Endocrine effects of the tapeworm Ligula intestinalis in its teleost host, the roach (Rutilus rutilus)

SUMMARYThe effects of parasite infection by the cestode Ligula intestinalis on the reproductive function and endocrine system of wild roach Rutilus rutilus were evaluated. Gonad maturation, plasma vitellogenin, plasma steroid concentrations (i.e. progesterone, 11-keto-testosterone and 17-β-estradiol) and brain aromatase activity were investigated in relation with parasitization. A low prevalence (8%) of ligulosed roach and a moderate impact of parasitization (mean parasitization index of 8·8%) were found in the studied population. Inhibition of gonad maturation generally resulted from infestation but 5% of the ligulosed roach nevertheless reached maturity. Main sex steroid plasma content was depleted in both genders. Male 11-keto-testosterone, female 17-β-estradiol and progesterone plasma concentrations of both genders were, respectively, 27, 5 and 3 times lower in ligulosed fish when compared to their non-infected counterparts. Progesterone levels were negatively correlated with the parasitization index in females. Brain aromatase activity of infected roach was reduced to 50% of that of the non-infected fish. These results demonstrate significant negative effects on the reproductive function of wild roach infected by the tapeworm L. intestinalis collected from a site with low contamination.

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

Parasitology ◽

10.1017/s0031182010001514 ◽

2010 ◽

Vol 138 (5) ◽

pp. 648-659 ◽

Cited By ~ 9

Author(s):

ACHIM TRUBIROHA ◽

HANA KROUPOVA ◽

SABRINA N. FRANK ◽

BERND SURES ◽

WERNER KLOAS

Keyword(s):

Steroid Receptors ◽

Gonadosomatic Index ◽

Plasma Concentrations ◽

Secondary Growth ◽

Parasite Burden ◽

Rutilus Rutilus ◽

Roach Rutilus Rutilus ◽

Infected Female ◽

Ligula Intestinalis ◽

Laboratory Conditions

SUMMARYReproductive 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.

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Influence of Ligula intestinalis plerocercoids (Cestoda: Diphyllobothriidea) on the occurrence of eyeflukes in roach (Rutilus rutilus) from a lake in south-east England

Journal of Helminthology ◽

10.1017/s0022149x17001213 ◽

2018 ◽

Vol 93 (1) ◽

pp. 66-70 ◽

Cited By ~ 2

Author(s):

N.J. Morley ◽

J.W. Lewis

Keyword(s):

Rutilus Rutilus ◽

Body Cavity ◽

Infected Fish ◽

Fish Host ◽

Helminth Species ◽

Roach Rutilus Rutilus ◽

Ligula Intestinalis ◽

Freshwater Habitats ◽

Concurrent Infections ◽

South East England

AbstractVertebrate hosts commonly harbour concurrent infections of different helminth species which may interact with each other in a synergistic, antagonistic or negligible manner. Direct interactions between helminths that share a common site in the host have been regularly reported, but indirect interactions between species that occur in different sites are rarely described, especially in fish hosts. Plerocercoids of Ligula intestinalis are common infections of the peritoneal (body) cavity of roach (Rutilus rutilus) in freshwater habitats. These larval cestodes can cause extensive systemic pathologies to the fish host, which in turn may alter its susceptibility as a target host for other helminth species. The present study, using an existing dataset, investigates the influence of L. intestinalis (ligulosis) on frequently occurring eyefluke infections in roach sampled from a lake in south-east England. The occurrence of two species of eyefluke (Diplostomum sp. and Tylodelphys sp.) in the roach population demonstrated no significant levels of interaction with each other. The prevalence but not mean intensity or abundance of Diplostomum sp. was significantly increased in ligulosed roach, while the incidence of Tylodelphys sp. remained unchanged. Analyses of bilateral asymmetry in the occurrence of eyeflukes in left and right eyes of infected fish demonstrate that Tylodelphys sp. shows significant asymmetry in non-ligulosed roach, which is not replicated in ligulosed individuals. In contrast, Diplostomum sp. shows no evidence of asymmetry in either ligulosed or non-ligulosed fish.

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

Canadian Journal of Zoology ◽

10.1139/z02-043 ◽

2002 ◽

Vol 80 (4) ◽

pp. 738-744 ◽

Cited By ~ 19

Author(s):

Géraldine Loot ◽

Stéphane Aulagnier ◽

Sovan Lek ◽

Frédéric Thomas ◽

Jean-François Guégan

Keyword(s):

Rutilus Rutilus ◽

Infected Fish ◽

Experimental Demonstration ◽

Roach Rutilus Rutilus ◽

Ligula Intestinalis ◽

Behavioural Changes ◽

Proximate Mechanisms ◽

Behavioural Modification ◽

Avian Predators ◽

The Vertical Distribution

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.

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

Veterinarski glasnik ◽

10.2298/vetgl0402127o ◽

2004 ◽

Vol 58 (1-2) ◽

pp. 127-133 ◽

Cited By ~ 1

Author(s):

Cemal Oguz ◽

Öztürk Oguz ◽

Hayati Güre

Keyword(s):

Seasonal Variation ◽

Parasite Species ◽

Abdominal Cavity ◽

Rutilus Rutilus ◽

The Other ◽

Host Fish ◽

Roach Rutilus Rutilus ◽

Mean Intensity ◽

Ligula Intestinalis ◽

Irrigation Pond

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.

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

Journal of Fish Biology ◽

10.1111/j.1095-8649.1989.tb03337.x ◽

1989 ◽

Vol 34 (4) ◽

pp. 583-596 ◽

Cited By ~ 20

Author(s):

M. Taylor ◽

D. Hoole

Keyword(s):

Rutilus Rutilus ◽

Roach Rutilus Rutilus ◽

Ligula Intestinalis ◽

Induced Changes

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Host switch and infestation by Ligula intestinalis L. in a silver bream (Blicca bjoerkna L.) population

Parasitology ◽

10.1017/s003118201100206x ◽

2012 ◽

Vol 139 (3) ◽

pp. 406-417 ◽

Cited By ~ 6

Author(s):

M. VANACKER ◽

G. MASSON ◽

J-N. BEISEL

Keyword(s):

Gonadosomatic Index ◽

Rutilus Rutilus ◽

Condition Index ◽

Gonad Maturation ◽

Host Switch ◽

Ligula Intestinalis ◽

Fat Reserves ◽

Host Sex ◽

Significant Difference ◽

The Impact

SUMMARYSampling 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.

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Host manipulation by Ligula intestinalis: accident or adaptation?

Parasitology ◽

10.1017/s0031182001008678 ◽

2001 ◽

Vol 123 (5) ◽

pp. 519-529 ◽

Cited By ~ 26

Author(s):

S. P. BROWN ◽

G. LOOT ◽

B. T. GRENFELL ◽

J. F. GUÉGAN

Keyword(s):

Linear Models ◽

Rutilus Rutilus ◽

Infected Fish ◽

Life Cycles ◽

Fish Host ◽

Host Manipulation ◽

Ligula Intestinalis ◽

Game Theoretic ◽

Effect Hypothesis ◽

The Impact

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.

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Ligulaintestinalis infection is associated with alterations of both brain and gonad aromatase expression in roach (Rutilusrutilus)

Journal of Helminthology ◽

10.1017/s0022149x10000660 ◽

2010 ◽

Vol 85 (3) ◽

pp. 339-344 ◽

Cited By ~ 4

Author(s):

C. Boulange-Lecomte ◽

P. Geraudie ◽

J. Forget-Leray ◽

M. Gerbron ◽

C. Minier

Keyword(s):

Quantitative Polymerase Chain Reaction ◽

Gonadosomatic Index ◽

Gonad Development ◽

Endocrine Disrupting Compounds ◽

Infected Fish ◽

Aromatase Activity ◽

Aromatase Expression ◽

Brain Aromatase ◽

Functional Relevance ◽

The Brain

AbstractThe tapeworm Ligulaintestinalis commonly infests roach (Rutilusrutilus) and is responsible for the inhibition of gonad development. In order to better understand the effect of the plerocercoid on fish physiology, and to discriminate parasitization effects from those of endocrine-disrupting compounds (EDC), Cyp19b and Cyp19a aromatase expression was investigated by real-time quantitative polymerase chain reaction (PCR) in brain and gonads of ligulosed roach, caught from a reference site. Data were compared to reproductive and endocrine endpoints previously reported in a larger cohort study (including the sampled population of the present one), such as gonadosomatic index, Fulton index, gonadal histology, plasma sex steroid levels and brain aromatase activity. A decrease in Cyp19b expression in the brain of infected fish was demonstrated, in agreement with the reduction of aromatase activity previously described. In contrast, Cyp19a expression in the gonads appeared to be enhanced in ligulosed fish, in accordance with the presence of immature but differentiated sexual tissues. Together these results show that: (1) L. intestinalis infestation results in an alteration of aromatase expression which, in particular, may have profound effects on the fish brain; and (2) L. intestinalis infection must be considered as a major confounding factor in ecotoxicological studies using aromatase expression as an EDC biomarker. Moreover, the concordance between activity and expression – investigated for the first time in the same population – gives a functional relevance to the transcript aromatase dosage in the brain. Finally, quantitative PCR was confirmed as a sensitive approach, enabling aromatase status to be defined in the poorly developed gonads of ligulosed individuals.

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