Ligula Intestinalis Research Articles

The occurrence and dynamics of Ligula intestinalis in its cyprinid fish host, tench, Tinca tinca, in MoganLake (Ankara, Turkey)

Although Ligula intestinalis (L., 1758) has been recorded in several fish hosts, available data on the parasitization parameters of Ligula intestinalis plerocercoids such as prevalence, mean intensity and parasitic index in tench (Tinca tinca L., 1758) is limited. In this study, totally 272 fishes were investigated for the presence of L. intestinalis plerocercoids. The prevalence value was 40.01% of the whole fish sample and the mean intensity was 2.48. The lower IP values and mean intensity levels may provide some evidence of the strategy of Ligula in order to complete its life cycle. None of the parasitization parameters showed significant differences between the sexes.

Comparative study on the accumulation of heavy metals in different organs of tench (Tinca tinca L. 1758) and plerocercoids of its endoparasite Ligula intestinalis

Concentrations of heavy metals (Cu, Fe, Zn, Mn, Cr, Pb and Cd) in some organs of tench and tissues of its parasite found in Kovada Lake (Turkey) were analyzed using atomic absorption spectrophotometry and subsequently compared with the data from sediments and water. Only Cu, Fe, Zn and Mn were detected in water, sediment, plerocercoids of Ligula intestinalis and fish samples, while levels of Cr, Pb and Cd were below the detection limits. Four elements were found at higher concentrations in the plerocercoid than in different fish tissues (muscle, liver and gill), being 1.6-37.4 times higher than that measured in muscle, liver and gill. Significant positive (for Cu) and negative (for Fe, Zn and Mn) correlations were found between the quantity of heavy metals in water and tissues of L. intestinalis plerocercoids while there were significant positive (for Cu and Zn) and negative (for Fe and Mn) correlations between the quantity of heavy metals in bottom sediment and tissues of L. intestinalis plerocercoids. Cestodes were found suitable to reflect the amount heavy metals in sediments, providing more reliable information about the actual pollution of the reservoirs.

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.

Parasitism in fish—an endocrine modulator of ecological relevance?

Wild bream ( Abramis brama) were collected from the river Elbe, and the influences of parasitic infection by the tapeworm Ligula intestinalis on endocrine and related functions (vitellogenin [VTG]; plasma sex steroids: 17β-estradiol [E2], 11-ketotestosterone [11-KT] and testosterone [T]; relative gonad [GSI] and liver [HSI] growth; maturation stages of germ cells [MS]; prominence of spawning tubercles [STI]) were investigated. Distinct regional differences in infection rates of bream with L. intestinalis were observed along the Elbe with the highest prevalences at the Czech border (up to 45%) and Magdeburg (up to 65%), areas that are heavily contaminated with complex mixtures of organic chemicals and metals. Parasitized fish of both sexes had significantly lower GSIs and poorly developed gonads (low MS). In males, a significant reduction in the prominence of spawning tubercles occurred. Infected females had significantly lower plasma VTG concentrations. A selective suppression of the sex steroids 11-KT and E2 was observed in male and female bream, respectively. Testosterone was not affected in the same manner in fish of both sexes. At sites with an elevated prevalence of L. intestinalis, the extent of the infection of an individual was significantly correlated with the suppression of the measured biomarkers. However, when applying a linear model to compare regional differences in infection prevalence with biological parameters, not all of the observed differences could be explained by parasitization by L. intestinalis. This indicates that other factors such as pollution may have contributed to the effects on reproductive and endocrine processes that occurred along the river. Given that sites with high prevalences of L. intestinalis were also characterized by elevated pollution, it is possible that there exists a combinatory effect of both pollution and parasitization that can have a serious impact on the reproductive capacity of a population, such as was observed at the sampling site at Magdeburg.

The occurence and dynamics of Ligula intestinalis in its cyprinid fish host, tench, Tinca tinca in Mogan Lake (Ankara, Turkey)

Although Ligula intestinalis (L., 1758) has been recorded in several fish hosts, available data on the parasitization parameters of Ligula intestinalis plerocercoids such as prevalence, mean intensity and parasitic index in tench (Tinca tinca L., 1758) is limited. In this study, totally 272 fishes were investigated for the presence of L. intestinalis plerocercoids. The prevalence value was 40.01% of the whole fish sample and the mean intensity was 2.48. The lower IP values and mean intensity levels may provide some evidence of the strategy of Ligula in order to complete its life cycle. None of the parasitization parameters showed significant differences between the sexes.

Parasites of fish at Lake Tana, Ethiopia

This study was conducted at Lake Tana Ethiopia, to identify parasites of fish from a total of 1766 fish of different species sampled during 1998–1999. The study showed that Contracaecum spp. were the most common larval nematode parasite that were identified from the mesentery of 52 (41.94%) Catfish ( Clarias gariepinus ), 17(24.64%) Barbus acutirostris , 102 (9.44%) Barbus tsanensis , 14(12.84%) Barbus brevicephalus , and from the pericardial cavity of 52 (59.8%) Nile tilapia ( Oreochromis niloticus ). The other larval nematodes identified from the mesentery included Amplicaecum spp. and Eustrongylides spp. Cuccullanus spp. (new geographic record) were recovered from the intestinal lumen of 2(0.19%) B. tsanensis . Among the digeneans, Clinostomum spp. were identified from the branchial cavity and skin of 50 (57.47%) and 4 (1.15%) O. niloticus , respectively. The Euclinostomum spp. were recovered from the kidney of 4 (4.6%) and branchial cavity of 2 (2.3%) O. niloticus . Mixed infection by Clinostomum spp. in their branchial cavity and Contracaecum spp. in the pericardial cavity was observed in 35 (40.23%) O. niloticus. Allocreadium sp. (new geographic record) was recovered from the intestinal lumen of 1 Barbus dainellii and Tetracotyle spp. (new geographic record) from the mesentery of 6 (50.0%) Barbus nedgia. Ligula intestinalis was the most prevalent cestode affecting 88 (8.14%) of B. tsanensis , 20 (40.0%) other small barbs and 32 (54.24%) of B. trispilopleura and it was considered as a significant pathogen. Proteocephalus spp. (new geographic record) was recovered from the intestinal lumen of 9 (0.83%) B. tsanensis . Among the crustaceans Dolops ranarum was recovered from the caudal fin of 1 C. gariepinus . The prevalence and pathogenic significance of the parasites as causes of diseases to fish related to the diverse fish fauna of the lake is discussed. Key words/phrases: Cestodes, digeneans, fish parasites, Lake Tana, nematodes SINET: Ethiop. J. Sci Vol.26(1) 2003: 31-36

Seasonal variation of the plerocercoid ligula intestinalis (L) observed in roach (Rutilus rutilus, L) from the yenice irrigation pond, Çanakkale, Turkey

This study was carried out at the Yenice Irrigation Pond between October 1999 and October 2000. For this study 368 roach (Rutilus rutilus) were examined and 37 parasites and 93 Ligula intestinalis were found in the abdominal cavity of the host (prevalence 10.1%, mean intensity 2.51 specimens/fish). Based on season, the highest number of infected fish occurred during summer (33.3%, 4 parasite/fish), and during the other season the mean intensity of infection was relatively low (prevalence 3.3%, 1 specimens/fish). On the other hand, the parasite species was determined especially on small and medium host fish sizes (2.17-100%). Basic criteria for the assessment of the parasite species of host fish were the general parameters related to parasite populations, which are prevalence, mean intensity, seasonal variation, and relationship between host size and infection.

Parasites as indicator of fish behaviour

In the present study two species of gobies, Pomatoschistus microps and P. minutus from southwest Wales were studied and appearance of some unusual parasite of gobies, were used as an indicator for fish behaviour. The occurrence of pleurocercoids of Ligula intestinalis in the body cavity of these fish and Proteocephalus sp., excysted metacercariae and adult of Timoniella spp., excysted metacercariae of Bucephalusbaeri, the excysted metacercariae of Podocotyle atomon and progenetic adult of Bucephaloides gracilescens in their gut indicate host anadromous, cannibalistic and scavenging behaviour.

The occurrence of the tapeworm Ligula intestinalis (L.), in Barbus paludinosus from a small dam in Zimbabwe

Cestode parasites were collected from Barbus paludinosus from Munwahuku Dam near Harare, Zimbabwe over a period of 13 months. Plerocercoids of Ligula intestinalis were found in 7.2% of the fish. The majority of the infected fish carried one parasite, with 3.1% having two and 1.6% with three. There was a positive correlation (r = 0.59, P < 0.05) between the weight of L. intestinalis and that of their host, but there was no significant relationship between the condition factor of the fish and the weight of the parasite, and the parasite index was low (7.97 ± 3.38) compared to previous studies in South Africa. The gonads of all infected fish were atrophied. The prevalence of L. intestinalis in B. paludinosus was high between July and September 2000 and low thereafter. There was no clear seasonal variation in the occurrence of the parasite, although the lengthy dry season might have had an effect on the prevalence.

The taxonomic status of Digramma (Pseudophyllidea: Ligulidae) inferred from DNA sequences.

The traditional classification of the ligulid tapeworms into 2 genera, Ligula Bloch, 1782 and Digramma Cholodkovsky, 1914, remains controversial. Molecular data of sequences for the 5' end of the nuclear 28S ribosomal ribonucleic acid (rRNA) gene, the mitochondrial cytochrome c oxidase subunit I (COI) gene, and the nicotinamide adenine dinucleotide dehydrogenase subunit 1 (ND1) gene, as well as the first internal transcribed spacer (ITS1) of the nuclear ribosomal deoxyribonucleic acid (DNA), were used to characterize Digramma and to investigate its relationship with Ligula. Digramma spp. exhibited identical sequences with Ligula intestinalis both in the 28S rRNA and the COI gene and differed from L. intestinalis by 0.7% in the ITS1 region and 7.4% in the ND1 gene, respectively. A high degree of genetic conservation within 28S ribosomal DNA, COI, ITS1, and even ND1 genes, was found in Ligula and Digramma. The low genetic divergence in the 4 genes between Ligula and Digramma indicates that Digramma is probably not an independent genus. Therefore, it is proposed that Ligula and Digramma should be considered as 2 species within the genus Ligula and the tapeworms of Digramma collected from diverse localities in China belong to the same species. The present study also suggests that ITS1 and ND1 sequences can act as useful genetic markers to distinguish Ligula and Digramma.

Endocrine disruption, parasites and pollutants in wild freshwater fish.

Disruption of the endocrine system has been shown to occur in wild freshwater fish populations across the globe. Effects range from subtle changes in the physiology and sexual behaviour of fish to permanently altered sexual differentiation, impairment of gonad development and/or altered fertility. A wide variety of adverse environmental conditions may induce endocrine disruption, including sub-optimal temperatures, restricted food supply, low pH, environmental pollutants, and/or parasites. Furthermore, it is conceivable that any/all of these factors could act simultaneously to cause a range of disparate or inter-related effects. Some of the strongest evidence for a link between an adverse health effect, as a consequence of endocrine disruption, and a causative agent(s) is between the condition of intersex in wild roach (Rutlius rutilus) in UK rivers and exposure to effluents from sewage treatment works. The evidence to indicate that intersex in roach (and other cyprinid fish living in these rivers) is caused by chemicals that mimic and/or disrupt hormone function/balance in treated sewage effluent is substantial. There are a few parasites that affect the endocrine system directly in fish, including the tape worm Ligula intestinalis and a few parasites from the micropsora phylum. L. intestinalis acts at the level of the hypothalamus restricting GnRH secretion (resulting in poorly developed gonads) and is one of the very few examples where an endocrine disrupting event has been shown to result in a population-level effect (reducing it). It is well established that many parasites affect the immune system and thus the most common effect of parasites on the endocrine system in fish is likely to be an indirect one.

Distribution and biology of Galaxias truttaceus (Galaxiidae) in south-western Australia, including first evidence of parasitism of fishes in Western Australia by Ligula intestinalis (Cestoda)

The freshwater trout minnow, Galaxias truttaceus, is restricted to the small catchments of the Goodga and Kalgan Rivers in Western Australia. Its large geographic separation from populations in south-eastern Australia, and subsequent reproductive isolation and variation in the prevailing environmental conditions, has created marked differences in biology (and morphology) between the eastern and western populations of G. truttaceus. The biology (spawning period, longevity, growth rates, diet and parasitism) of G. truttaceus in the Goodga River is described and then compared with information on the biology of diadromous and landlocked populations in south-eastern Australia (i.e. Tasmania) (see Humphries 1989). In the Goodga River, ca. 34 and 8% of males and females, respectively, attain maturity at the end of their first year, while only four mature males and one mature female 0+ fish were found in the Tasmanian populations. Adults migrate upstream prior to spawning which peaks during April and May. Larvae, which hatch at ca. 6.5thinspmm (cf. 7.5–9.0thinspmm in Tasmania), move downstream into Moates Lake for a few months before re-entering the river. Of the 810 G. truttaceus collected, ca. 53, 34, 10, 2, 1, 0.2 and 0.1% belonged to the 0+, 1+, 2+, 3+, 4+, 5+ and 7+ age classes, respectively. In contrast, the Tasmanian populations have a much higher proportion of older fish. At the end of their first, second and third years, the males on average attain 60, 84 and 95thinspmm total length (TL), respectively, whereas females attain 63, 89 and 103thinspmm TL, respectively at those ages. Only one fish > 140thinspmm TL was captured, which contrasts with the Tasmanian fish, where a substantial proportion are > 140thinspmm TL. The diet of fish > 40thinspmm TL consisted of between 65 and 96% terrestrial fauna (mainly coleopterans and hymenopterans) in the different seasons. Larval fish diets were largely comprised of copepods. The occurrence of the introduced cestode Ligula intestinalis in ca. 7% of G. truttaceus represents the first record of this parasite in Western Australia. It was found to cause gonadal retardation and gross morphological deformities, the latter of which possibly increases the risk of avian predation.

The differential effects ofLigula intestinalis(L.) plerocercoids on host growth in three natural populations of roach,Rutilus rutilus(L.)

Abstract – This study reports the differential effect of the pseudophyllidean cestode,Ligula intestinalis, on the growth rates of three fish populations of the roach,Rutilus rutilus, under field conditions. Here, we show that only one host‐population is affected by parasite‐induced gigantism in the first 2 years of host life. Paradoxically, this increase in fish growth is strongly correlated with the parasitic load in plerocercoid stages, in that only the roach population subjected to the heaviest parasitic pressure shows an enhanced growth of cestode‐parasitized individuals. This host gigantism observed in only one locality is associated with parasite‐induced fish mortality occurring, on average, one year earlier in this fish population when compared to other populations. We discuss the different reasons for this differential parasite effect on growth enhancement across host‐population in natural settings. Whether the growth effects represent an adaptive response by the host or a manipulation byL. intestinalisof the host, remains to be elucidated.

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.

Experimental demonstration of a behavioural modification in a cyprinid fish, Rutilus rutilus (L.), induced by a parasite, Ligula intestinalis (L.)

Behavioural changes in parasitized hosts have been experimentally investigated by comparing the swimming behaviour of roach, Rutilus rutilus, infected by the tapeworm Ligula intestinalis with that of uninfected roach when they were exposed to the same overhead heron stimulus. Before the stimulus was presented, infected fish swam close to the surface and uninfected fish were preferentially found near the bottom of the tank. The stimulus clearly induced a change in the vertical distribution of infected fish only. On the other hand, infected roach were less active than un infected fish before, during, and after the stimulus was presented. Proximate mechanisms of these behavioural changes are discussed. These behavioural differences, i.e., roach surfacing, swimming, and response to stimulus, probably favour the predation of infected roach by avian predators.

A non-destructive morphometric technique to predict Ligula intestinalis L. plerocercoid load in roach ( Rutilus rutilus L.) abdominal cavity

The aim of the present work was to propose a model for the estimation of the endoparasitic load using morphological descriptors easily accessible without killing the animal i.e. non-destructive method. The study was conducted using plerocercoid forms of Ligula intestinalis in its second intermediate host, the roach ( Rutilus rutilus). The Kohonen Self-Organizing Map (non-supervised neural network) made it possible to present the complex data matrix in a two-dimensional space, with individual clusters visualised by the U-matrix method. The six main descriptors were selected and used to build the predictive model, four lateral and two thickness measures. The generalisation ability of the backpropagation algorithm (supervised neural network) is confirmed by a determination coefficient higher than 0.90 between observed and predicted values. The study for the first partial derivatives of the parasitic load with respect to the six morphological variables is used to identify the factors influencing the parasitic load and the mode of action of each factor.

Host manipulation by Ligula intestinalis: accident or adaptation?

Numerous studies have demonstrated that parasites with complex life-cycles can cause phenotypic modifications in their hosts that lead to an increased rate of transmission, and suggest that these modifications are the result of parasitic adaptations to manipulate the host. Little attention is paid, however, to separating the possibility of adaptive host manipulation from incidental (if fortuitous) side-effects of infection. In this study we combine statistical and analytical tools to interpret the impact of the macroparasite Ligula intestinalis L. (Cestoda, Pseudophyllidea) on the behaviour of its intermediate fish host (the roach, Rutilus rutilus L.), using field data on a natural system. Two distinct sets of generalized linear models agree that both the presence and the intensity of infection contribute to a modified behavioural response in the host. This was illustrated by a preference for the lake-edge in infected fish during autumn. Furthermore, the effect of parasites upon their host is heterogeneous with respect to parasite size, with larger parasite individuals having a disproportionate impact. A series of game-theoretic models of adaptive host manipulation illustrate a potential rationale for a size-dependent manipulation strategy in parasites. These findings illustrate the potential complexity and functionality of the impact of L. intestinalis upon its fish host, which together reduce the parsimony of the alternative 'incidental effect' hypothesis.

The three hosts of the Ligula intestinalis (Cestoda) life cycle in Lavernose-Lacasse gravel pit, France

The life cycle of Ligula intestinalis, a pseudophyllidean cestode, was studied in a South-Western French gravel pit. Copepods, fish and piscivorous birds, constitute the hosts necessary for complete parasite development. In order to determine the actual species likely to be responsible for the very high level of parasitism observed, a two-year study was carried out. Our results show that the copepod Eudiaptomus gracilis, the roach (Rutilus rutilus) and the great crested grebe (Podiceps cristatus) were the most favourable hosts for continuation of the parasite life cycle. The study shows how alterations exerted by infective larval stages of L. intestinalis affect the population dynamics of roach.

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 &gt;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.

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.