphocytes), increase of the quantity of foam cells, inhibition of T-lymphocytic link of immunity, and a decrease in the content of the total protein, albumin, and gamma-globulin fractions of protein. The change of hematological and immune reactions of a host organism ensures a prolonged mutual adaptation of the parasite and host.     

Interspecific dominance amongst three species of coarse fish in Slapton Ley, Devon

Marked changes in the relative numbers of roach Rutilus rulilus (L.), rudd Scardinius erylhroplhalmus (L.) and perch Perca fIuviatilis L. , in Slapton Ley, Devon, have been observed over the period 1967–1978. Historically, the lake had been dominated by rudd and perch; significant numbers of roach were not thought to be present until 1967. From then onwards the roach population exhibited a considerable expansion, apparently replacing the rudd, which had virtually disappeared by 1974. In 1975 extensive mortalities of roach were caused by the pseudophyllidean cestode Ligula intestinalis L. During 1976 and 1977 larger number of rudd, belonging to the 1975 and 1976 year classes, were present, suggesting that the roach mortalities might be giving the rudd a chance to recover. However, very few rudd were present during 1978, possibly because lower incidences of ligulosis during 1976–1978 had allowed the roach to recover from the main outbreak of the disease in 1975, and to replace the rudd for the second time. Evidence from trap catches indicated that the perch population had shown a consistent decline between 1970 and 1977. The major phase of this decrease occurred between 1971 and 1973, when the roach population was increasing the most rapidly. Comparisons were made with changes in fish populations in other localities. The major reason for the changes observed was thought to be a competitive relationship between the plankton feeding younger stages, with roach being the dominant species, although other factors may also have been involved.     

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.     

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.     

Biological and ecological effects of a Ligula intestinalis (L.) infestation of the gudgeon, Gobiogobio (L.), in Lough Neagh, Northern Ireland

A study was made of the effects of a Ligula intestinalis infestation on the biology and distribution of gudgeon in Lough Neagh, Northern Ireland. During the summer months, when the majority of the gudgeon population was restricted to the inshore areas of the lough, Ligula was present in all age (size) classes of the host although levels of infestation were highest in the oldest individuals. While there was no significant effect on the length-weight relationship of the gudgeon, the presence of the parasite did adversely affect gonad size in both sexes. Ligula also influenced the distribution of the gudgeon population by decreasing the swimming depth of infested individuals and by delaying their autumnal migration to the deeper offshore parts of the lough.     

Host immunization shapes interspecific associations in trematode parasites

1. Individuals of free-living organisms are commonly infected by multiple parasite species. Under such circumstances, positive or negative associations between the species are possible because of direct or indirect interactions, details in parasite transmission ecology and host-mediated factors. One possible mechanism underlying these processes is host immunity, but its role in shaping these associations has rarely been tackled experimentally.
2. In this study, we tested the effect of host immunization on associations between trematode parasites infecting eyes of fish. We first analysed the associations between three species ( Diplostomum spathaceum , Diplostomum gasterostei and Tylodelphys clavata ) in wild hosts, roach ( Rutilus rutilus ) and perch ( Perca fluviatilis ). Second, using rainbow trout ( Oncorhynchus mykiss ) as a model fish species, we experimentally investigated how sequential immunization of the host (i.e. one parasite species infects and immunizes the host first) could affect the associations between two of the species.
3. The results indicated that most of the associations were positive in wild hosts, which supports between-individual variation in host susceptibility, rather than competitive exclusion between the parasite species. However, positive associations were more common in roach than in perch, possibly reflecting differences in ecological conditions of exposure between the host species. The experimental data showed that positive associations between two of the species were eroded by host immunization against one of the parasite species.
4. We conclude that sequential immunization of hosts has a marked effect on interspecific parasite associations and basically can determine if positive associations are detected or not. This implies that correlative results suggesting non-interactive community structure in general may be obscured by the sequence of previous parasite exposure and corresponding dynamics of host immunization.