Fish parasitism in a new impoundment and differences upstream and downstream

The parasitic fish fauna in Guelph Lake, a four-year old impoundment, were compared with those in upstream and downstream localities. The lacustrine assemblage of the young mesotrophic to eutrophic impoundment was dominated by the cestodes, Ligula intestinalis and Proteocephalus ambloplites, and the nematode, Philometra sp. The acanthocephalan, Neoechinorhynchus saginatus, and the nematode, Rhabdacona cascadilla dominated the rheophilous assemblage of fish parasites, but the prevalence rate and intensity of R. cascadilla was significantly reduced downstream.     

Distribution and occurrence of <Emphasis Type="Italic">Ligula intestinalis</Emphasis> (L.) plerocercoids (Cestoda,Ligulidae) in the fishes of Lake Tana,Ethiopia

The infection rate by Ligula intestinalis has been studied in 14 fish species (Varicorhinus beso, Garra dembecha, Labeobarbus intermedius, L. crassibarbis, L. tsanensis, L. megastoma, L. brevicephalus, L. nedgia, L. acutirostris, L. gorgorensis, L. dainellii, L. macrophthalmus, Barbus humilis, and B. tanapelagius) from Lake Tana (Ethiopia). Plerocercoids have been found only in the fishes of gg. Labeobarbus and Barbus. Ligula has been found in seven out of ten studied large barbels. Barbels larger than 23 cm are not infected with ligula. It is revealed that a specific “synergism” exists between Ligula intestinalis and cestode Khawia sp. parasitizing the intestine of barbels. This synergism is manifested as a regular cooccurrence of these parasites. In juvenile Labeobarbus, fish coparasitized by Khawia sp. and L. intestinalis occurred more often than fish infected with each of this parasite separately.     

The occurrence of the tapeworm Ligula intestinalis (L.), in Barbus paludinosus from a small dam in Zimbabwe

Cestode parasites were collected from Barbus paludinosus from Munwahuku Dam near Harare, Zimbabwe over a period of 13 months. Plerocercoids of Ligula intestinalis were found in 7.2% of the fish. The majority of the infected fish carried one parasite, with 3.1% having two and 1.6% with three. There was a positive correlation (r = 0.59, P < 0.05) between the weight of L. intestinalis and that of their host, but there was no significant relationship between the condition factor of the fish and the weight of the parasite, and the parasite index was low (7.97 ± 3.38) compared to previous studies in South Africa. The gonads of all infected fish were atrophied. The prevalence of L. intestinalis in B. paludinosus was high between July and September 2000 and low thereafter. There was no clear seasonal variation in the occurrence of the parasite, although the lengthy dry season might have had an effect on the prevalence.     

Expression of gonadotropin subunits in roach (Rutilus rutilus, Cyprinidae) infected with plerocercoids of the tapeworm Ligula intestinalis (Cestoda)

Plerocercoids of the tapeworm Ligula intestinalis (Cestoda: Bothriocephalidea) have been reported to inhibit gametogenesis of their intermediate fish hosts. However, mechanistic studies are rare and the proximate cues leading to impaired reproduction still remain unknown. In the present study we investigated the effects of infection by L. intestinalis on reproductive parameters of roach (Rutilus rutilus, Cyprinidae), a common fish host of this parasite. Field studies on roach demonstrated that in both genders infection prevented gonad development. As revealed by quantitative PCR, infection was accompanied by essentially lower pituitary expression of follicle-stimulating hormone β-subunit (FSHβ) and luteinizing hormone β-subunit (LHβ) mRNA compared with uninfected roach, providing clear evidence for gonadotropin-insufficiency as the cause of arrested gametogenesis. Under controlled laboratory conditions infected roach showed lower mRNA levels of FSHβ but not of LHβ, despite histology revealing similar gonad stages as in uninfected conspecifics. These findings indicate the involvement of FSH rather than LH in mediating effects of infection early during gonad development in roach. Moreover, the impact of L. intestinalis on reproductive parameters of roach appeared to be independent of the parasite burden. Together, these data provide valuable information on the role of FSH and LH as mediators of parasite-induced sterilization in a vertebrate and implicate the selective inhibition of host reproduction by L. intestinalis as a natural source of endocrine disruption in fish.     

Life history shifts in an exploited African fish following invasion by a castrating parasite

Evolutionary theory predicts that infection by a parasite that reduces future host survival or fecundity should select for increased investment in current reproduction. In this study, we use the cestode Ligula intestinalis and its intermediate fish host Engraulicypris sardella in Wissman Bay, Lake Nyasa (Tanzania), as a model system. Using data about infection of E. sardella fish hosts by L. intestinalis collected for a period of 10 years, we explored whether parasite infection affects the fecundity of the fish host E. sardella, and whether host reproductive investment has increased at the expense of somatic growth. We found that L. intestinalis had a strong negative effect on the fecundity of its intermediate fish host. For the noninfected fish, we observed an increase in relative gonadal weight at maturity over the study period, while size at maturity decreased. These findings suggest that the life history of E. sardella has been shifting toward earlier reproduction. Further studies are warranted to assess whether these changes reflect plastic or evolutionary responses. We also discuss the interaction between parasite and fishery‐mediated selection as a possible explanation for the decline of E. sardella stock in the lake.     

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.     

Little evidence for morphological change in a resilient endemic species following the introduction of a novel predator

Human activities, such as species introductions, are dramatically and rapidly altering natural ecological processes and often result in novel selection regimes. To date, we still have a limited understanding of the extent to which such anthropogenic selection may be driving contemporary phenotypic change in natural populations. Here, we test whether the introduction of the piscivorous Nile perch, Lates niloticus, into East Africa's Lake Victoria and nearby lakes coincided with morphological change in one resilient native prey species, the cyprinid fish Rastrineobola argentea. Drawing on prior ecomorphological research, we predicted that this novel predator would select for increased allocation to the caudal region in R. argentea to enhance burst‐swimming performance and hence escape ability. To test this prediction, we compared body morphology of R. argentea across space (nine Ugandan lakes differing in Nile perch invasion history) and through time (before and after establishment of Nile perch in Lake Victoria). Spatial comparisons of contemporary populations only partially supported our predictions, with R. argentea from some invaded lakes having larger caudal regions and smaller heads compared to R. argentea from uninvaded lakes. There was no clear evidence of predator‐associated change in body shape over time in Lake Victoria. We conclude that R. argentea have not responded to the presence of Nile perch with consistent morphological changes and that other factors are driving observed patterns of body shape variation in R. argentea.     

Copepods as the first intermediate hosts of Ligula intestinalis L.: Parasite of bream Abramis brama L. in the Vistula Lagoon of the Baltic Sea

Seven copepod species (potential intermediate hosts of Ligula intestinalis L.) are recorded in the Vistula Lagoon. Megacyclops viridis (Jurine) and Diacyclops bicuspidatus (Claus) are dominant species among the Cyclopoida group and may be the main potential first intermediate host of L. intestinalis. Cytopoidae is unevenly distributed in the lagoon. The parts of the lagoon with high crustacean densities and high levels of bream infestation coincide. The peaks of Cyclopoidae abundance and the highest infestation of the bream by L. intestinalis were recorded in 1998–2000. This study shows that bream infestation in the Vistula Lagoon is directly connected with the presence of freshwater copepods (the first intermediate hosts of L. intestinalis), its abundance, and its spatial distribution over the lagoon area.     

Comparative cytogenetics of Diphyllobothrium ditremum (Creplin, 1925) and Ligula intestinalis (Linnaeus, 1758) (Cestoda: Pseudophyllidea)

An investigation carried out on two species of pseudophyllidean cestodes belonging to different families showed very close karyological affinity between them. The karyotypes of Diphyllobothrium ditremum and Ligula intestinalis both consist of 18 bi-armed chromosomes and are almost identical with respect to the relative length and the centromeric indices of corresponding chromosomes. Statistically significant differences exist in the morphology of chromosomes 2 and 4, but they are not striking and may be due in part to errors of measurement. Differences in the absolute length of the chromosomes were noted: the chromosomes of D. ditremum are somewhat larger (from 2.7 to 8.5 μm) than those of L. intestinalis (from 1.9 to 5.4 μm). The results obtained were compared with data existing for other pseudophyllidean cestodes and preliminary conclusions on the karyotypic evolution in that group of helminths were made.     

Niche expansion in a resilient endemic species following introduction of a novel top predator

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Spatial and Temporal Variation of Cestode Infection and its Effects on Two Small Barbs (Barbus humilis and B. tanapelagius) in Lake Tana, Ethiopia

Pseudophyllidean cestodes as Ligula have a complex life cycle with cyclopoid copepods as first intermediate host, zooplanktivorous fish as second, and piscivorous birds as final host. We studied the effects of diet, season and habitat occupation on the prevalence of plerocercoid larvae of the tapeworm Ligula intestinalis in two closely related small barbs and the effects of the parasites on the barbs life histories in Lake Tana (Ethiopia) during 1 year. In all affected barbs L. intestinalis caused retardation in gonad development, maturation at reduced size and lower absolute fecundity. Infection rate, averaged over all habitats was significantly higher in B. tanapelagius (10%) than in B. humilis (6%). Below a threshold of 48 mm the infection rate was zero for both barbs, this coincided with a very low proportion of copepods in their diets, increasing up to 90 and 55%, respectively, for their largest size class (81–90 mm). The relatively high infection rate in B. tanapelagius is explained by its obligatory zooplanktivorous feeding behaviour, ingesting a relatively high proportion of infected cyclopoid copepods. This is in contrast with B. humilis, which is a polyphagous species, feeding both on zooplankton and benthic invertebrates. Significant seasonal effects in infection rates were observed. In both barb species infection rates were lower during the breeding season. Only for B. tanapelagius a significant negative correlation was observed between rain fall and infection rate, probably caused by an increased turbidity that decreases feeding efficiency on zooplankton. Habitat type had also a significant effect on infection rate. Barbus humilis showed a much higher infection rate in shallow clear water (10%) than in shallow turbid water (3%), whereas B. tanapelagius showed much higher infection rates in the shallow sublittoral (13%) than in the deeper pelagic (7%). Most likely, birds predate more efficiently on barbs in shallow clear waters than in shallow turbid and deep waters.     

Parasites of native and exotic freshwater fishes in south‐western Australia

In this study, 1429 fishes of 18 different species (12 native and six exotic) were sampled from 29 localities to compare the levels of parasitism between native and exotic fish species and to examine the relationship between environmental degradation and parasite diversity. Forty‐four putative species of parasites were found and most of these appear to be native parasites, which have not previously been described. Two parasite species, Lernaea cyprinacea and Ligula intestinalis, are probably introduced. Both were found on or in a range of native fish species, where they may cause severe disease. Levels of parasitism and parasite diversity were significantly greater in native fishes than in exotic species, and this may contribute to an enhanced demographic performance and competitive ability in invading exotics. Levels of parasitism and parasite diversity in native fishes were negatively related to habitat disturbance, in particular to a suite of factors that indicate increased human use of the river and surrounding environment. This was due principally to the absence in more disturbed habitats of a number of species of endoparasites with complex life cycles, involving transmission between different host species.     

Schistocephalus solidus and Ligula intestinalis: Pinocytosis by the tegument

Using ruthenium red as a macromolecule, endocytosis was demonstrated in the plerocercoid of Ligula intestinalis and adult Schistocephalus solidus. Uptake, transport across the tegument, and exocytosis across the basal plasma membrane occurred within 6 min. The types of vesicles in the tegument of L. intestinalis are redescribed and their former classification is modified. The vertical and longitudinal distribution of pinosomes in the tegument of adult S. solidus and L. intestinalis plerocercoids were determined. The possible role of macromolecular uptake in the economy of pseudophyllidean tapeworms is discussed with particular reference to growth and defence of an unencysted larval stage in the tissues of the intermediate host.     

Mass Death of Predatory Carp,Chanodichthys erythropterus,Induced by Plerocercoid Larvae of Ligula intestinalis (Cestoda: Diphyllobothriidae)

We describe here the mass death of predatory carp, Chanodichthys erythropterus, in Korea induced by plerocercoid larvae of Ligula intestinalis as a result of host manipulation. The carcasses of fish with ligulid larvae were first found in the river-edge areas of Chilgok-bo in Nakdong-gang (River), Korea at early February 2016. This ecological phenomena also occurred in the adjacent areas of 3 dams of Nakdong-gang, i.e., Gangjeong-bo, Dalseong-bo, and Hapcheon-Changnyeong-bo. Total 1,173 fish carcasses were collected from the 4 regions. To examine the cause of death, we captured 10 wondering carp in the river-edge areas of Hapcheon-Changnyeong-bo with a landing net. They were 24.0-28.5 cm in length and 147-257 g in weight, and had 2-11 plerocercoid larvae in the abdominal cavity. Their digestive organs were slender and empty, and reproductive organs were not observed at all. The plerocercoid larvae occupied almost all spaces of the abdominal cavity under the air bladders. The proportion of larvae per fish was 14.6-32.1% of body weight. The larvae were ivory-white, 21.5-63.0 cm long, and 6.0-13.8 g in weight. We suggest that the preference for the river-edge in infected fish during winter is a modified behavioral response by host manipulation of the tapeworm larvae. The life cycle of this tapeworm seems to be successfully continued as the infected fish can be easily eaten by avian definitive hosts.     

The nature of changes of some immunophysiological characteristics in bream (Abramis brama) infected with plerocercoids (Ligula intestinalis) at various stages of parasite development

The data from studies of the antimicrobial properties of blood serum, the content of total lipids, and antioxidant activity of immunocompetent tissues and organs of breams Abramis brama infected with plerocercoids Ligula intestinalis depending on the phase of development of the parasite are presented. The quantitative characteristics of the studied parameters are determined.     

Geography and host specificity: two forces behind the genetic structure of the freshwater fish parasite Ligula intestinalis (Cestoda: Diphyllobothriidae)

Parasite species with global distributions and complex life cycles offer a rare opportunity to study alternative mechanisms of speciation and evolution in a single model. Here, genealogy and genetic structure, with respect to geography and fish host preference, have been analyzed for Ligula intestinalis, a tapeworm affecting freshwater fish. The data analyzed consisted of 109 tapeworms sampled from 13 fish host species in 18 different localities on a macrogeographic scale. Two mitochondrial genes, cytochrome oxidase subunit I and cytochrome B, and the nuclear sequence of intergenic transcribed spacer 2 (ITS2) were used for the genetic reconstruction. Different evolutionary patterns were found at the local and at the global geographic scales. On a local scale, the flat genetic structure was mainly attributed to contiguous range expansion. Migrating birds are the most likely cause of the homogenisation of the whole population, preventing the creation of significant genetic barriers. By contrast, on a global scale, genetically distant and well-separated clusters are present in different geographic areas. Reproductive isolation was found even between clades living in sympatry and infecting the same definitive host, suggesting the existence of efficient biologically determined genetic barriers, and thus possibly separate species. Although the ITS2 sequences were found to display considerable intragenomic variability, their relationships were generally in good agreement with the topology derived from mitochondrial genes.     

Variation in the reproductive potential of Schistocephalus infected male sticklebacks is associated with 11-ketotestosterone titre

Parasites can impact host reproduction by interfering with host endocrine systems, but the adaptive nature of such effects is disputed. Schistocephalus solidus plerocercoids are parasites of three-spined sticklebacks Gasterosteus aculeatus that are often associated with impaired host reproduction. Here, we relate reproductive behavior and physiology to levels of the androgen 11-ketotestosterone (11KT) in naturally infected and non-infected male sticklebacks from two UK populations. In one population infected males harbored heavy infections and showed uniformly reduced 11KT titres and kidney spiggin (nesting glue protein) content compared to non-infected fish. However in a second population infection levels were more variable and males with smaller infections recorded 11KT and spiggin titres that overlapped those of non-infected fish; among infected males from this population 11KT and kidney spiggin also both correlated negatively with infection severity. Male reproductive behavior correlated closely with 11KT titre in both populations, and infected males with high 11KT levels exhibited normal reproductive behavior. Our results suggest that Schistocephalus infection per se does not block reproductive development in male sticklebacks, and that some male fish may have the ability to breed whilst infected. Our results are not consistent with the hypothesis that Schistocephalus adaptively castrates male hosts via endocrine disruption; rather they support the hypothesis that reproductive disruption is a side effect of the energetic costs of infection.     

The development and reproductive output of three species of Cladocera (Crustacea,Branchiopoda) with different size spectra as the result of vertebrate and invertebrate predation impact

Seasonal changes in development and reproduction of three species of Cladocera, Bosmina longirostris, Bosmina coregoni and Diaphanosoma brachyurum, were studied in regard to impact of vertebrate (planktivorous fish) and invertebrate (cladoceran Leptodora kindtii and cyclopoid copepods Mesocyclops leuckarti and Thermocyclops oithonoides) predators. Each of the cladocerans represented a different prey type. The population of the largest body-sized D. brachyurum was not affected by predators suggesting unidentified mechanisms of predation-avoidance. Diaphanosoma displayed low reproductive output coinciding with high density. Medium-sized B. coregoni, influenced by planktivorous fish, invested in reproduction and carried large egg-clutches resulting in gradual increase in population density. The population of small body-sized B. longirostris, that was influenced by invertebrate predators, displayed high density and reproductive effort in spring, followed by extreme collapse in abundance and reproduction during summer months. The results suggest that invertebrate predators may suppress populations of some Cladocera more strongly than planktivorous fish.     

Development of microsatellite markers in the green algae Enteromorpha intestinalis (Chlorophyta)

The fouling green algae Enteromorpha intestinalis is a cosmopolitan benthic species, which causes green tides in many coastal areas and is used as an indicator species for eutrophication in the Baltic Sea area. The life cycle of E. intestinalis alternates between two morphologically identical reproductive stages, a haploid gametophyte phase and a diploid sporophyte phase. However, it also reproduces through asexual propagation. The reproductive cycles of E. intestinalis in the Baltic Sea and elsewhere are largely unknown. Here we report five polymorphic microsatellite markers developed from enriched genomic libraries. The number of alleles per locus ranged from 7 to 25.     

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.