Behaviour of roach (Rutilus rutilus L.) altered by Ligula intestinalis (Cestoda: Pseudophyllidea): a field demonstration

1. We studied the influence of a cestode parasite, the tapeworm Ligula intestinalis (L.) on roach ( Rutilus rutilus L.) spatial occupancy in a French reservoir (Lake Pareloup, South-west of France).
2. Fish host age, habitat use and parasite occurrence and abundance were determined during a 1 year cycle using monthly gill-net catches. Multivariate analysis [generalized linear models (GLIM)], revealed significant relationships ( P  < 0.05) between roach age, its spatial occupancy and parasite occurrence and abundance.
3. Three-year-old roach were found to be heavily parasitized and their location toward the bank was significantly linked to parasite occurrence and abundance. Parasitized fish, considering both parasite occurrence and abundance, tended to occur close to the bank between July and December. On the contrary, between January and June no significant relationship was found.
4. These behavioural changes induced by the parasite may increase piscivorous bird encounter rate and predation efficiency on parasitized roach and therefore facilitate completion of the parasite's life cycle.     

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

The effects of the plerocercoid of Ligula intestinalis (L.) (Cestoda: Pseudophyllidea) on the major lymphoid organs, the spleen and pronephros, of roach, Rutilus rutilus (L.), and gudgeon, Gobio gobio (L.), are described. The spleen of ligulosed roach showed a significant decrease in weight. Differential cell counts suggested this was due to a reduction in erythrocytes, despite significant increases in macrophages and vacuolated granulocytes. The spleen of gudgeon, which consisted almost entirely of erythrocytes, showed a slight reduction in weight in ligulosed fish. In both roach and gudgeon this decrease was independent of parasite burden. Differential cell counts of the pronephros from ligulosed roach revealed a significant decrease in neutrophils and increase in vacuolated granulocytes. In the pronephros of gudgeon, however, cell counts were unaffected by ligulosis. Ultrastructural observations included an apparent disintegration of vacuolated granulocytes and increased pinocytic activity in specialized endothelial cells in the spleens of ligulosed roach. Also, melano-macrophage centres and melano-macrophages increased in the spleen of ligulosed roach and gudgeon, respectively. The marked changes in spleen weight and differential cell counts in ligulosed roach and lack of such changes in ligulosed gudgeon correlate with the differential response to the parasite by these two fish species.     

Peculiarities of lipid peroxidation indices in Ligula intestinalis (Cestoda: Pseudophyllidea) and its host--Abramis brama (L.)

A comparative analysis of indices of peroxidation lipids in tissues of Ligula inteslinalis plerocercoids and in the intermediate fish host, the bream Abramis brama, was performed for the content of common lipids (CL), malonate di-aldehyde (MDA), which is a product of lipid peroxidation (POL), and common antioxidate activity (CAA). The dependence of indices upon size of parasites is recovered. The long-sized parasites had higher rate of MDA and intense CAA. The higher rate of MDA and low one of CAA was observed in the infected fishers comparing to the healthy ones.     

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 .     

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

Reproductive 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.     

The effects of a change in the growth rate of roach, Rutilus rutilus (L.), on the biology of the fish tapeworm Ligula intestinalis (L.)

Investigations into the biology of the roach and the pathogenic tapeworm Ligula intestinalis (L.) populations at Slapton Ley, Devon were carried out between October 1982 and December 1984. Data collected from the lake since 1977 have also been re-analysed to determine how the dramatic improvement in the individual growth rate of the roach over this period may have affected the growth, maturation and life-cycle of Ligula. Only the very young roach at this site become infected, so it was possible to follow cohorts of plerocercoids of similar age through each roach year class. Results for the 1978 and 1983 year classes are presented in detail. The roach grew extremely rapidly from May to August in each year, resulting in a pronounced cyclical pattern of changes in the condition of the roach, with the lowest condition occurring in late winter and spring. The yearly increase in the roach growth rate was accompanied by an increase in plerocercoid growth rate in the 0 + roach, but not in the 1 + roach. The growth rate of the plerocercoids was very high compared to that at other sites. It is usual for the parasite index (PI) of Ligula-infected fish to be high and to increase throughout their first few years of life. At Slapton, however, a lack of multiple infections has prevented high PIs from occurring, and in recent years the growth rate of the roach has been so high that the plerocercoids were unable to maintain a high weight relative to the fish, and the highest PIs occurred in the 0 + roach throughout late winter and spring. In recent year classes, therefore, the maximum PIs and highest pathogenicities coincided with the period of lowest condition in the 0+ roach. Observations of both caged and natural populations of 0+ roach over winter showed that a significant loss of roach containing the larger plerocercoids occurred from the population. In vitro cultivation of Ligula plerocercoids showed that they were capable of maturation at weights of 0.5 g, and only 6 months after having infected the roach. The increase of the growth rate of the plerocercoids in the 0+ roach has therefore resulted in a greater proportion of these plerocercoids being capable of infecting the definitive host. As a result of the increase in individual growth rate of the roach at Slapton, the potential for Ligula transmission, as measured in terms of both their pathogenicity and maturity, has shifted from the 1 + to the 0+ roach.     

Isolation and characterization of microsatellite loci in the tapeworm Ligula intestinalis (Cestoda: Pseudophyllidea)

Ligula intestinalis is a species with a complex biology. Several strains, distinct in the host specificity and biogeography, are supposed to exist; however, their morphological or molecular identification remains unresolved. We describe the isolation of 16 polymorphic microsatellite markers. The number of alleles ranged from four to 14 in a population of 21 L. intestinalis individuals. Loci showed amplification success across samples of worldwide distribution. A cross‐amplification of 14 markers in Digramma interrupta (Cestoda: Pseudophyllidea) was observed.     

Histochemical characterization of myotomal muscle in the roach, Rutilus rutilus (L.)

A histochemical study of the myotomal muscles in the roach revealed three main muscle regions: red, intermediate and white. These were distinguished on the basis of glycogen content, succinate dehydrogenase (SDH), and myofibrillar ATPase (mATPase) activity. Except for the red fibre region, none of these described regions is homogeneous. The principal new findings are the toniclike fibre, the presence of a transitional zone with two fibre types, and the mosaic organization of the white fibre region. The significance of this type of myotome architecture in relation to the locomotion of the species is discussed.     

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.     

Sperm quality, secondary sexual characters and parasitism in roach (Rutilus rutilus L.)

According to sperm competition models, a male spawning in a disfavoured role should have spermatozoa with higher velocity but shorter longevity compared with a male spawning in a favoured role. Moreover, immunosuppressive androgens are needed to produce both secondary sexual characters and sperm cells. The 'sperm protection' hypothesis suggests that the immunosuppressive action of androgens has evolved to protect haploid spermatozoa, which are antigenic, from autoimmune attacks. Therefore, a male with high sexual ornamentation may be more susceptible to diseases but may possess better quality ejaculate than his less ornamented rival. We studied sexual ornamentation (breeding tubercles), ejaculation quality (sperm concentration, longevity and spermatozoal velocity) and intensity of parasitism in the cyprinid, Rutilus rutilus . Sperm longevity and spermatozoal velocity were positively correlated. Males having elaborated sexual ornamentation had longer-lived sperm and more Myxobolus mülleri parasites in the liver compared with males with low ornamentation. However, no difference was found between males with different degrees of ornamentation with respect to sperm concentration, spermatozoal velocity or other parasites. Since the highly ornamented males had higher sperm longevity, the present results are partly consistent with the predictions of the sperm competition models and the 'sperm protection' hypothesis.  © 2004 The Linnean Society of London, Biological Journal of the Linnean Society , 2004, 81 , 111–117.     

Ontogenetic changes in haemoglobins in roach, Rutilus rutilus (L.) and rudd, Scardinius erythrophthalmus (L.)

The haemoglobins and globins of the roach, Rutilus rutilus (L.) and the rudd, Scardinius erythrophthalmus (L.) have been studied by starch gel electrophoresis. At all stages of development studied, the roach and rudd haemoglobins give a similar electrophoretic pattern, the young fish of about 2 cm standard length possessing three separate haemoglobins, of which two bands only persist in the adult. The evolutionary significance of multiple haemoglobins in fishes is briefly discussed.     

The morphology and histology of the pineal organ in roach, Rutilus rutilus (L.)

The pineal organ in the roach, Rutilus rutilus (L.), is covered by a semi-transparent area, the pineal window. Beneath this the pineal is attached to a long robust stalk, lying just under the parietal bone. The pineal is attached to the brain through the dorsal sac. Three cell types have been identified histologically. These are the sensory cells, supporting cells and the ganglia cells. The inner segment of the sensory cells respond to PAS and AF staining, while the remaining cells respond to Orange G, LG, or Acid Fuchsin. The evidence suggests that the roach pineal may have a dual photosensory and glandular function.     

Studies on Ligula intestinalis (L.) effects on a roach population in a gravel pit

The effects of the plerocercoids of Ligula intestinalis were studied on a population of roach, Rutilus rutilus in a gravel pit. The incidence of the cestode fell from 92% in 0+ roach in April to 25 % in January of the succeeding year. The fall in the number of parasitized fish was due to predation, mainly by pike, Esox lucius. Observations indicated most of the parasitized fish failed to become sexually mature although the actual growth rate of the fish was not markedly reduced. The plerocercoids of L. intestinalis grew more rapidly during the summer. The author recommends roach of less than 9 months of age should not be introduced into confined water such as a gravel pit, since after this period they appear to be much less likely to be parasitized.     

Changes in roach (Rutilus rutilus L.) population structure induced on draining a large reservoir

The influence of draining a large reservoir (Pareloup, South of France) on the population structure and the growth of roach is studied in this work. This reservoir, with an area of 13 km², drained in June 1993, was refilled 2 months later. Fish were sampled monthly before draining (1981) and after refilling (1997) by nylon monofilament gill nets used at the same catching effort for both periods. This permitted a comparison to be made between the density of roach and length distribution before and after refilling. Changes in growth were determined by scalimetry. The observed difference in population structure and growth underlined that the differences are mainly due to a greater growth rate after refilling during the first 2 years of roach life. These growth changes are explained by the decrease in roach density and the increase in 1993 of the biomass of Zooplankton, which constitute the main feeding resource for 0⁺ and 1⁺ roach. The study led us to propose hypotheses on the ecological significance of growth changes induced by refilling, which can be considered as a rejuvenation of the aquatic ecosystem.     

Digestive processes during the development of the roach, Rutilus rutilus L.

During development of the roach from larvae to adults relative gut length increases from 44 to 104% of the body length. Gut passage rate correlates with gut length, ranging from 2.25 h in larvae to 6.2 h in adults (at 20 ± 1°C). In controlled experiments (20°C, feeding on carp diet) tryptic activity of the gut content increases with the age of the fish. In larvae artificial diet leads to considerable increase of tryptic activity, but to low growth rate and finally to total mortality. The reabsorption of digestive enzymes in the hindgut is efficient only in adults in which tryptic activity in the second half of the intestine is reduced to about 12% of total activity.     

Occurrence of an intersex condition in the roach Rutilus rutilus (L)

The roach, Rutilus rutilus , is normally a dioecius species. During an experimental study of reproduction in this species, a condition of apparently functional intersex was discovered. Anatomically the gonad was a testis, exhibiting various normal stages of spermatogenesis. A group of oocytes was found during the microscopical examination of the gonad, interspersed between lobules of normal testicular tissue. A few small oocytes were found to be in the chromatin-nucleolus stage, while the rest were in the perinucleolus stage. In addition, some large oocytes with an average diameter of 40 μm were randomly distributed among the lobules of the testis.