The tapeworm Ligula intestinalis (Cestoda: Pseudophyllidea) inhibits LH expression and puberty in its teleost host, Rutilus rutilus

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 host gonadal development. The mechanism by which infected fish are prevented from reproducing is unknown. Comparison of parameters, such as body length and weight, and condition factor and age, between infected and uninfected individuals, indicated only minor effects of parasitism on growth and condition. In contrast, seasonal gonadal development, as observed in uninfected fish, did not occur in infected fish, and gonads remained small and blocked at the primary oocyte stage in female roach. As immature ovaries and testes are still present, the parasite is presumed to act upon the brain -pituitary -gonadal axis of the fish to inhibit further development of reproductive organs. We investigated the Ligula/fish interaction at the level of the pituitary gland by determination of gonadotrophin (LH) content using a heterologous RIA for carp (Cyprinus carpio) LHb subunit. The results indicated that the pituitary glands of infected roach contained approximately 50% less LH than non-infected fish. After the cloning and sequencing of roach LHb subunit, we measured roach LHb mRNA levels by real-time RT-PCR. A corresponding 50% reduction in LHb mRNA pituitary levels was determined. These results reflect a significant and measurable effect of parasitism on the pituitary gland, and lend support to the hypothesis that excretory/secretory products released from the parasite interact with the brain -pituitary -gonadal axis of the fish host and thus inhibit gonadal development. Reproduction (2005) 130 939-945 IntroductionPrevious studies have revealed that several parasitic infections can affect host reproduction. For example, Joose & van Elk (1986) noted that Trichobilharzia ocellata induces gigantism and the cessation of egg production in its molluscan host, a snail Lymnea stagnalis, and Crews & Yoshino (1989) observed that Schistosoma mansoni similarly suppresses reproduction and gonadal growth in another snail species, Biomphalaria glabrata. Furthermore, in vertebrate hosts, Taenia taeniaeformis appears to directly affect the testis in the rat (Lin et al. 1990) and Taenia crassiceps induces feminisation in infected mice (Larralde et al. 1995).Ligula intestinalis, which 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.g. Arme & Owen 1968, Mahon 1976, Sweeting 1977, Bean & Winfield 1989, the mechanism of the action of this parasite remains unknown. Previous studies have indicated effects of infection at the pituitary gland level. Kerr (1948) and Arme (1968) noted that in ligulosed roach, Rutilus rutilus, the putative gonadotrophs are much reduced in number, compared with non-ligulosed individuals, are only lightly granulated, and have an irregular nucle...

THE OCCURRENCE OF Ligula intestinalis IN ITS FISH HOST Rutilus rutilus (L.) AND THE EFFECTS OF PARASITE ON THE FISH GROWTH (BÜYÜKÇEKMECE RESERVOIR, TURKEY)

“…Also, many researchers have studied some effects of this parasite for fish host such as growth, endocrine system, gonadal development and had determined that L. intestinalis was caused many pathogenic effect on host fish. The parasite can cause damage to the host fish specimens especially by compression and atrophy of vital organs including the gonads, liver in the coelomic cavity of the infected fish (Öztürk and Altınel, 2001;Jopling and Taylor, 2003;Oğuz et al, 2004;Carter et al, 2005;Hecker and Karbe, 2005;Dejen et al, 2006). Similarly, in present study, macroscopic investigations showed that stomachs of fish specimens were swollen and gonads were deformed.…”

“…According to Williams and Hoole (1992), numerous ecological and pathological studies have revealed that the parasite can seriously affect the population dynamics of both wild fish and those involved in aquaculture. There is limited data on relation of the parasite and its fish host R. rutilus (Kennedy and Burrough, 1981;Loot et al, 2001;Oğuz et al, 2004;Carter et al, 2005). The aim of the present study is to determine the occurrence of the parasites on host and investigate the effects of parasite for condition and length-weight relationship of host fishes living in Büyükçekmece Reservoir.…”

Impact ofBothriocephalus acheilognathi(Cestoda: Pseudophyllidea) onCyprinella lutrensisCondition and Reproduction

“…Tapeworm infections in the three-spined stickleback (Gasterosteus aceleatus) did impact fish reproduction and was manifested as a decrease in ovum mass (Heins and Baker 2003). Carter et al (2005) reported decreases in condition, gonadal development, and a reduction of almost 50% in gonadotropin concentration in roach, Rutilus rutilus. Laboratory experimentation is needed to fully assess the impact of B. acheilognathi on cyprinid reproduction in order to account for the above mentioned confounding variables.…”

Feminization and reduction of testicular weight in mouse sparganosis

“…In the present study, we observed variations of testicular weight instead of the sexual behaviors of sparganuminfected mice. Recently, the loach (Rutilus rutilus) infected with a pseudophyllidean tapeworm, Ligula intestinalis, showed approximately 50% less gonadotropin (LH) contents than non-infected fish and its negative effects on gonadal development in infected fish (Carter et al, 2005). Therefore, the present results suggest that the sparganum, i.e., a larval stage of pseudophyllidean tapeworm, may interact with the brain-pituitary-gonadal axis and affect gonadal development of the mouse host.…”