Pomphorhynchus Laevis Research Articles

Crustacean-acanthocephalan interaction and host cell-mediated immunity: parasite encapsulation and melanization

Host-parasite interactions of Pomphorhynchus laevis (Müller, 1776) in naturally infected amphipod, Echinogammarus stammeri (Karaman), from the Brenta River (northern Italy) are described. A fully developed acanthocephalan larva occupies a large portion of an amphipod's haemocoelic space; thus, the parasite frequently induces displacement of host digestive tract and other internal organs. However, no apparent damage to the host's internal structures was observed. Within the haemocoel of E. stammeri, each larva of P. laevis is surrounded with a membranous layer, formed by microvilli, which maintains intimate contact with the amphipod's internal organs and haemocytes. Three types of circulatory haemocytes were identified based upon their distinct appearance: hyaline cell, semi-granular cell and granular cell. Echinogammarus stammeri haemocytes surrounded acanthocephalan larvae and in some instances a partially and/or totally melanized P. laevis larva was noticed. Interestingly, no melanized larvae were found in E. stammeri parasitized with other acanthocephalans namely Echinorhynchus truttae (Schrank, 1788), Polymorphus minutus (Goeze, 1782) and Acanthocephalus clavula (Dujardin, 1845).

The effects of parasite age and intensity on variability in acanthocephalan-induced behavioural manipulation

Numerous parasites with complex life cycles are able to manipulate the behaviour of their intermediate host in a way that increases their trophic transmission to the definitive host. Pomphorhynchus laevis, an acanthocephalan parasite, is known to reverse the phototactic behaviour of its amphipod intermediate host, Gammarus pulex, leading to an increased predation by fish hosts. However, levels of behavioural manipulation exhibited by naturally-infected gammarids are extremely variable, with some individuals being strongly manipulated whilst others are almost not affected by infection. To investigate parasite age and parasite intensity as potential sources of this variation, we carried out controlled experimental infections on gammarids using parasites from two different populations. We first determined that parasite intensity increased with exposure dose, but found no relationship between infection and host mortality. Repeated measures confirmed that the parasite alters host behaviour only when it reaches the cystacanth stage which is infective for the definitive host. They also revealed, we believe for the first time, that the older the cystacanth, the more it manipulates its host. The age of the parasite is therefore a major source of variation in parasite manipulation. The number of parasites within a host was also a source of variation. Manipulation was higher in hosts infected by two parasites than in singly infected ones, but above this intensity, manipulation did not increase. Since the development time of the parasite was also different according to parasite intensity (it was longer in doubly infected hosts than in singly infected ones, but did not increase more in multi-infected hosts), individual parasite fitness could depend on the compromise between development time and manipulation efficiency. Finally, the two parasite populations tested induced slightly different degrees of behavioural manipulation.

A Common sole (Solea solea Linnaeus, 1758): Actinopterygii: Pleuronectiformes: Soleidae caught in the Coastal Zone of Lithuania

A specimen of common sole (Solea solea) was caught in the southeastern part of the Baltic Sea (ICES fishing subdivision 26) on 6 October 2007. It is the first documented report on this fish species from the southeastern part of the Baltic Sea. The fish had presumably strayed there from waters of higher salinity. It was caught during the hydrological autumn before the disappearance of the seasonal thermocline. The total body length of the specimen was 29 cm, and weight 290 g. It was a 2.5–3 year-old female with its gonads in the second stage of maturity. Parasitic helminths detected in its intestine were typical of brackish-water fish of the southeastern Baltic Sea: three immature specimens of acanthocephalans (Pomphorhynchus laevis Zoega (Muller, 1776)) and larvae L3 of roundworms (Hysterothylacium Aduncum Rudolphi, 1809). No remains of nutritive organisms were found in the stomach and intestine. From a biological viewpoint, it was a specimen that strayed into waters of low salinity beyond the species rep...

Species richness, diversity and specificity of the parasites of bream Abramis brama (L.) and perch Perca fluviatilis L. in the estuary of the Odra River, Poland

Abstract The parasitological studies were carried out on bream and perch from brackish water of Pomeranian Bay and the Szczecin Lagoon — a mouth of the Odra River. Bream and perch hosted 21 and 13 parasitic species, respectively. The species richness and diversity of parasites were much higher for bream and the abundance of parasites in bream was nearly four-fold higher than that in perch. Faunistic similarity of both parasite communities was low. The dominant group of parasites in both fish hosts was digeneans. Five species were specialists of bream, while only one species was a perch specialist. Five new host records have been reported in Poland for the following species: Myxobolus dispar, Hysterothylacium aduncum, Khawia sinensis, Echinorhynchus gadi and Pomphorhynchus laevis.

MODIFICATION OF HOSTS' BEHAVIOR BY A PARASITE: FIELD EVIDENCE FOR ADAPTIVE MANIPULATION

Parasites relying on trophic transmission to complete their life cycles often induce modifications of their host's behavior in ways that may increase their susceptibility to predation by final hosts. These modifications have often been interpreted as parasite adaptations, but very few studies have demonstrated that host manipulation has fitness benefits for the parasite. The aim of the present study was to address the adaptive significance of parasite manipulation by coupling observations of behavioral manipulation to estimates of trophic transmission to the definitive host in the natural environment. We show that the acanthocephalan parasite Pomphorhynchus laevis manipulates the drifting behavior of one of its intermediate hosts, the amphipod Gammarus pulex, but not of a sympatric host, the introduced amphipod Gammarus roeseli. We found a 26.3-28.3 times higher proportion of infected G. pulex in the stomach content of one of the definitive hosts of P. laevis, the bullhead Cottus gobio, than in the benthos. No such trend was observed for G. roeseli. The bell-shaped curve of mean parasite abundance (MPA) relative to host size observed in G. pulex also supported an increased predation mortality of P. laevis-infected individuals compared to uninfected amphipods. Again, no such pattern was observed in G. roeseli. Furthermore, our results indicate that the modifications induced by P. laevis are specific to the definitive host and do not increase the risk of predation by inappropriate hosts, here the adult edible frog Rana esculenta. Overall, our study is original in that it establishes, under field conditions, a direct link between parasitic manipulation and increased transmission to the definitive host, and more importantly, identifies the specificity of the manipulation both in the intermediate host species and toward the definitive host.

Differential influence of two acanthocephalan parasites on the antipredator behaviour of their common intermediate host

Fish acanthocephalans can modify the antipredator behaviour of their intermediate hosts in response to cues from fish predators. However, it is still unclear whether such behavioural changes are adaptive, or are just the consequence of infection. We addressed this question through studying two acanthocephalans, Pomphorhynchus laevis and Polymorphus minutus, and their intermediate host, the amphipod Gammarus pulex. Pomphorhynchus laevis completes its cycle in a freshwater fish, whereas P. minutus exploits waterbirds as final hosts. We first assessed vulnerability of infected and uninfected gammarids to predation by bullheads, Cottus gobio. Pomphorhynchus laevis-infected gammarids were more susceptible to predation than uninfected ones when a refuge was available, whereas no selective predation on P. minutus-infected individuals was recorded, independently of refuge availability. We then quantified refuge use when a bullhead was present in an enclosure or when the enclosure was empty. Individuals of each group significantly increased refuge use in the presence of a bullhead. However, a larger proportion of P. laevis-infected gammarids remained out of the refuge in the presence of a predator, compared with uninfected controls, whereas no such effect was observed in P. minutus-infected ones. Finally, we assessed reaction to bullhead olfactory cues, using a Y-maze apparatus. Pomphorhynchus laevis-infected gammarids spent significantly more time in the predator-scented arm, whereas the reverse was observed in uninfected ones. Polymorphus minutus-infected individuals, however, did not differ from uninfected controls. We discuss our results in relation with the adaptiveness of host manipulation by parasites.

FIELD EVIDENCE OF HOST SIZE-DEPENDENT PARASITISM IN TWO MANIPULATIVE PARASITES

The distribution of parasites within host natural populations has often been found to be host age-dependent. Host mortality induced by parasites is the commonest hypothesis proposed for explaining this pattern. Despite its potential importance in ecology, the parasitism intensity in relation with the host age has rarely been studied in the field. The 2 manipulative acanthocephalans, Polymorphus minutus and Pomphorhynchus laevis, use the amphipod Gammarus pulex as an intermediate host, and their infection intensity and incidence among G. pulex populations were examined by analyzing 2 large samples of hosts collected in eastern France. Both parasites had low prevalence in the host populations, but their mean abundances were highly related with gammarid age. For the 2 acanthocephalans, results reported a disappearance or an absence of heavily infected hosts in the older host age classes. These results suggested that parasites that alter intermediate host behavior for enhancing their transmission success to the definitive host reduce the survival of their intermediate host. In conclusion, manipulative parasites might act as a mechanism regulating the density of gammarid populations.

Do eel parasites reflect the local crustacean community? A case study from the Rhine river system

In 2003, the parasite fauna of 197 European eels Anguilla anguilla, captured at three different locations (Laufenburg, Karlsruhe and Beneeden Leeuwen) in the River Rhine, was analysed. The eels harboured a total of 18 species, among them the protozoa (Myxidium giardi, Myxobolus kotlani and Trypanosoma granulosum), acanthocephalans (Acanthocephalus anguillae, Acanthocephalus lucii, Echinorhynchus truttae, Pomphorhynchus laevis), nematodes (Paraquimperia tenerrima, Pseudocapillaria tomentosa, Camallanus lacustris, Raphidascaris acus, Spinitectus inermis and Anguillicola crassus), cestodes (Bothriocephalus claviceps and Proteocephalus macrocephalus) and monogeneans (Pseudodactylogyrus sp.). The parasite fauna at the different locations is discussed with respect to the crustacean fauna present at these locations. The investigation shows that changes in the composition of the crustacean fauna, due to the anthropogenic breakdown of a biogeographic barrier, are reflected in the composition of the intestinal eel parasite fauna.

Is the host or the parasite the most locally adapted in an amphipod–acanthocephalan relationship? A case study in a biological invasion context

Manipulative endoparasites with complex life cycles can alter their intermediate host immunity and behaviour in ways that increase survival probability within the host body cavity and enhance successful transmission to the definitive host. These parasitic manipulations are variable among and within parasite species and may result from co-evolutionary processes, in which the parasite is constrained for adaptation to the local intermediate host. Hence, arrival of a new host species in a local host population may promote local parasite maladaptation. This study tested the occurrence of local adaptation in two distantly located populations of the acanthocephalan parasite Pomphorhynchus laevis and its effect on the immunity and behaviour of its gammarid intermediate host Gammarus roeseli. This was done in France (an area for which G. roeseli is a recent invader) and Hungary (an area from which G. roeseli was believed to be native). As expected, we found no alteration in G. roeseli’s immune defence and behaviour associated with infection by P. laevis in localities, where the gammarid is invasive. Unexpectedly, we found similar results in Hungarian populations, where the parasite was even more exposed to the host immune response. Whilst these results suggest maladaptation of the parasite to the gammarid in both countries, they also suggest that the gammarid host might be locally adapted to the parasite. Genetic analyses were performed on both the parasite and the host and the results suggest that the two subsets of populations we studied harbour rather isolated host–parasite systems, both probably deriving from a common ancestral population. We propose that G. roeseli is also of recent acquisition in Hungary, and that a recent co-evolutionary history between P. laevis and G. roeseli in association with a long generation time in the parasite has constrained parasite adaptations in Europe or even favoured host adaptation to the parasite.

Differential influence of Pomphorhynchus laevis (Acanthocephala) on brain serotonergic activity in two congeneric host species.

The physiological mechanisms by which parasites with complex life cycles manipulate the behaviour of their intermediate hosts are still poorly understood. In Burgundy, eastern France, the acanthocephalan parasite Pomphorhynchus laevis inverses reaction to light in its amphipod host Gammarus pulex, but not in Gammarus roeseli, a recent invasive species. Here, we show that this difference in manipulation actually reflects a difference in the ability of the parasite to alter brain serotonergic (5-HT) activity of the two host species. Injection of 5-HT in uninfected individuals of both host species was sufficient to inverse reaction to light. However, a difference in brain 5-HT immunocytochemical staining levels between infected and uninfected individuals was observed only in G. pulex. Local adaptation of the parasite to the local host species might explain its inability to manipulate the behaviour and nervous system of the invasive species.

Divergent location of ribosomal genes in chromosomes of fish thorny-headed worms, Pomphorhynchus laevis and Pomphorhynchus tereticollis (Acanthocephala)

We studied distribution of ribosomal DNA (rDNA) sequences along with chromosomal location of the nucleolar organizer regions (NORs) in males of two fish parasites, Pomphorhynchus laevis and Pomphorhynchus tereticollis (Acanthocephala). Fluorescence in situ hybridization with 18S rDNA probe identified two clusters of rDNA in each species, but revealed a remarkable difference in their location on chromosomes. In P. laevis, the rDNA-FISH signals were found in long arms of the first chromosome pair and in short arms of the second pair. Whereas in P. tereticollis, rDNA clusters were located in long arms of both the first and second chromosome pairs. The divergent location of rDNA clusters in the chromosome No. 2 supports current classification of P. tereticollis, previously considered a synonym of P. laevis, as a separate species. A possible scenario of the second chromosome rearrangement during karyotype evolution of the two species involves two successive pericentric inversions. In both species, one or two prominent nucleoli were apparent within interphase nuclei stained with either silver nitrate or a fluorescent dye YOYO-1. However, a single large nucleolus was observed in early stages of mitosis and meiosis I regardless the number of rDNA clusters. Nevertheless, two bivalents with silver-stained NORs in diakinesis and two silver-stained sites in early prophase II nuclei indicated that all NORs are active. This means that each Pomphorhynchus NOR generates a nucleolus, but the resulting nucleoli have a strong tendency to associate in a large body.

Metazoa parasites of the invasive round goby Apollonia melanostoma (Neogobius melanostomus) (Pallas) (Gobiidae: Osteichthyes) in the Gulf of Gdańsk, Baltic Sea, Poland: a comparison with the Black Sea

The known metazoa parasite fauna of the invasive round goby Apollonia melanostoma (formerly Neogobius melanostomus) consists of 12 species. The core of the parasite fauna comprises two species: Cryptocotyle concavum and Diplostomum spathaceum; secondary species are absent; satellite species include Cercariae gen. sp. and Ergasilus sieboldi; rare species are Acanthocephalus lucii, Anguillicola crassus, Bothriocephalus sp., Dichelyne minutus, Hysterothylacium aduncum, Pomphorhynchus laevis, Piscicola geometra, and Tylodelphys clavata. Fifty percent of metazoa parasites that occurred in the invasive round goby in the Gulf of Gdańsk (an invasion that was first detected in 1990) are also typically found in the native Gulf of Gdańsk gobiids. The round goby hosts common fish parasite species: C. concavum and D. minutus, but none that are unique to the species and no Ponto-Caspian parasites. Notably, the parasite species of the invasive round goby in the Gulf of Gdańsk includes species that are atypical for this species in its native habitat. In its new habitat, the round goby variously serves the roles of definitive, second intermediate, and paratenic host for different parasite species. The fish species is involved in a parasitic system that includes fish-eating birds, fishes of different ecological groups (predatory, planktivorous, and benthivorous), and invertebrates.

Infection with an acanthocephalan manipulates an amphipod’s reaction to a fish predator’s odours

Many parasites with complex life cycles increase the chances of reaching a final host by adapting strategies to manipulate their intermediate host’s appearance, condition or behaviour. The acanthocephalan parasite Pomphorhynchus laevis uses freshwater amphipods as intermediate hosts before reaching sexual maturity in predatory fish. We performed a series of choice experiments with infected and uninfected Gammarus pulex in order to distinguish between the effects of visual and olfactory predator cues on parasite-induced changes in host behaviour. When both visual and olfactory cues, as well as only olfactory cues were offered, infected and uninfected G. pulex showed significantly different preferences for the predator or the non-predator side. Uninfected individuals significantly avoided predator odours while infected individuals significantly preferred the side with predator odours. When only visual contact with a predator was allowed, infected and uninfected gammarids behaved similarly and had no significant preference. Thus, we believe we show for the first time that P. laevis increases its chance to reach a final host by olfactory-triggered manipulation of the anti-predator behaviour of its intermediate host.

Some remarks on parasitic infections of the invasive Neogobius spp. (Pisces) in the Hungarian reaches of the Danube River, with a description of Goussia szekelyi sp. n. (Apicomplexa: Eimeriidae)

Summary During a survey of the parasite fauna Neogobius spp., which only recently invaded Hungarian reaches of the Danube River upstream from Budapest, it was found that Neogobius melanostomus and N. fluviatilis had become common species. Neogobius kessleri was less frequent and the previously widespread Proterorhinus marmoratus was drastically reduced. The parasite fauna of the newcomer fish species was characterized by ubiquitous parasites of a wide host range, such as the trematode Nicolla skrjabini, the metacercariae of Metagonimus yokogawai and Apatemon cobitidis, the larval stages of the acanthocephalan Pomphorhynchus laevis and the nematode Rhaphidascaris acus, the glochidia of an Anodonta sp. (Mollusca) and the ciliophoran Ichthyophthirius multifiliis. The specific parasites of Neogobius spp. were represented by three intestinal coccidia: Eimeria daviesae, Goussia kessleri, and a new species described here as Goussia szekelyi sp. n. This survey showed that the rapid invasion of Ponto-Caspian gobies in the northern Danube caused important changes in the fish fauna composition of the Danube River and enriched the parasite fauna of Hungarian fishes.

Metazoan parasites of Neogobius fishes in the Slovak section of the River Danube

Summary Metazoan parasites were investigated in three non-native fishes (monkey goby Neogobius fluviatilis, bighead goby Neogobius kessleri and round goby Neogobius melanostomus) collected from the former and current main channel of the River Danube and from the River Hron, Slovakia, in November 2003. Thirteen parasite species were identified: Triaenophorus crassus, Diplostomum sp., Tylodelphys clavata, Metorchis xanthosomus, Nicolla skrjabini, Gyrodactylus proterorhini, Pomphorhynchus laevis, Contracoecum sp., Raphidascaris acus, Anguillicola crassus, Unio tumidus, Anodonta anatina and Pseudoanodonta complanata. The maximum parasite diversity was found in N. fluviatilis. Total parasite abundance was significantly higher in N. kessleri, but no significant differences among sampling sites were observed. Pomphorhynchus laevis and glochidia of Anodonta anatina reached 100% prevalence in N. kessleri in the new channel of the Danube and, in general, these species were also the most prevalent parasites in all three goby species. For endoparasites, gobies served mostly as intermediate (digenean, cestodes and nematodes) or paratenic (acantocephalan and nematodes) hosts. All parasite species found are common parasites in the Middle Danube basin. No parasites specific to Neogobius, known from their native populations, were observed.

Helminth communities of the barbel Barbus barbus from large river systems in Austria

The composition and diversity of the total and intestinal component endohelminth communities were determined in the cyprinid barbel from three study areas in two large river systems in Austria. Two sample sites in the Danube and one site in the River Drau are the only free flowing stretches of these rivers in Austria. Nine helminth species were identified, with the acanthocephalan Pomphorhynchus laevis being dominant in the Danube, with up to 100% prevalence. In the Drau, where the dominant species was the cestode Bathybothrium rectangulum, species diversity was higher than in the Danube.

Response of the gut neuroendocrine system of Leuciscus cephalus (L.) to the presence of Pomphorhynchus laevis Müller, 1776 (Acanthocephala).

Immunohistochemical tests were applied to sections of intestine of uninfected and Pomphorhynchus laevis Muller-infected chub, Leuciscus cephalus (L.) using 15 different antisera. Nerve cell bodies and fibres immunoreactive (IR) to the anti-bombesin, -Cholecystokinin-8 (CCK-8), -galanin, -Gastrin-Releasing Peptide (-GRP), -Nitric Oxide Synthase (-NOS), -Substance P (-SP), and -Vasoactive Intestinal Peptide (-VIP) sera were observed in the myenteric plexus of uninfected chub. The density of nerve components immunoreactive to these antisera was high in the intestine of the infected fish, especially near the site of attachment. Moreover, numerous nerve fibres, immunoreactive to anti-bombesin, -GRP, -galanin, -SP, and -VIP sera, were encountered in the connective tissue capsule surrounding the bulb and proboscis of P. laevis. The occurrence of P. laevis in the chub gut significantly increased the number of endocrine cells per intestinal fold immunoreactive to galanin, met-enkephalin and leu-enkephalin antisera. CCK-8, Neuropeptide Y and glucagon-like immunoreactive cells were less numerous in the intestine of infected chub. A large number of cells in the tunica propria-submucosa of L. cephalus infected with P. laevis were immunoreactive to anti-serotonin and -leu-enkephalin sera.

Histochemistry of glycoconjugates in mucous cells of Salmo trutta uninfected and naturally parasitized with intestinal helminths

Mucus secreted onto the surface of the intestine forms a physical barrier to invading parasites so that a possible attachment of helminths to the surface is prevented and their expulsion by peristalsis facilitated. In mammals, intestinal parasites induce hyperplasia and hypertrophy of intestine goblet cells and provoke changes in the mucus composition. In fish, this topic has received less attention. In the present investigation, histochemical methods were employed to compose intestinal mucous cell numbers and their glycoconjugate composition were compared by uninfected brown trout Salmo trutta and in S. trutta parasitized with Cyathocephalus truncatus or Pomphorhynchus laevis. When P. laevis was present in the intestine of the brown trout, the total mucous cell number, and the number of mucous cells containing acid or mixed glycoconjugates were significantly enhanced. No significant change in the total mucous cell number was detected in the intestine of fish parasitized with C. truncatus in comparison with uninfected brown trout. A significant increase was observed in the number of both acid (especially sulphated) and mixed glycoconjugates containing mucous cells as well as a significant decrease in the number of neutral glycoconjugates containing mucous cells. When intestinal helminths were present, the thickness of the adherent mucous gel increased. In a limited number of other fish species, the occurrence of gill and intestinal parasites has been reported to increase the mucosal glycoconjugate secretions. Our study is the first quantitative report on the effects of intestinal helminths on the density of mucous cells and mucus composition in a fish species.

Parasites of young Baltic cod, Gadus morhua callarias L. in the Gulf of Puck, Poland

Background. The hitherto published records of the parasite fauna of Baltic cod, Gadus morhua callarias cover commercially-caught adult fish. The aim of this study was to determine the composition of the parasite fauna of young Baltic cod, the relevant infection parameters and to relate those data to published records on the diet of cod. Material and Methods. This survey was carried out on 154 young cod, caught in May and June 2002 in the Gulf of Puck, the Baltic Sea, Poland. The fish were examined using standard methods applied in parasitology. Results. No external parasites were found. In the digestive tracts of 58 cod, 3 species of parasites belonging to 2 higher taxa (Nematoda and Acanthocephala) were found. The dominant parasite was Echinorhynchus gadi Zoega in Muller, 1776. The mean abundance ranged from 0.15 to 2.75. The prevalence ranged from 14.6%, in the smallest fish, to 66.7% in the larger ones. Only two acanthocephalan specimens of Pomphorhynchus laevis (Zoega in Muller, 1776) and five nematode larvae of Hysterothylacium aduncum (Rudolphi, 1802) were found. Conclusion. The parasite fauna of young Baltic cod is significantly sparser than in larger fish examined by other authors. It is suggested that the occurrence of the species found, can be related to the composition of diet available.

Intestinal helminth parasites in flounder Platichthys flesus from the River Thames: an infracommunity analysis

An analysis was undertaken of intestinal helminth communities in flounder Platichthys flesus from two sites on the River Thames. A comparison was made between helminth community richness and diversity from these sites at the component and infracommunity levels. At the component community level, a richer and more diverse parasite community was found in flounder from the Tilbury location (marine influence) than that from the Lots Road location (freshwater influence). At the infracommunity level, more parasite species and parasite individuals per host were found at Lots Road and the percentage of similarity values were low at both locations. Helminth species with high prevalence values in the parasite communities of the flounder are the dominant species in any individual fish, harbouring multi-specific infections. The presence of more invertebrate species, which are intermediate hosts in the helminth life cycle in the Thames, fish vagility and the high prevalence and abundance values of Pomphorhynchus laevis in the flounder, may explain the differences between the two locations.