Parasites of Salmo trutta L. from the Titino River. Part III. Histological observations of parasites of the intestinal tract

During researches on helminth parasites of Salmo trutta L. from the River Tirino (L'Aquila - Italy) histological studies of the intestinal tract of brown trout infected by the following species: Crowcrocaecum testiobliquum (Wisnewski, 1932) Skrjabin e Koval, 1956; Cyathocephalus truncatus (Pallas, 1781);o Truttaedacnitis truttae (Fabricius, 1794) Petter, 1974 and Dentitruncus truttae Sinzar, 1955 have been carried out. The attachment of the single species and the histological changes in the host gut due to parasite species have been described.     

Parasites of Salmo trutta L. from the Tirino River. II. Host-parasite interactions of helminth species

The hundred and sixteen brown trout (Salmo trutta L.) which were examined for helminth parasites were captured in the River Tirino, (L'Acquila - Italy). Six parasite species (Phyllodistomum simile, Crowcrocaecum testiobliquum, Crepidostomum metoecus, Cyathocephalus truncatus, Truttaedacnitis truttae and Dentitruncus truttae) were recovered. Ecological studies on each helminth species recovered have been carried out analysing the following aspects; the preference of each parasite species for certain microhabitats in the host; the incidence and intensity of each parasitic infection according to sex, age and season.     

Pairing success and sperm reserve of male Gammarus pulex infected by Cyathocephalus truncatus (Cestoda: Spathebothriidea)

Manipulative parasites with complex life cycles are known to induce behavioural and physiological changes in their intermediate hosts. Cyathocephalus truncatus is a manipulative parasite which infects Gammarus pulex as intermediate host. G. pulex males display pre-copulatory mate guarding as a response to male-male competition for access to receptive females. In this paper, we tested the influence that C. truncatus-infection might have on male G. pulex sperm number and pairing success. We considered 3 classes of G. pulex males in our experiments: (i) uninfected males found paired in the field, (ii) uninfected males found unpaired in the field, or (iii) infected males found unpaired in the field. Both infected males and uninfected unpaired males paired less with a new female than uninfected paired males did. Furthermore, infected males appear to be at a strong disadvantage when directly competing for females with a healthy rival male, and had fewer sperm in their testes. We discuss the potential effect of male and female mating strategies on such male host mating alteration.     

Selective predation on parasitized prey--a comparison between two helminth species with different life-history strategies.

In Lake Fjellfr?svatn, northern Norway, the larval helminths Cyathocephalus truncatus and Cystidicola farionis use Gammarus lacustris as intermediate hosts and Arctic charr (Salvelinus alpinus) as final hosts. There was sampled 1,433 live G. lacustris from the lake and 1,964 G. lacustris from stomach contents of the charr. Prevalence of infection were, respectively, 0.49% and 3.72% for C. truncatus, and 0.21% and 0.20% for C. farionis. Usually, only 1 parasite was present in each host, and the 2 parasite species never co-occurred. Gammarus lacustris amphipods parasitized by C. truncatus were positively selected by the Arctic charr and were consumed approximately 8 times as often as were the unparasitized amphipods or the amphipods infected with C. farionis. This suggests that G. lacustris amphipods infected with C. truncatus larvae are more susceptible to predation than noninfected specimens, probably because of parasite-induced alterations in behavior or visibility. Alternatively, this could also be explained by selection toward the largest G. lacustris specimens observed, which are also the most frequently parasitized amphipods. However, the data show clearly that this was not a result of size-selective predation by the charr. In contrast, the presence of C. farionis did not increase the susceptibility to predation of its intermediate host. The discrepancy between the 2 helminth species supports the hypothesis that parasite-increased susceptibility to predation is related to the life history strategies of the parasites.     

Studies on the development of the oncosphere and procercoid of Cyathocephalus truncatus (Cestoda) in the intermediate host, Gammarus pulex

Cultured eggs of Cyathocephalus truncatus were found to develop optimally at 20°C, but they did not develop at 6°C and above. The oncosphere of the tapeworm has been seen to be a true hexacanth embryo. Specimens of the intermediate host. Gammaurs pulex , were infected by being forced to feed on pieces of lettuce leaves on which infective eggs of the tapeworm were placed. The young drveloping porocercoid was first recovered from the haemocoel of Gammarus pulex 5 days after infection. The procercoid was found to reach the infective stage within the amphipod after about ten weeks.     

Parasitic fauna of Salmo trutta L. of the Tirino river. I. Redescription of Dentitruncus truttae Sinzar, 1955 and considerations on the genus Dentitruncus Sinzar, 1955]

Dentitruncus truttae Sinzar, 1955 is redescribed and figured from specimens from Salmo truttae L. collected in the Tirino river (L'Aqula-Italy). The diagnosis of the genus Dentitruncus is completed and the characteristics separating Dentitruncus Sinzar, 1955 from Pseudorhadinorhynchus Achmerov e Drombrowskaja-Achmerova, 1941 are discussed.     

Associations and interactions among intestinal helminths of the brown trout, Salmo trutta, in northern Italy

Species co-occurrences and interspecific associations between intensity of infection were studied in helminth communities of three populations of brown trout, Salmo trutta, from northern Italy. Of the eight helminth species, only four were common enough to be included in the analyses: Pomphorhynchus laevis, Acanthocephalus anguillae, Echinorhynchus truttae and Cyathocephalus truncatus. The observed frequencies of co-occurrences of the different species, based on presence/absence data, did not differ from those predicted by a null model derived from prevalence data. However, the intensity of infection (number of individuals per fish) of different helminth species were generally, but not always significantly, negatively correlated in tests of pairwise associations. Variation in fish sizes and its effect on infection levels, and whether or not two helminth species used the same or different intermediate hosts, had no influence on these findings. Of the few significant negative associations found between pairs of helminth species, none was found in more than one fish population. This suggests that interspecific associations may be condition-dependent: even in apparently similar localities, the same combinations of helminth species show different associations. Without evidence of replicability, it is almost impossible to conclude to the consistent role of competition between any pair of helminth species in the field.     

Parasites of freshwater resident and anadromous Arctic charr (Salvelinus alpinus) in Greenland

Twenty-one metazoan parasite species were found in Arctic charr at three coastal sites in west Greenland, including Neascus sp. and the nematode Pseudoterranova decipiens , new records for Arctic charr. Twelve species are new records for Arctic charr in Greenland. The quantitative composition of the parasite communities varied, but the freshwater species ( Diphyllobothrium ditremwn, Eubothriutn salvelini, Proteocephalus longicollis, Crepidostotnutn farianis ) were usually numerically dominant, even in anadromous fish. The absence from Greenland of Mysidacea, Amphipoda, Ephemeroptera and Odonata excludes parasites requiring such organisms as intermediate hosts, including the cestode Cyathocephalus truncatus , nematodes of the genus Cystidicola , and freshwater acanthocephalans.     

Effect of Acanthocephala infection on the reproductive potential of crustacean intermediate hosts

The effect of a naturally acquired infection by three acanthocephalan parasites Dentitruncus truttae, Echinorhynchus truttae, and Polymorphus minutus on the reproductive potential of their intermediate host, Echinogammarus tibaldii (Amphipoda) from Lake Piediluco (Centre of Italy) was assessed. During May 2007, 1135 amphipods were collected from two different samplings and examined for larval helminths. Forty-five amphipods were infected and of those, 16 were infected with D. truttae (intensity = 1-3 larvae), 15 with E. truttae (intensity = 1-2 larvae), and 14 with P. minutus (intensity = 1 larva). The sex ratio was nearly 1:1 in all examined amphipods. One female infected with D. truttae contained six eggs in the brood pouch and another female infected with E. truttae contained five eggs. However, none of the eight female amphipods harbouring P. minutus larva contained eggs in their brood pouch. Uninfected females of the same size and body length as that of the infected females contained between 20 and 32 eggs. No acanthocephalan species were found to co-occur.     

Identification of life cycle stages of Cyathocephalus truncatus (Cestoda: spathebothriidea) using molecular techniques

Morphological identification of tapeworm species at larval stages (procercoids and cysticercoids) is often difficult because few diagnostic characters are available. In the present study, a molecular approach (sequencing of partial 18S rDNA gene) was used to evaluate the genetic similarity between adult specimens of Cyathocephalus truncatus (Pallas, 1871) (Cestoda: Spathebothriidea) found in fish, its definitive host, and procercoids of the same species recovered from amphipod, Echinogammarus stammeri (Karaman, 1931). Furthermore, cestode cysticercoids of uncertain species were found in the amphipod's hemocoel. The sequences obtained from adults and procercoids were identical, and even very similar to those of C. truncatus available in GenBank, whereas the sequences obtained from cysticercoids differed significantly from those of adults and procercoids, indicating that these larvae belong to another species; later it was demonstrated that they were cysticercoids of Microsomacanthus pachycephala (Linstow, 1972), a cestode of the Hymenolepididae (Cyclophyllidea). The results of this investigation show that the comparison of nucleotide sequence data may avoid misclassification of developmental stages of parasites, which use the same intermediate host.     

A parasite spatially structures its host population

Acanthocephalan parasites are capable of altering the behavior of their intermediate amphipod hosts by inducing hyperactivity and increasing downstream drift. We used a laboratory and field study to investigate how Echinogammarus stammerii amphipods infected by the acanthocephalan Pomphorhychus laevis compensated for downstream displacement and responded to a fish extract predator cue. Experiments conducted in laboratory streams showed infected amphipods drifted more and compensated for drift less than non-infected individuals. When fish extract was added to the channels, non-infected individuals decreased their activity while infected individuals did not. A field study examined the up- and down-stream movements of a population of E. stammerii infected with P. laevis in the River Brenta, Italy. Drift by E. stammerii was positively influenced by acanthocephalan infection. Infected amphipods made up 40% of the drift but accounted for just 5% of the E. stammerii population. Infected individuals, however, were under-represented among upstream-moving amphipods collected from the main river channel and a near-shore migration column, comprising only 3% of sampled individuals. These data suggest that infected individuals may be effectively displaced downstream, creating a mechanism for spatial separation of the non-infected and infected sub-populations.     

On some cestodes parasitizing freshwater fish in Italy.

The paper presents a systematic survey of some cestodes parasitizing freshwater fish in Italy. The following eight species were recorded: Monobothrium wageneri, Cyathocephalus truncatus, Triaenophorus nodulosus (plerocercoids and adults), Bothriocephalus acheilognathi, B. claviceps, Ligula intestinalis (plerocercoids), Schistocephalus sp. (plerocercoids) and Proteocephalus percae from Perca fluviatilis which is reported from freshwater fish in Italy for the first time. All the tapeworms recovered are described and figured.     

On the crustacean hosts of larval acanthocephalan parasites of fishes from a coastal lagoon of River Po Delta

A total of 4664 crustaceans of 2 species of gammarids (Gammarus insensibilis Stock, G. aequicauda Martynon) were collected and examined in search of larval helminth parasites. Larvae of Telosentis exiguus Von Linstow 1901 (Acanthocephala) were found in 6 out of 2806 G. insensibilis so far examined. This is the first record of an intermediate host for T. exiguus, of which a definitive host in Italy has already been indicated by us in Atherina boyeri.     

Helminths in an intensively stocked population of lake trout, Salvelinus namaycush, from Lake Huron

Eighty stocked lake trout Salvelinus namaycush (Salmonidae), collected from 2 locations in Lake Huron in May 1995, were examined for parasites. The parasite fauna of this top predator in Lake Huron was characterized by only 6 helminth species. Echinorhynchus salmonis infected all lake trout with a mean intensity of 163.9. The intensity of this acanthocephalan species significantly increased with host length and weight. Eubothrium salvelini infected 78 lake trout with a maximum number of 81 scoleces counted. Diplostomum sp., Cyathocephalus truncatus, Capillaria salvelini, and Neoechinorhynchus sp. infrequently infected lake trout. The low parasite species richness in these lake trout is believed to be due to their large size at stocking and to the loss of historical enzootic host-parasite relationships that followed the absence of this fish species in Lake Huron for 26 yr.     

Seasonal and ontogenetic dynamics in trophic transmission of parasites

Transmission rates from the intermediate (amphipods) to the definitive hosts (fish) were quantified for two helminth species ( Cyathocephalus truncatus , Cestoda, and Cystidicola farionis , Nematoda) both seasonally and through the ontogeny of the final hosts (arctic charr, Salvelinus alpinus , and brown trout, Salmo trutta ). Amphipods ( Gammarus lacustris ) were important prey for both fish species, especially in the autumn. Both parasite species had low infection levels in amphipods compared to high abundance in fish. The seasonal variations in transmission rate of C. truncatus procercoids from amphipods to fish were in accordance with the observed abundance in fish hosts, being highest in the autumn and lowest during late winter and early summer. During summer, however, the estimated monthly transmission rates of C. truncatus were higher than the observed infection levels in the fish, suggesting restricted establishment success and shorter development time and longevity of the cestode in fish at higher temperatures. The accumulated transmission of C. farionis over the ontogeny of arctic charr was similar to the observed age-specific infection levels, reflecting a high establishment success and longevity of this parasite in charr. In contrast, brown trout exhibited an infection level that was much lower than the estimated transmission rates, suggesting a high resistance against C. farionis in these fish. The magnitudes of the estimated transmission rates were sufficient to explain the paradoxical contrast between low infection levels in the intermediate and high in the final hosts.     

Schistocephalus solidus parasite prevalence and biomass intensity in threespine stickleback vary by habitat and diet in boreal lakes

Trophically-transmitted parasites can affect intermediate host behaviors, resulting in spatial differences in parasite prevalence and distribution that shape the dynamics of hosts and their ecosystems. This variability may arise through differences in physical habitats or biological interactions between parasites and their hosts, and may occur on very fine spatial scales. Using a pseudophyllidean cestode (Schistocephalus solidus) and the threespine stickleback (Gasterosteus aculeatus) as a model parasite–host complex, we investigated the association of infection with host diet composition and stomach fullness in different habitats of two large lakes in southwest Alaska. To become infected, the fish must consume pelagic copepods infected with the parasite’s procercoid stage, so we predicted higher infection rates of fish in offshore habitats (where zooplankton are the primary prey) compared to fish from the littoral zone. Sticklebacks collected from the littoral and limnetic zones were assayed for parasites and their stomach contents were classified, counted, and weighed. Contrary to our prediction, permutational multivariate analysis of variance and principal components analysis revealed that threespine sticklebacks in the littoral zone, which consumed a generalist diet (pelagic zooplankton and benthic invertebrates), had higher parasite prevalence and biomass intensity than conspecifics in the limnetic zone, which consumed zooplankton. These results, consistent in two different lakes, suggest that differences in parasite prevalence between habitats may have been determined by a shift in host habitat due to infection, differential host mortality across habitats, differential procercoid prevalence in copepods across habitats, or a combination of the three factors. This paradoxical result highlights the potential for fine spatial variability in parasite abundance in natural systems.     

Aprocta matronensis in crows (Corvus corone corone) from northern Italy.

Aprocta matronensis (Nematoda, Spirurida) has been found in the orbital cavities of carrion crows. Hooded crows and crows from the hybrid crow zone in the studied areas were not infected. The parasite population showed the typical morphology described for this species. This is the first record of A. matronensis in crows in Italy and in Corvus corone corone. Some hypotheses about the distribution of the parasites in crow populations are discussed.     

Segmentina hemisphaerula: a new molluscan intermediate host for Echinostoma cinetorchis in Korea.

Three species of Planorbidae have been reported from Korea, e.g., Gyraulus convexiusculus, Hippeutis (Helicorbis) cantori, and Segmentina (Polypylis) hemisphaerula. Of these, only H. cantori was reported as the first and second intermediate host for Echinostoma cinetorchis, an important human intestinal parasite in Korea. Segmentina hemisphaerula has also been found to be an intermediate host. In field-collected planorbids, only S. hemisphaerula was found shedding echinostome cercariae and infected with metacercariae of E. cinetorchis, whereas no G. convexiusculus and H. cantori were found to be infected. In experiments with laboratory-bred snails, G. convexiusculus and S. hemisphaerula were susceptible to infection by miracidia of E. cinetorchis, but H. cantori could not be infected. Tadpoles of Rana nigromaculata and laboratory-bred snails of the 3 planorbid species were exposed to E. cinetorchis cercariae shed from field-collected S. hemisphaerula. All tadpoles, S. hemisphaerula, and G. convexiusculus became infected, but no H. cantori were infected. Metacercariae from tadpoles, S. hemisphaerula, and G. convexiusculus were fed to rats per os, and eggs of E. cinetorchis were detected in the rat feces 1 wk later. The rats were killed, and adult E. cinetorchis were recovered from the small intestines. This is the first report of G. convexiusculus as a potential first and second intermediate host and of S. hemisphaerula as a new first and second intermediate host for E. cinetorchis in Korea.     

Species associations among larval helminths in an amphipod intermediate host

Larval helminths that share the same intermediate host may or may not also share the same definitive hosts. If one or more of these helminth species can manipulate the phenotype of the intermediate host, there can be great advantages or severe costs for other helminths resulting from co-occurring with a manipulator, depending on whether they have the same definitive host or not. Among 2372 specimens of the amphipod Echinogammarus stammeri collected from the river Brenta, northern Italy, there was a positive association between two acanthocephalan species with the same fish definitive hosts, the relatively common Pomphorhynchus laevis and the much less prevalent Acanthocephalus clavula.The number of cystacanths of P. laevis per infected amphipod, which ranged from one to five, did not influence the likelihood that the amphipod would also host A. clavula. A third acanthocephalan species, Polymorphus minutus,which matures in birds, showed no association with either of the two other species. These results show that associations among helminth species in intermediate hosts are not random, and are instead the product of selection favouring certain pathways of transmission.     

Ecological factors influencing the composition of the parasite fauna of the European eel, Anguilla anguilla (L.), in Ireland

The parasites of 121 eels from three contrasting sites in the Corrib catchment area, western Ireland, were investigated. Thirteen species, Ergasilus gibbus, Diplostomum gasierostei, Diplostomum spathaceum, Sphaerostoma bramae. Bothrocephalus claviceps, Proteocephalus macrocephalus, Camallanus lacustris, Cucullanus truttae, Paraquimperia tenerrima, Raphidascaris acus, Acanthocephalus clavula, Acanthocephalus lucii and Pomphorhynchus laevis , were recorded. Two species, P. macrocephalus and P. tenerrima , have not previously been reported from Ireland. Microhabitat preferences of the parasites were noted. Variations in the occurrence and intensities of the parasites observed were analyzed in relation to sampling period, host habitat and characteristics of the eel populations studied. A variety of factors were shown to be of importance, including composition of the fish communities and distributional patterns of intermediate hosts and piscivorous birds. Differences were noted in the parasit-ocoenoses of eels in still and running water sites. The occurrence and intensities of infection of several parasite species were shown to be related to age and size of host: the occurrence of B. claviceps. C. truttae, P. tenerrima and R. acus was shown to be related to either age or size of eels, which is accounted for by the fact that eels become increasingly piscivorous with age and increasing size. Little evidence of interspecific interactions was noted.