J Parasitol. Aug;75(4) Changes in numbers and growth of Ligula intestinalis in the spottail shiner (Notropis hudsonius), and their roles in. Abstract. The tapeworm Ligula intestinalis occurs in the body cavity of its cyprinid second intermediate host, in this study the roach Rutilus rutilus, and inhibits. Since its use as a model to study metazoan parasite culture and in vitro development, the plerocercoid of the tapeworm, Ligula intestinalis, has.

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Previous studies have revealed that several parasitic infections can affect host reproduction. Furthermore, in vertebrate hosts, Taenia ontestinalis appears to directly affect the testis in the rat Lin et al.

Ligula intestinaliswhich is found in the body cavity of certain cyprinid fish, inhibits reproduction in both male and female fish. The gonads, however, are present but remain in an immature state, irrespective of fish age or season. Although this phenomenon has been reported several times e. Previous studies have indicated effects of infection at the pituitary gland level.

Kerr and Arme noted that in ligulosed roach, Rutilus rutilusthe putative gonadotrophs are much reduced in number, compared with non-ligulosed individuals, are only lightly granulated, and have an irregular nuclear membrane, no prominent nucleolus and a marked reduction in the cytoplasmic volume.

Ligula intestinalis – Wikipedia

These studies have led to the belief that the effects of Ligula on gonadal development may be mediated through the pituitary gland. The effects noted in the wild are reproducible with a small plerocercoid implanted into a large mature fish, which precludes pressure effects on fish organs or general debilitation from parasite metabolic demands Arme In addition, analogous effects have been shown when L. In this study, our objective was to establish whether gonadal inhibition induced by Ligula in its primary fish host, Rutilus rutilusis mediated through effects on pituitary gland hormone levels, i.

Ligulosed and non-ligulosed roach were collected from the Altami Angling Club, Chester, Cheshire, UK during — at three times during the reproductive year: February leading up to spawning in springAugust post spawning intestinalid December mid cycle.

Fish used for hormonal ihtestinalis molecular biological analysis were examined within 7 days of capture.

WoRMS – World Register of Marine Species – Ligula intestinalis (Linnaeus, ) Gmelin,

A subset of four non-infected female fish from each group was used for histological analysis of gonadal development and two categories of oocytes were observed, i. Because of the lack of sequence data available for roach, fragments of LH and the control gene 18S ribosomal RNA were amplified and sequenced to identify specific primers for use in real-time PCR. The following degenerate lgula were used: As an internal control, 18S rRNA was amplified in an identical intesinalis.

Data were analysed using the Abi Prism sequence detection system Applied Biosystems. Transcript levels were normalised to those of 18S rRNA and data for infected fish presented as a fold change relative to the values obtained for non-infected fish.

Correlations between body parameters were subjected to regression analysis. Details of fish used and effects of parasitism are shown in Table 1. While roach were caught up to 54 g in weight, fish exceeding 20 g were not infected ligupa Ligula Fig. However, because of ihtestinalis low sample size in certain age classes of infected fish, body lengths were considered according to age class, and differences were less apparent.

Further analysis of the — cohort of fish also revealed a similar trend in the association with parasitisation and growth parameters.

Young infected roach, 2 and 3 years old, rarely attained the same body weight as their non-infected counterparts mean body mass: As with length, in 4 year-old fish there was no statistically significant difference between the body mass of infected and non-infected individuals infected 8. The condition factor assumes that heavier fish of a given length are in better condition and eliminates variation attributable to gonadal development over the reproductive season.

Because of the very small amount of gonadal tissue present in infected fish, and thus the problem of finding and confirming the presence of gonads without histological examination, the condition factor was calculated including the gonadal tissue in parasitised individuals.

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Figure 2 shows the condition factor of fish according to age, showing lower K values in infected fish, reflecting the fact that non-infected individuals are in better condition, irrespective of age, than their infected counterparts. Because of the small amount of gonadal tissue in infected roach weighing less than 0. Natural variations were found within the sampled population, i. GSI leading up to spawning February varied between 0. The majority of non-infected fish achieved sexual maturation by 2 years of age as determined by the presence of yolky oocytes and all non-infected females were mature by 3 years of age.

In non-infected females, the ovaries contained large, mature eggs and several smaller, primary oocytes with only immature stages of development occurring post spawning. In contrast, in infected fish, only these immature stages of oogenesis were present throughout and no cyclical variations were recorded see Arme Further quantification was performed in sections of the ovaries to determine the extent of oocyte development.

The use of a heterologous assay for carp LH was fully justified in view of the high level of sequence identity of the roach molecule see below. Although individual variation was high, LH content of non-infected individuals was at its peak post-spawning August and lowest over the winter period December; Fig.

In order to do this, fragments of the R. The fragments and nucleotides respectively obtained were cloned and sequenced Genbank accession numbers: Our results have confirmed previous observations made by Armeon the biometric effects of Ligula intestinalis on its roach intermediate host. Importantly, it also revealed that the roach—parasite interaction under investigation is typical of that found in other sampled populations.

In addition, GSI recorded in this infection suggested that non-infected host populations were undergoing normal reproductive cycles. Ligula intestinalis could affect reproductive development of the fish at any level of the reproductive axis, from the first key hormones, gonadotrophin-releasing hormones GnRHto the gonads.

For example, the expression of gonadotrophin hormones and their receptors e. Furthermore, peripheral stimulators and inhibitors, active at all levels of the brain—pituitary—gonadal BPG axis, may be targets of the putative hormonal disruption by Ligulawhich results in an inability of the gonads to respond to hormonal signals. As has been noted previously by Kennedy et al. The fact that this inhibition was not observed when we compared older fish may arise from the negative effect of sexual maturation on growth and condition e.

Indeed, sexual maturation will occur every year in non-infected fish but not in infected ones. This may explain why the growth curves of infected and non-infected fish become more similar in older fish. As in other vertebrates, body growth and condition have been suggested to act as triggers for the initiation of puberty in fish, although the mechanisms by which such a trigger is initiated is still largely unknown for reviews see Peter et al.

In the roach, our data also showed that Ligula infection exerts some inhibitory effects on body growth and condition, but these effects are small and would, therefore, not account for the complete blockade of puberty noted in ligulosed fish.

The reproductive system in fish is particularly susceptible to stress and immediate cessation of reproductive function is not uncommon when fish are brought into captivity Wendelaar Bonga It may not be surprising, therefore, that the presence of a large parasite burden, which could be considered as a potent stressor, resulted in the observed dramatic effects on host reproduction.

However, the relationship between Ligula and the induction of a possible stress effect on its fish host has been recently questioned by the work of Loot et al. Previous observations have revealed that two GnRH forms salmon and chicken occurred in the brain of non-infected and infected roach Williams et al.

The distribution, cell number and staining intensity of both these types of neurones, which are considered to be the first steps in BPG axis activation, were not affected by Ligula Penlington et al. However, seasonal variations in GnRH cell activity in non-infected fish were not investigated, and it cannot therefore be deduced that GnRH cells or GnRH release are not affected in infected fish. Whilst it is true that gonadotrophs are much reduced in number, the cells that are present do appear to be functional, indicating that Ligula infection neither completely prevents gonadotroph differentiation nor basal activity.

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However, seasonal variations in pituitary LH content observed in non-infected fish were absent in infected roach. This suggested that Ligula infection decreases LH synthesis by inhibiting its expression and indicates that the levels of gonadotrophin-producing cells being affected by parasitisation are critical to normal reproductive function. Further studies are required to ascertain the mechanisms by which Ligula induces its inhibitory effect on roach LH production.

Given that fish infected with Ligula intestinalis do not exhibit normal behaviour patterns in terms of shoaling e. Orrpheromonal stimuli which would normally be received within the group-shoaling situation are absent from infected individuals, which may enhance the delay in puberty Francis et al. This abnormal behaviour may also expose roach to different light intensities, a parameter vitally important in the control of the reproductive cycle in fish Bromage et al.

Ligula infection could also affect LH production by acting directly on the gonadotrophs. However, an apparently increased LH production in the eel suggested possible species differences in the action on gonadotroph activity.

Although this effect was dose dependent, significant differences were found between Ligula and a related tapeworm species, Schistocephalus solidus.

This not only supports the hypothesis by Arme that reproductive inhibitory effects are specific to Ligulabut also suggests that effects of the parasite extend to non-host species e. The latter has been demonstrated in other cyprinids where positive and negative responses have been noted for GnRH and dopamine respectively for review see Peter et al.

Investigations of the effect of Ligula on the production of the other gonadotrophin follicle-stimulating hormone are also required, especially considering the potential effect of the parasites on the early stages of gametogenesis. We have also demonstrated that infected roach have a decreased condition factor, weight, length and gonadal development with respect to their age- and season-matched uninfected counterparts.

In addition, we have for the first time revealed that the LH pituitary content and mRNA levels are also significantly decreased in infected individuals. Although the mode of action of the parasite remains elusive, it is clear that the pituitary gland morphology and gonadotrophic hormone production are affected by the parasite.

Whether this is mediated by direct effects of Ligula products or general endocrine disruption requires elucidation. Table 1 Data summary for all experimental fish. Figures given are means with range. Fish exceeding 20 g were not infected with Ligula. Reproduction6; Comparison of body mass to condition factor of ligulosed and non-ligulosed roach. Infected fish have lower K values, reflecting a lower body growth rate.

Ligula intestinalis

The sample size is shown above each bar. Introduction Previous studies have revealed intestinalsi several parasitic infections can affect host reproduction. Materials and methods Fish Ligulosed and non-ligulosed roach were collected from the Altami Angling Club, Chester, Cheshire, UK during — at three times during the reproductive year: Results Parasite burden Details of fish used and effects of parasitism are shown in Table 1. Effects of parasitism on host: Gonadal development Because of the small amount of gonadal tissue in infected roach weighing less than 0.

Discussion Our results have confirmed previous observations made by Armeon the intestinali effects of Ligula intestinalis on its roach intermediate host.

Download Figure Figure 2 Comparison of ligulw mass to condition factor of ligulosed and non-ligulosed roach.

I, infected fish; NI, non-infected fish; F, female; M, male.