Biological and ecological effects of a Ligula intestinalis (L.) infestation of the gudgeon, Gobiogobio (L.), in Lough Neagh, Northern Ireland

A study was made of the effects of a Ligula intestinalis infestation on the biology and distribution of gudgeon in Lough Neagh, Northern Ireland. During the summer months, when the majority of the gudgeon population was restricted to the inshore areas of the lough, Ligula was present in all age (size) classes of the host although levels of infestation were highest in the oldest individuals. While there was no significant effect on the length-weight relationship of the gudgeon, the presence of the parasite did adversely affect gonad size in both sexes. Ligula also influenced the distribution of the gudgeon population by decreasing the swimming depth of infested individuals and by delaying their autumnal migration to the deeper offshore parts of the lough.     

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

Sampling 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.     

Compared parasitic infection of Ligula intestinalis (Cestoda: Diphyllobothridae) in Cyprinidae species: Rutilus rubilio and Scardinius erythrophthalmus in two dam reserves in Tunisia

Monitoring quantitative parameters of parasitism by ligula intestinalis (Cestoda: Diphyllobothridae) was performed by examining 516 fish belonging to two introduced freshwater species: Rutilus rubilio (350 individuals) and Scardinius erythrophthalmus (166 individuals). These fish were collected in two dam reserves in Tunisia, Sidi Salem and Nebhana. The analysis of the aquatic bird's composition in these two reserves revealed the existence of piscivorous bird species that were previously reported as final host of Ligula. Monitoring the bird's composition highlighted higher relative abundance and frequency in Sidi Salem than in Nebhana dam reserve. The analyses of the prevalence, mean intensity and abundance of the parasite revealed the most important values in roach, Rutilus rubilio which seems to be the preferential second intermediate host of the parasite Ligula intestinalis in these environments. Comparative analysis of parasitism in both explored sites suggests that Ligula intestinalis presents two different strategies of infestation. In Sidi Salem reserve, which is larger than Nebhana and containing on important and diversified piscivorous species, the parasite infects a maximum of host individuals with low parasite mean intensity values. However, at Nebhana, which is a smaller reserve, the parasite infects fewer individuals than Sidi Salem but with higher mean intensity. The highest prevalence values were recorded in large size classes of roach species in Sidi Salem reserve.     

Parameters of the blood and immune system of Rutilus rutilus lacustris (Cypriniformes: Cyprinidae) during an invasion with pleurocercoids of Ligula intestinalis (Pseudophyllidae: Ligulidae)

The morphological composition of blood and the reaction of the immune system in a Siberian roach Rutilus rutilus lacustris (Baikal, Chivyrkuiskii Bay) both infested and not infested with pleurocercoids of Ligula intestinalis is investigated. An infestation with L. intestinalis renders a negative effect on the morphological and immunological parameters of blood supporting the immunological homeostasis of its host. In comparison with individuals not infested, the following changes are recorded in the infested individuals: a decrease in the count of erythrocytes and leukocytes (due to a decrease in lymphocytes), increase of the quantity of foam cells, inhibition of T-lymphocytic link of immunity, and a decrease in the content of the total protein, albumin, and gamma-globulin fractions of protein. The change of hematological and immune reactions of a host organism ensures a prolonged mutual adaptation of the parasite and host.     

The establishment and subsequent history of a population of Ligula intestinalis in roach Rutilis rutilis (L.)

The introduction, establishment and subsequent history of a population of Ligula intestinalis in roach, Rutilus rutilus , of a small lake was studied over a period of seven years. The introduction is believed to be a natural, chance colonization achieved by the return of Great Crested Grebes as permanent residents. Within two years the parasite had infected 33% of the roach between 60–120 mm in size. It exhibited a pronounced seasonal cycle in infection. Fish were often infected when only a few months old in autumn, and young fish and parasites over-wintered together. Parasite growth resumed in the following summer, when some further infections occurred. The majority of infected fish died in or before their second winter, possibly as a result of selective predation, but a small proportion survived into a third year. Dispersion of the parasite was close to random for most of the time. Multiple infections and slight over-dispersion occurred only in summer months. Infections were scarcer in large fish, due partly to selective mortality of infected fish and partly to a change in the host diet. The pattern of seasonal infection compared favourably with other localities, but prevalence and intensity of infection were consistently lower, parasite dispersion closer to random and multiple infections much scarcer than elsewhere. Infection levels and parasite growth rates varied from year to year, but these annual fluctuations were irregular and showed no consistent pattern. The Ligula population exhibited both regulatory and destabilizing features and there was no definite evidence that it was stable. It is suggested that Ligula is an opportunist species. It is endemic in some sites but in others, especially small lakes, the populations are unregulated and unstable and so persist for short periods only in a non-equilibrium state.     

Population biology of the helminth parasites of Phoxinus phoxinus (L.), the minnow, in a Cardiganshire lake

Specimens of Phoxinus phoxinus (L.) were collected over a period of a year from September 1967 to September 1968 from Frongoch Lake, Cardiganshire, Wales. Of a total of 650 fish examined for helminth parasites, 32 % were definitive hosts for Macrolecithus papilliger , and 16·5% for Neoechinorhynchus rutili (Müller), both parasites of the alimentary canal. All the fish examined were second intermediate host for Diplostomum phoxini (Faust) in the brain and 1·67% for Ligula intestinalis (L.) in the coelom. An increase in incidence of infestation with M. papilliger in spring and autumn and with N. rutili in summer were evident. The sex of the fish had no apparent effect on worm burden whereas size was more significant. There was a decrease in incidence of infestation with M. papilliger and an increase with N. rutili together with an increase in intensity of infestation with D. phoxini as the fish became larger. The latter species accumulated in the brain as the host increased in age.     

Changes in numbers and growth of Ligula intestinalis in the spottail shiner (Notropis hudsonius), and their roles in transmission

Eighteen species of fishes were collected during the open water (1985-1987) and winter seasons (1985-1986) from Dauphin Lake, Manitoba, Canada (51 degrees 17'N, 99 degrees 48'W) and examined for plerocercoids of Ligula intestinalis (L.). Plerocercoids were most prevalent (5.3%) in spottail shiners (Notropis hudsonius), the major fish host for Ligula in Dauphin Lake. Detailed analysis of the spottail shiner-Ligula host-parasite system revealed that the number of plerocercoids differed between years and among habitats but there was no statistically significant seasonal pattern; recruitment of new worms was highest in young fish and decreased with age, and infected spottails had reduced gonad development. Analysis of host and parasite growth revealed that the soma of male spottails infected with Ligula weighed more but had a reduced growth rate. Growth rate of females was unaffected by Ligula but somatic weight was slightly increased. This appears to be related to the greater metabolic stress on infected males. Based on increased mean somatic weight and skewness of the weight distribution for infected fish, we propose that infected spottails are subjected to size-selective mortality. Some of the contradictions in the literature may be attributed to underestimated prevalence due to increased numbers of spawning fish in the spring, mixed age-classes of Ligula in separate age-classes of fish, and differential effects on growth due to infection in male versus female hosts.     

Infestation by the mite Harpirhynchus nidulans in the Bearded Tit Panurus biarmicus

Capsule Mites sometimes induced voluminous subcutaneous cysts in featherless parts.

Aims To describe the first reported infestation by the skin-dweller mite Harpirhynchus nidulans in Bearded Tits Panurus biarmicus and for the Timaliidae family, to detect possible fitness costs for the host and to determine the distribution of the parasite within the distribution range of the host.

Methods Parasites were identified using a microscope. Wing-length and body mass were recorded on both uninfected and infected birds captured at different times during the year. We also considered historical data, and contact was made with 32 European ringing stations to identify the distribution range of the parasite.

Results Subcutaneous reproduction of the mite Harpirhynchus nidulans induced the development of voluminous dermal nodules in Panurus biarmicus. There were no differences in body mass or wing-length with respect to infestation. In the south of France, prevalence changed from 10.6% in spring to 4.7% in autumn. Both sexes are equally parasitized. Occurrence of dermal cysts is reported from several southern European populations of Bearded Tits, whereas it seems to be absent from northern latitudes.

Conclusion The occurrence of a Harpirhynchus mite in wild bird populations is reported for the first time. We consider aspects of its biology, host–parasite system, host-specificity, co-adaptation of the mite reproductive cycle to the social dynamics of its host and metapopulational host–parasite dynamics.     

Molecular Characterization of a Parasitic Tapeworm (Ligula) Based on DNA Sequences from Formalin-Fixed Specimens

Museum specimens of Ligula (Pseudophyllidea, Ligulidae), a fish parasite tapeworm, that have been preserved in ethanol or fixed permanently in formalin up to 24 years were used for DNA extraction and molecular characterization. DNA was amplified via PCR from samples collected from different fish hosts that lived in both salt and fresh water bodies in the Chinese Qinghai-Tibet Plateau, Russia, and England. Phylogenetic analyses based on partial nucleotide sequences of the 5'-end of nuclear 28S rRNA gene and the mitochondrial cytochrome c oxidase subunit I (COI) gene support the morphologically based taxonomy that groups the Chinese Ligula within the same species as their Europe counterpart: Lingula intestinalis. No nucleotide variation was detected in either the 28S rRNA gene or the COI gene among the seven plerocercoid samples, suggesting a considerable genetic homogeneity among Ligula from different regions. Our results show that geographic isolation, affinity of hosts, and host habitats are not reliable taxonomic criteria for Ligula classification. Our data also indicate a low genetic diversity in the Ligula prevalent in China and in Europe. Our experiments demonstrate that endogenous DNA from specimens that were subjected to permanent formalin fixation can be routinely amplified from parasitic tapeworms, suggesting that fixation time in formalin may not be a critical factor affecting DNA degradation in such museum specimens.     

Parasitic Nematode Abundance Aggregation as a Mechanism of the Adaptive Response of the Host Plant to Temperature Variations

The mathematical model of host–parasite relations suggested previously by the authors was applied to analyze the formation of the aggregated distribution of parasites in the case of the host plant–parasitic nematode system. For nearly the same conditions and empirical infection levels, nematode abundances in the host population followed the gamma distribution. Exposure to temperature stresses modifies the resistance of the plant population to infection. Experiments with prolonged chilling of potato plants prior to nematode infestation revealed no statistically reliable increase in the share of resistant plants compared to the control, although the mean and the range of variation of the infection rate, as well as the aggregation of the parasite distribution, decreased. Short-term chilling of the plants prior to infestation led to a reliable decrease in the mean abundance of parasites and to the lowest aggregation of the parasitic nematode in the host plant population. The results of this study showed that this temperature stress caused potatoes to develop a reliably high and uniform resistance to the nematode.     

Ectoparasites and age-dependent survival in a desert rodent

Host age is one of the key factors in host–parasite relationships as it possibly affects infestation levels, parasite-induced mortality of a host, and parasite distribution among host individuals. We tested two alternative hypotheses about infestation pattern and survival under parasitism in relation to host age. The first hypothesis assumes that parasites are recruited faster than they die and, thus, suggests that adult hosts will show higher infestation levels than juveniles because the former have more time to accumulate parasites. The second hypothesis assumes that parasites die faster than they are recruited and, thus, suggests that adults will show lower infestation levels because of acquired immune response and/or the mortality of heavily infested juveniles and, thus, selection for less infested adults. As the negative effects of parasites on host are often intensity-dependent, we expected that the age-related differences in infestation may be translated to lower or higher survival under parasitism of adults, in the cases of the first and the second hypotheses, respectively. We manipulated ectoparasite numbers using insecticide and assessed the infestation pattern in adult and juvenile gerbils (Gerbillus andersoni) in the Negev Desert. We found only a partial support for age-dependent parasitism. No age-related differences in infestation and distribution among host individuals were found after adjusting the ectoparasite numbers to the host’s surface area. However, age-related differences in survival under parasitism were revealed. The survival probability of parasitized juveniles decreased in about 48% compared to unparasitized hosts while the survival probability of adults was not affected by ectoparasites. Our results suggest that the effect of host age on host–parasite dynamics may not explicitly be determined by age-dependent differences in ectoparasite recruitment or mortality processes but may also be affected by other host-related and parasite-related traits.     

Infection of Atlantic salmon, Salmo salar L., by Gyrodactylus salaris, Malmberg 1957, in the River Lakselva, Misvær in northern Norway

Gyrodacrylus salaris was most probably introduced to the River Lakselva in 1975 through stocking of Atlantic salmon from an infected hatchery. The parasite population grew rapidly, and the parasite spread throughout the entire watercourse during the summer of 1976. This epidemic situation led to mortality among the young Atlantic salmon, and the density of salmon parr was heavily reduced from 1976 to 1977. The density of salmon parr has remained close to zero since then, while there are no apparent trends toward decrease or increase in the density of brown trout. In spite of the reduced density of young salmon, a new epidemic has developed each year among the few young 0+ and 1+ Atlantic salmon present in the river. Results from successive sampling during the summer of 1987, 1988 and 1989 indicate that most of the presmolt salmon are attacked during their first summer or autumn of life. The infection develops into an epidemic during the first autumn, winter or the next summer. The build-up of the parasite burden on the fish leads in turn to mortality. Norwegian Atlantic salmon probably have no resistance against G. salaris, since the parasite has recently been introduced to Norwegian rivers.     

Impact of Ligula intestinalis (L.1758) (Cestode), on the growth of Barbus setivimensis (Cyprinidae) in a lake system in Algeria

The Algerian freshwater fish fauna is mainly represented by the Cyprinidae family, in particular, the genus Barbus. This is represented only by natural populations of the subgenus Barbus. The systematic, based mainly on the methods of biometrics, is quite different from one author to another. However, two nominal species are usually cited: Barbus callensis (Valenciennes, 1842), which is limited to the region of El Kala (eastern Algeria) and Barbus setivimensis (Valenciennes, 1842) in other parts of the North. During the ecological study of this fauna, many individuals were found infested with the tapeworm Ligula intestinalis (Linné, 1758), which led us to study the effect of this parasite on B. setivimensis using the ecological parasites' index (prevalence, abundance and parasite intensity) and to focus on the impact of the parasite on the growth of fish. Tapeworm L. intestinalis presents a wide geographical distribution and a complex lifecycle to multiple hosts: the cycle starts in the body of birds. The life expectancy in the major host is a maximum of 5 days, but in this time, they will lay a multitude of eggs. These eggs are passed into water via the faeces of the bird. Once in the aquatic medium, they hatch and are eaten by a wide range of copepod zooplankton (first intermediate host). The cycle continues when fish (second intermediate host) ingests the copepod. The worm then burrows through the gut wall and continues to develop in the fish's body cavity. The cycle is then complete when the bird (final host) eats the tapeworm-hosting fish. We studied the effects of diet, the hosting period, the habitat on the prevalence, abundance and intensity of the parasitic larvae plerocercoid L. intestinalis and the parasiting effect on the Cyprinids fishs of the genus Barbus in the Keddara dam (Boumerdes, Algeria) during one year. Although L. intestinalis was recorded in several host fish, the available data on the parameters of parasitism are limited and no studies are reported on B. setivimensis. In this study, a total of 613 individuals were sampled and checked on the presence of L. intestinalis plerocercoid stages. Only 64 were infested. The value of the prevalence was 10.44% and the average intensity was 1.89 parasites (average two parasites per infested fish). The infection rate is high during the autumn and low during the spring season. The latter corresponds with the breeding period.     

Are parasite intensity and related costs of the milichiid fly Carnus hemapterus related to host sociality?

Ectoparasites have often been shown to have detrimental effects on their host. Not much is known, however, about determinants of infestation, e.g. the question of which factors affect distribution and occurrence of parasites on different host species (degree of host specificity) and their infestation rates. In this study we examine possible effects of host determinants on parasite intensity of Carnus hemapterus (Carnidae), an ectoparasitic fly on nestling birds, in the European bee-eater (Merops apiaster), which is a common host of C. hemapterus. Our results show that European bee-eaters seem to be one of the most heavily infested host species of C. hemapterus. We found that brood size, nestling age, and colony size are the most important determinants of infestation by C. hemapterus. This parasite seems to prefer medium-sized bee-eater chicks and to select them according to their condition. Our results further suggest a negative effect of C. hemapterus on chick development.     

Seasonal occurrence and ecological aspects of Afrodiplozoon polycotyleus (Monogenea: Diplozoidae) from the gills of three cyprinids from the Nwanedi-Luphephe dams,South Africa

The effect of seasonal changes and ecological aspects of Afrodiplozoon polycotyleus (Paperna, 1973) collected on Labeobarbus marequensis (Smith, 1841), Enteromius trimaculatus (Peters, 1852) and Enteromius radiatus (Peters, 1853) was investigated from January to October 2008. Fish were collected at the Nwanedi-Luphephe dams, Limpopo River System, South Africa using gill, cast and seine nets and electrofishing gear. Enteromius radiatus and E. trimaculatus were the most infested compared with L. marequensis. Seasonal changes had an influence on the intensity of A. polycotyleus, with infestation rates higher in spring, summer and autumn. The adults predominantly infected the medial region of the second gill arch, whereas diporpae were mainly found on the first gill. Neither sex nor water quality changes had an influence on the intensity of the parasite. The health condition of the hosts was not affected by the parasite. The different infestation rates of the parasite between the species could be attributed to host characteristics, behaviour and habitat preferences. The selection of a particular gill/region could be attributed to space for attachment organs and food supply, as well as flow and velocity of the water over the gills. The occurrence of A. polycotyleus on E. radiatus constitutes a new host record.     

Population dynamics of Gyrodactylus sp. (Monogenea) infecting the sand goby in the Oslo Fjord, Norway

Prevalence and abundance of Gyrodactylus sp. on the 1993 year-class of sand gobies Pomatoschistus minutus in the Oslo Fjord, Norway, decreased slightly during the cold months, increased as temperature increased in spring, reaching a peak in June, then decreased significantly, corresponding with a decline in the number of hosts from August. Abundance and, especially, prevalence increased again in September, and decreased in late autumn. Death of the most heavily infected hosts, and/or host resistance might be responsible for the decline in parasite numbers on post-spawners in summer. The young of the year (1994 year-class) were probably infected shortly after they commenced benthic life in July, and prevalence and abundance increased significantly throughout late summer and autumn. Parasite abundance on males was significantly higher than on females at the height of the breeding season in June, but significantly lower at the end of the breeding season in July. Two-thirds of the parasites infected the gills, oral cavity and pharynx. The proportion of parasites on the body, head and fins increased on both sexes, but significantly more so on males, during the breeding season of the host, when parasite intensity was highest. Possible routes of transmission of the parasite are discussed.     

The effect of ligula intestinalis on some lipid exchange indexes of the spleen of the host, bream abramis brama of different age

The results of the comparative analysis of the spleen in healthy individuals of bream Abramis brama and those infected by the Ligula intestinalis plerocercoids are given. Two age groups of bream were studied. The comparison was carried out by the index of common lipids (CL), the content of common lipids, the intensity of lipid peroxidation (POL), and the common antioxidant activity (CAA). The dependence of the lipid exchange character in the fishes infected by Ligula on age, as well as on different levels of the infestation is demonstrated.     

Experiments on Spirulina culture on waste-effluent media and at the pilot plant

The prevalence of the microsporidian, Nosema herpobdellae, in the leech, Erpobdella octoculata, collected from a eutrophic English lake, was examined at monthly intervals over two years. The leech has an annual life cycle and, for each cohort, infection appeared in recently recruited animals in early autumn and prevalence levels rose to a peak in late autumn or winter before declining till the cohort died out the following autumn. Prevalence levels never exceeded 9%. The effect of the parasite on young leeches was difficult to assess, but there was some evidence of parasite-induced host mortality in older animals.     

Nestling sex predicts susceptibility to parasitism and influences parasite population size within avian broods

Vertebrate hosts differ in their level of parasite susceptibility and infestation. In avian broods, variation in susceptibility of nestlings to ectoparasites may be associated with non‐uniform distributions of parasites among brood mates, with parasites concentrating feeding on the most vulnerable hosts. The presence of a highly susceptible nestling in a brood can benefit the remaining young by reducing the parasite pressure they experience; however, from a parasite’s perspective, broods with fewer susceptible hosts may provide effectively fewer resources than broods of the same size containing a greater abundance of susceptible hosts, and this could limit the number of parasites that a host brood can sustain. To test whether variation in number of susceptible hosts affects the number of parasites in bird nests, we first examined the role of host sex and induced immunity (via methionine supplementation) on susceptibility of mountain bluebirds Sialia currucoides to parasitism by blow flies Protocalliphora spp. We then assessed the effect of variation in number of susceptible hosts on the number of parasites inhabiting the nest. Only females showed a benefit of methionine supplementation, gaining mass more rapidly following supplementation compared to males. This suggests that females are more susceptible to parasites in this system; this was further supported by parasite feeding trials, in which parasites extracted larger blood meals from female than male hosts. Finally, the abundance of parasites in nests was predicted by brood sex ratio: broods containing more female young harboured more parasites. Hence, within‐brood variation in host susceptibility to parasites can not only influence the costs of parasitism for individual nestlings, but may also have consequences for the size of parasite populations within nests. If patterns of maternal investment affect the abundance of nest‐dwelling parasites, these interactions may be important for understanding fitness consequences of maternal resource allocation in many vertebrate hosts.     

Habitat and host associations of the fish‐burrowing parasite Artystone minima (Cymothoidae: Isopoda) in eastern Amazonia

Cymothoid fish parasites settle on hosts in ways that may impact fish health and energetics. High abundances of Artystone minima observed in Nannostomus beckfordi from the Jeju River in eastern Amazonia were investigated to answer the following questions: (a) What factors are associated with the high prevalence at this locality?; (b) Is high abundance associated with co‐infestation of alternative hosts?; and (c) Is parasite presence associated with host species growth and/or reproduction? Fish assemblages were sampled quarterly (August 2017–May 2018) from five habitats along with environmental data. Parasitic indices were calculated, and parasite presence used to evaluate differences in growth of hosts using analysis of covariance considering host sex and sampling season (wet vs. dry). Parasites were only abundant in one of the habitats, a large, shallow backwater bay with macrophytes. Abiotic environmental factors (flow and depth) likely impact parasite transmission and are, therefore, particularly important in producing these local patterns. Two secondary hosts, Hyphessobrycon cf. rosaceus and Moenkhausia collettii, were found in the wet season. Based on host biology compared to other fish in the habitat, parasite infestation is inferred to be depth associated and long‐term infestation is apparently limited in alternative hosts. Parasite presence was significantly associated with reduced weight (standardized for length) of female Nannostomus beckfordi in the wet season. Furthermore, ovaries of non‐parasitized females from the wet season presented a range of maturation stages, while parasitized females were all immature, indicating a significant association of parasites with host reproductive capacity. Abstract in Portuguese is available with online material