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.     

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.     

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 .     

Ligulosis associated with mortality in largescale suckers

Investigations of a fish kill at an irrigation reservoir in the Deschutes River basin, Oregon, documented at least 153 dead largescale suckers Catostomus macrocheilus , all heavily infected with large Ligula intestinalis (Cestoda). Moribund fish nearshore were similarly infected, with no evidence of secondary disease or infection. Morbidity and mortality in all cases was probably due to severe mechanical damage to internal host organs resulting from infection with multiple, large L. intestinalis . The pathology of L. intestinalis documented in largescale sucker in this study contrasts sharply with previous accounts and may represent a new and emerging disease for largescale suckers.     

First record of Ligula intestinalis from stone loach

The cestode Ligula intestinalis was recorded for the first time from stone loach Barbatula barbatulus . Details regarding their site of capture and intensity of infection are provided.     

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.     

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.     

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.     

First records of Ligula intestinalis (Cestoda) in rainbow trout, Salmo gairdneri, and common bully, Gobiomorphus cotidianus, in New Zealand

Plerocercoids of the tapeworm Ligula intestinalis are reported from a salmonid, Salmo gairdneri , and an eleotrid, Gobiomorphus cotidianus , in New Zealand for the first time. There was no significant difference in condition factors between infected and uninfected trout. The prevalence of infection in bullies sampled increased with total length.     

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.     

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.     

The effects of suspensoids on fish

High suspensoid loads are a common feature of many Southern Hemisphere inland waters. Case studies on a natural lake (Chilwa), a man-made lake (Le Roux) and S.W. Indian Ocean estuaries reveal that the effects of turbidity on fish in these systems differ widely. In Lake Le Roux, high suspensoid loads influence fish by causing a reduced growth rate, a decrease in size at first maturity and maximum size, and a movement inshore by large fishes to feed on phytobenthos. High turbidities in Lake Chilwa sharply reduce food availability in benthic offshore zones, and restrict fishes to pelagic and inshore food resources. The resuspension of sediments by wind action may cause fish mortalities through deoxygenation of the water column. Moderate turbidity levels appear to be beneficial to fish in estuaries by affording protection from predators in shallow, food-rich areas. Turbidity gradients may also provide a navigational aid to fish entering estuaries.While ecological studies on Southern Hemisphere inland waters are fairly advanced, experimental work is restricted. Such research in the Northern Hemisphere has revealed that high suspensoid loads may influence breeding success, egg and larval survival, population structure and size, as well as food availability and feeding efficiency. The effect of suspensoids on the breeding success and feeding efficiency of Southern Hemisphere fish needs further investigation.Moderate suspensoid loads are a natural feature of many inland waters, but sustained high levels reduce the photic zone, blanket the benthos and interfere with the feeding efficiency of fish. The curtailment of soil erosion should therefore be regarded as a priority in the management of inland fisheries, especially in Third World countries where poor land-use practises have resulted in a marked deterioration of water quality. The need to study and manage river catchments holistically is emphasized.     

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.     

青海湖裸鲤寄生舌状绦虫的空间格局研究

舌状绦虫裂头蚴只寄生在体长小于２２０ｍｍ的青海湖裸鲤中,其种群在宿主种群中呈聚集分布。其聚集分布的强度随寄生虫种群平均密度的增加而降低。由于舌状绦虫在宿主体腔生长,产生明显的空间拥挤效应,可能导致宿主死亡或被食鱼鸟类捕食而转移到终末宿主中。在体长小于１２０ｍｍ的宿主中,密度依赖的死亡过程可能是使聚集强度降低的原因;而体长１４０－２００ｍｍ的鱼中,则是非密度依赖的全死过程使聚集强度增加．     

Distribution and occurrence of <Emphasis Type="Italic">Ligula intestinalis</Emphasis> (L.) plerocercoids (Cestoda,Ligulidae) in the fishes of Lake Tana,Ethiopia

The infection rate by Ligula intestinalis has been studied in 14 fish species (Varicorhinus beso, Garra dembecha, Labeobarbus intermedius, L. crassibarbis, L. tsanensis, L. megastoma, L. brevicephalus, L. nedgia, L. acutirostris, L. gorgorensis, L. dainellii, L. macrophthalmus, Barbus humilis, and B. tanapelagius) from Lake Tana (Ethiopia). Plerocercoids have been found only in the fishes of gg. Labeobarbus and Barbus. Ligula has been found in seven out of ten studied large barbels. Barbels larger than 23 cm are not infected with ligula. It is revealed that a specific “synergism” exists between Ligula intestinalis and cestode Khawia sp. parasitizing the intestine of barbels. This synergism is manifested as a regular cooccurrence of these parasites. In juvenile Labeobarbus, fish coparasitized by Khawia sp. and L. intestinalis occurred more often than fish infected with each of this parasite separately.     

青海湖裸鲤体腔寄生蠕虫群落研究

青海湖裸鲤体腔为三种寄生蠕虫寄生,即裂头绦虫裂头蚴,舌状绦虫裂头蚴和对盲囊缄虫的三期幼虫,这几种蠕虫不同大小的青海湖裸鲤中数量差异很大,将其看作一个组分群落,并根据其发生数量进行模糊聚类和极点排序,结果将其分为二个亚组分群落,即体长小于１５０ｍｍ的青海湖裸鲤体腔蠕虫亚组分群落和体长大于１５０ｍｍ的个体的体腔蠕虫亚组分群落。这与宿主的行为和食性改变有密切关系,舌状绦虫与另两种蠕虫间有显著负协调关系。     

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.     

Joint effects of parasitism and pollution on oxidative stress biomarkers in yellow perch Perca flavescens

Yellow perch Perca flavescens were collected from a contaminated site and a reference site in the St. Lawrence River, Quebec, Canada. Fish were assessed for oxidative stress (lipid peroxidation and reduced glutathione levels) and parasitism by the nematode Raphidascaris acus and metacercariae of the digenean Apophallus brevis. Lipid peroxidation is not only considered a measure of oxidative stress, but of stress in general, and thus serves as an indicator of fish health. Fish from the contaminated site exhibited higher levels of lipid peroxidation than those from the reference site, independent of parasitic infections. However, fish infected with R. acus at the contaminated site tended to have higher levels of lipid peroxidation than uninfected fish at the same site, whereas no difference was observed between infected and uninfected fish at the reference site. Yellow perch infected with > 10 metacercariae of A. brevis expressed higher levels of lipid peroxidation than those infected with < 10 metacercariae at both the contaminated and the reference sites. No differences were found in levels of reduced glutathione in liver or muscle in relation to site or either parasite species. Results support the use of lipid peroxidation as a biomarker of water contamination. They further suggest that lipid peroxidation may be used as a biomarker of pathological effects caused by parasitism. Most importantly, results demonstrate that contaminants and parasites occurring together exacerbate oxidative stress in fish, suggesting that parasitized fish in polluted environments are in a poorer state of health than uninfected fish.     

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.