Effect of Ligula intestinalis on the reproductive capacity of Rastrineobola argentea in Lake Victoria

This study examined the potential effect of the cestode Ligula intestinalis on the reproduction of the indigenous cyprinid Rastrineobola argentea in Lake Victoria. Ligula intestinalis had a marked effect on the breeding cycle of R. argentea. The proportion of the infected population in advanced stages of maturation prior to spawning was considerably reduced compared with uninfected fish. Infection by L. intestinalis significantly reduced the fecundity of individual fish, particularly in the 45–60 mm size range; the component of the population that makes the greatest contribution to reproductive output. The reduction in reproductive output of the R. argentea population could potentially affect replenishment of stocks in this important fishery.     

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.     

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.     

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.     

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.     

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.     

Comparative morphology of surface ultrastructure of diphyllobothriidean tapeworms (Cestoda: Diphyllobothriidea)

Microtriches on the scolices and adjacent strobila of seven species of diphyllobothriidean cestodes (Bothridium pithonis, Cephalochlamys namaquensis, Dibothriocephalus latus, Duthiersia expansa, D. fimbriata, Ligula intestinalis, and Schistocephalus solidus) from different hosts (frogs, snakes, lizards, birds, and mammals) and biogeographic areas were examined using scanning and transmission electron microscopy. The basic structure of the tegument of the seven species studied does not differ markedly from that found in other cestodes. The main characteristic is the presence of electron‐dense bodies and vesicles in the distal cytoplasm. However, this study has shown differences in the morphology of microtriches even among species of the same family. Two different types of microtriches were found, filitriches and spinitriches, with the latter represented by two forms. Our study reveals that capilliform filitriches are most commonly found in Diphyllobothriidea. They were observed mainly on the strobila and the scolices of all but one studied species; individuals of L. intestinalis bore only coniform spinitriches on their surface. The same type of microtriches was found on the cirrus in D. latus. Gladiate spinitriches covered the scolex in both species of Duthiersia, and gladiate spinitriches interspersed with capilliform filitriches were observed on the anterior part of the strobila in D. fimbriata and the posterior part of the scolex in B. pithonis. Individuals of C. namaquensis were covered only by small acicular filitriches. No obvious pattern in the type and distribution of microtriches was observed among species that belong to different families and parasitize distantly related definitive hosts.     

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.     

Effect of large weirs on abundance and diversity of migratory Labeobarbus species in tributaries of Lake Tana,Ethiopia

Lake Tana has a remarkable fish diversity, including 17 endemic Labeobarbus species, of which nine spawn in the inflowing rivers. Three of the migratory species are threatened, namely the endangered Labeobarbus macrophtalmus and the vulnerable L. acutirostris and L. platydorsus. In July–November 2016 during the wet season netting upstream and downstream of large weirs in two rivers and in two undammed rivers showed that weirs had a severe negative effect on migratory Labeobarbus, including the three threatened species. Of eight Labeobarbus species caught below the Gelda River weir, only L. intermedius was recorded above the weir, and in the Shini River, five Labeobarbus species were caught below the weir, but none above it. Labeobarbus diversity below the Gelda River weir (H’?=?1.4) was significantly different to that above the weir (H’?=?0), whereas in the two rivers without any weirs, Labeobarbus diversity downstream (H’?=?1.39 and 1.55) was not significantly different from that upstream (H’?=?1.52 and 1.40). Therefore, specific mitigation measures, such as fishways, need to be designed from the outset of proposed weir and instream dam construction.     

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.     

Influence of black spot disease on shoaling behaviour in female western mosquitofish, <Emphasis Type="Italic">Gambusia affinis</Emphasis> (Poeciliidae,Teleostei)

Parasites can fundamentally alter the cost–benefit ratio of living in a group, e.g. if infected individuals increase the predation risk of shoal mates. Here, the effect of an infection with a trematode, Uvulifer sp. (Diplostomatidae) on the shoaling behaviour of female western mosquitofish, Gambusia affinis, was investigated. The parasite examined causes a direct phenotypical change of the host by forming black spots on its body surface. When given a choice between a stimulus shoal and no shoal, we found shoaling tendencies to be significantly reduced in infected focal fish. In another experiment, we tested for association preferences relative to the infection status of the stimulus fish. Given the choice between an infected and a healthy stimulus fish, both infected and healthy focal fish preferred to associate with non-infected stimulus fish. Our results suggest that (1) the cost–benefit ratio of shoaling might be different for infected and non-infected individuals. Infected fish may be more affected by competition for food within a shoal. (2) Associating with infected conspecifics appears to be costly for female mosquitofish, maybe due to increased predation risk.     

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.     

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.     

Morphological and behavioral variation of <Emphasis Type="Italic">Rasbora paviei</Emphasis> (Cyprinidae,Cypriniformes) from lotic and limnic habitats (Central Vietnam)

Morphological and behavioral traits of Rasbora paviei from river and lake environments are studied. For investigations, the fish were caught from the middle reaches of the Cai River and from the inshore zone of the Kam Lam Reservoir (Khanh Hoa Province, Central Vietnam). Phenotypic differences are found in river and lake fish groups. Experimentally, differences in tactics and efficiency of defensive behavior are found in specimens from different habitats in the presence of a predator—Lepisosteus sp. (Lepisosteidae). In river specimens of Rasbora, the defensive reaction is more efficient in comparison with specimens from the reservoir. The river specimens of Rasbora used predominantly the tactics of group defense from the predator and stayed in a school longer than the lake specimens.     

Development and changes at settlement in the barbel structure of the reef fish,Upeneus tragula (Mullidae)

Synopsis The development of the sensory barbels of the tropical goatfish, Upeneus tragula (Mullidae), was examined from their first appearance early in planktonic life through to the reef-associated juvenile period. The structure of the barbel was examined histologically and found to represent an outgrowth of the gustatory (taste) system, composed of at least 50% sensory tissue at settlement. Abrupt changes in morphology were found to be coincident with the 6–12 h settlement period: barbels rapidly moved forward along the hyoid arch to abut the dentary; the length of the barbels increased by up to 52%; the epidermal layer increased to comprise 75% of the cross-sectional area; and the mean size of the taste bud cells increased by up to 100%. A strong relationship was found between barbel length and mean taste-bud size. This relationship was used to predict the mean taste-bud sizes for 237 newly-settled fish, collected as 12 samples over two recruitment seasons. Mean taste-bud size varied significantly among samples. Experiments examined whether food availability or temperature of the water within the pelagic phase influenced the size of the barbels at settlement. Food availability influenced the relationship between barbel length and fish size. Slower growing fish had larger barbels relative to fish length than those that grew faster. Temperature did not influence the relationship between barbel length and fish size. Variability in sensory development at settlement, and the factors which influence it, may have important ramifications for the potential success of the fish once on the reef.     

Relationship between prevalence of trematode parasite <Emphasis Type="Italic">Diplostomum</Emphasis> sp. and population density of its snail host <Emphasis Type="Italic">Lymnaea stagnalis</Emphasis> in lakes and ponds in Finland

Diplostomum sp. is a trematode parasite that infects aquatic snails, e.g. Lymnaea stagnalis (Gastropoda: Lymnaeidae), fish, and fish-eating birds. Ponds and lakes (n = 28) located in Finland between latitudes 61°45′N and 65°30′N were sampled for L. stagnalis, the first intermediate host for Diplostomum sp. L. stagnalis were found in 22 sites out of 28, and Diplostomum sp. in 10 of the 22 snail populations. Among the L. stagnalis populations that were infected by Diplostomum sp., the mean prevalence was 12.8%. Diplostomum sp. occurred in only one out of the seven L. stagnalis populations in four large lakes, but in 9 out of the 16 L. stagnalis populations in small lakes. In the pooled data, a positive correlation (r _s = 0.427; P = 0.047; n = 22) between L. stagnalis density and Diplostomum sp. prevalence was found. The results suggest that Diplostomum sp. is fairly common in L. stagnalis populations in small lakes but rare in large lakes. Furthermore, although trematode parasites, in general, should have a negative effect on snail population density, the study indicates that the relationship between host density and parasite prevalence may greatly differ for individual trematode species, such as Diplostomum sp.     

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.     

Metazoan parasites of Alburnus chalcoides in Tödürge Lake (Zara/Sivas,Turkey)

The metazoan parasites of the Danube bleak, Alburnus chalcoides (Güldenstädt, 1772), were determined in Tödürge Lake, since the parasite fish fauna had not yet been studied in this system. A total of 106 specimens were collected from October 2004 to September 2005. Six parasite species were found: two monogeneans (Diplozoon paradoxum and Diplozoon megan), one digenean (Posthodiplostomum cuticola), one cestode (Bothriocephalus acheilognathi), one nematod (Rhabdochona sp.), and one copepod (Argulus foliaceus). About 87.7% of the Danube bleak examined were infected by at least one parasite: Rhabdochona sp. (4080 specimens), Posthodiplostomum cuticola (312 specimens) and Diplozoon megan (159 specimens) being the dominant parasites. Only 33% of the fish carried one parasitic species whilst the remainder had two (21.7%), three (17.9%) and four different species (15.1%). The frequency of infestation changed according to seasonal conditions, with a maximum 94.3% observed in spring. Occurrence, density, seasonal changes, and preferences of the parasites species for various ages and size groups of the bleak were identified, despite the limited overall sample size. D. paradoxum, D. megan, P. cuticola, B. acheilognathi, Rhabdochona sp. and A. foliaceus were determined for the first time as parasites of Danube bleak in Turkey. D. megan was also a new record for the fish parasite fauna of Turkey.     

Taste preferences and feeding behavior of the stone loach <Emphasis Type="Italic">Barbatula barbatula</Emphasis> (Balitoridae,Cypriniformes) after partial deprivation of circum-mouth external gustatory and tactile receptors

Comparative study of the feeding behavior and gustatory preferences mediated by extraoral and intraoral gustatory reception in the stone loach Barbatula barbatula in the norm and 1–6 months after extirpation of all three pairs of barbels was performed. It was found that partial loss of external gustatory receptors and the sensory deficit caused by it do not lead to any noticeable disturbances of the ability of fish to evaluate taste properties of food objects (artificial agar-agar pellets containing L-isomers of alanine, lysine, cysteine or an water extract of chironomid larvae) and make an adequate decision of their grasping or ignoring and swallowing or refusing. The extirpation of the barbels does not influence feeding behavior related to determination by fish of the taste properties of pellets and completely retains in its ritual an obligatory preliminary examination of the food object using external gustatory reception. It is suggested that external taste buds having different localization are equally capable of providing for fish a preliminary evaluation of the taste properties of the object. After extirpation of the barbels, the efficiency of grasping pellets decreases in fish, which indicates an important role of tactile reception in the determination of the site of location of the food object and in providing of the accuracy of the hunter’s dart in fish with a weak vision development.