Trophically transmitted parasites in wild Atlantic salmon post‐smolts from Norwegian fjords

The community structure of trophically transmitted intestinal helminths of Atlantic salmon Salmo salar post‐smolts was highly variable among four fjords in Norway. There were no severely pathogenic parasite species. Post‐smolts from the southernmost Trondheimsfjord had a higher diversity of freshwater parasite species compared to the three northern fjords (Tanafjord, Altafjord and Malangen). In contrast, the highest diversity and proportion of marine species was found in the three northern fjords. Post‐smolts were generally more infected with marine parasites in the outer rather than inner parts of all of the fjords. The prevalence of the acanthocephalan Echinorynchus gadi (range: 13–42%) and marine trematodes (range: 14–47%) was higher in post‐smolts in outer zones of the northern fjords than in fish from Trondheimsfjord (0 and 6%, respectively). The within‐fjord variability and north‐south geographical gradient in parasite infection patterns reflected differences in marine feeding of the post‐smolts on potential intermediate hosts such as amphipods ( E. gadi ) and fish larvae (trematodes), which were higher in the northern fjords (range: 27–28 and 67–85%, respectively) than in Trondheimsfjord (5 and 19%, respectively). High intensities of marine parasites suggest that some post‐smolts from northern fjords may have a prolonged fjord‐feeding compared to those from Trondheimsfjord. Parasites of both freshwater and marine origin appear to be suitable as bio‐indicators of feeding and migratory pattern of Atlantic salmon post‐smolts and preadults during their seaward migration.     

Infection dynamics of Cichlidogyrus tilapiae and C. sclerosus (Monogenea, Ancyrocephalinae) in Nile tilapia (Oreochromis niloticus L.) from Uganda

The infection dynamics of the gill monogeneans Cichlidogyrus tilapiae and C. sclerosus on Oreochromis niloticus with respect to habitat type (reservoir, stream, ponds and cages), host sex, size and seasons was determined between January and November 2008. During the study period, 45.2% of the 650 fish examined were infected with Cichlidogyrus spp. The infected hosts harboured an average of 8.6 ± 3.4 parasites/fish. Across habitat types, the proportion of infected fish was not statistically different. In contrast, the number of parasites recorded on infected fish from different habitat types differed significantly. The highest parasite number was recorded in reservoir-dwelling fish and lowest in stream-dwelling hosts. Concerning sex, more female O. niloticus were infected and harboured a high number of parasites than male and sexually undifferentiated fish. A weak negative relationship was found between rainfall and monthly parasite infections. However, a higher number of parasites and proportion of infected hosts were found during dry than in wet seasons, except in ponds. Results of this study show that differential exposure due to changes in fish behaviour associated with habitat modification and sex may account for the infection difference across the sampled sites. Meanwhile, rainfall and the associated hydrological events are important factors regulating monogenean infections in tropical aquatic environments. The continuous presence of Cichlidogyrus spp. in fish provides evidence of possible parasite outbreaks, indicating the application of biosecurity measures as crucial for the success of intensive fish farming.     

Effects of dexamethasone on host innate and adaptive immune responses and parasite development in rainbow trout Oncorhynchus mykiss infected with Loma salmonae

The effects of dexamethasone (dex) treatment on infections with the microsporidian parasite, Loma salmonae and the effects of dex on initiation of the adaptive immune response were investigated in rainbow trout, Oncorhynchus mykiss experimentally infected with the parasite. Dex treatment resulted in significantly higher infections with the parasite in the gills and other internal organs, suggesting that dex inhibits aspects of the innate immune response to L. salmonae; the heavier infections in the gills and organs of rainbow trout resembled infections seen in Chinook salmon. Mean xenoma counts per microscope field in the gills of fish infected with L. salmonae treated with dex or left untreated were 169 and 30, respectively. Although higher numbers of xenomas were observed in dex treated fish, the xenomas were generally smaller in size than in infected control fish. The xenomas in dex treated fish showed morphological signs of degeneration including loss and degeneration of early parasite stages, accumulation of amorphous material in xenomas, and infiltration with phagocytic cells containing degenerated parasites. The xenomas in infected untreated fish had larger xenomas with a more uniform size and contained identifiable parasite stages in the cytoplasm. According to this study, once fish have developed an adaptive immune response to the parasite by previous exposure, then fish have 100% protection to reinfection even when treated with heavy doses of dex. L. salmonae immune fish treated or untreated with dex during reinfection with the parasite developed no xenomas in the gills 6 weeks post reinfection. These results indicate that once the cellular response is primed to L. salmonae, then dex related immunosuppression does not reduce the effectiveness of the adaptive immune response.     

Influence of environmental changes in the north-western Atlantic Ocean on a parasite, Echinorhynchus gadi (Acanthocephala) of Atlantic cod ( Gadus morhua) occurring off coastal Labrador, Canada

A study was conducted to determine the influence of environmental change on an endoparasite, Echinorhynchus gadi (Acanthocephala) of Atlantic cod (Gadus morhua) over a 30-year period off the coast of Labrador in the north-western Atlantic, North Atlantic Fisheries Organization subareas 2J-3K. Cod, once an abundant fish species that had been commercially exploited for many decades, declined precipitously during the mid-1980s onwards. This decline was attributed to climatic changes that affected the entire food chain from zooplankton to fish, sea birds and marine mammals. A monitoring programme was introduced, sampling cod by otter trawling using research vessels. The fish, after capture, were frozen at - 20 degrees C, subsequently thawed and the digestive tract removed and examined for the parasite in 2006. Data from samples taken in 1976, 1980-81, 1986, 1990, 2000 and 2003 were compared statistically with those collected in 2006. The results indicate a decline in the prevalence and mean abundance of E. gadi in 1986 with a minimum in 2000 but increasing gradually in 2003 and 2006. These changes were coincident initially with a decline of oceanic temperature and the entire food web, including capelin (Mallotus villosus), a preferred prey of cod and primary source of E. gadi. The increase in prevalence and mean abundance of the parasite in 2006 were associated with an increase of oceanic temperature and the return of small schools of capelin to offshore areas. Cod older than 4 years harboured a greater abundance of E. gadi than younger fish, while no difference was observed between the sexes. The results suggest that the abundance of E. gadi can be useful as a bioindicator of environmental changes in the north-western Atlantic.     

The genera Ceratomyxa Thélohan, 1892, Leptotheca Thélohan, 1895 and Sphaeromyxa Thélohan, 1892 (Myxosporea: Bivalvulida) in gadid fish of the Northeast Atlantic

The gall-bladders of four species of gadid fish from the North Sea and Norwegian waters were examined for myxosporeans. The host species were cod Gadus morhua L. (350 examined), haddock Melanogrammus aeglefinus (L.) (592 examined), saithe Pollachius virens (L.) (205 examined) and whiting Merlangius merlangus (L.) (368 examined). Four species of myxosporeans are redescribed from these fish. Ceratomyxa arcuata Thélohan, 1892 was the most common species and was found in whiting (42.8%) and cod (0.6%). Leptotheca informis Auerbach, 1910 was found only in whiting (6.5%). L. longipes Auerbach, 1910 was found only in haddock (6.2%). Sphaeromyxa hellandi Auerbach, 1909 was found in haddock (9.1%) and whiting (0.3%). None of the saithe examined, and no cod or haddock from Norwegian waters, was infected with these myxosporeans. All four species appear to have distributions limited to the Northeast Atlantic, with S. hellandi having a more northern distribution than the other three. The validity of reports of C. arcuata, L. informis and L. longipes from outside this area is discussed.     

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

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

Histopathological changes caused by Enteromyxum leei infection in farmed sea bream Sparus aurata

Histological examinations were carried out on the stomach, pyloric caeca and 4 different parts of the intestine, as well as the rectum, hepatopancreas, gall bladder and spleen of 52 sea bream Sparus aurata spontaneously infected by Enteromyxum leei. Fifteen fish from a non-infected farm were included as a control. Clinical signs appeared only in extensively and severely infected fish. We observed Enteromyxum leei almost exclusively in the intestinal tract, and very rarely in the intrahepatic biliary ducts or gall bladder. We observed heavily infected intestinal villi adjacent to parasite-free villi. Histological changes indicated a parasite infection gradually extending from villus to villus, originating from an initial limited infected area probably located in the rectum. The parasite forms were exclusively pansporoblasts located along the epithelial basement membrane. Periodic acid-Schiff (PAS)-Alcian blue was the most useful histological stain for identifying the parasite and characterising the degree of intestinal infection. We observed severe enteritis in infected fish, with inflammatory cell infiltration and sclerosis of the lamina propria. The number of goblet cells was considerably and significantly decreased in heavily infected fish. The intestines of 4 of the 5 survivor fish were totally free of parasites and showed severe chronic enteritis with a regenerative epithelium, suggesting that an acquired immune process may spontaneously eliminate parasites.     

Experimental transmission of Enteromyxum scophthalmi (Myxozoa), an enteric parasite of turbot Scophthalmus maximus

Several experiments were designed to elucidate the modes of transmission of the myxozoan parasite Enteromyxum scophthalmi to turbot Scophthalmus maximus. Direct transmission of the infections was achieved by cohabitation of infected and test fish, through waterborne contamination from the effluent of a tank containing infected fish, and via the oral route using parasite-infected intestines. The transmission of the turbot enteromyxosis was successful in all the fish exposed to the parasite by the 3 routes; accumulated mortality reached 100% at the end of most experiments. The progress of the infections was monitored by study of the histopathology. Influence of the mode of exposure was observed, with the oral route the fastest to initiate the parasite infections. The temperature also affected the course of the infections, which were established earlier at higher water temperature. Direct fish-to-fish transmission of the disease explains the rapid spreading of the turbot enteromyxosis in farms.     

Myxidium leei (Myxozoa) infections in aquarium-reared Mediterranean fish species.

An episode of parasitic enteritis causing trickling mortalities at an exhibition aquarium reproducing Mediterranean ecosystems was found to be caused by the myxozoan parasite Myxidium leei Diamant, Lom & Dykova 1994. The myxozoan was recorded in 25 different fish species belonging to 16 Genera, 10 Families and 4 Orders. It was mainly detected in the intestine of affected fish, and was responsible for severe chronic enteritis. The parasite was probably introduced into the facilities with infected wild fish, and transmitted directly from fish to fish by cohabitation, transfer of infected material and necrophagia. Fish belonging to the Families Labridae and Blenniidae appeared as most susceptible, and the incidence of infections in members of the Sparidae was low. This study significantly widens the host spectrum for this virulent parasite and now includes many ubiquitous coastal Mediterranean species. Wild fish may have a significant role in the transmission of myxidiosis of cultured sparid fish.     

The effect of Schistocephalus solidus infection on meal size of three‐spined stickleback

The effect of infection with the pseudophyllidean cestode Schistocephalus solidus on the meal size of individually housed three‐spined stickleback Gasterosteus aculeatus was quantified. Infected fish harboured plerocercoid loads that contributed from 1·1 to 33·9% of their total mass. Across this range of infection levels, the presence of S. solidus infection had no significant directional effect on standard length ( L _S) corrected meal size of host three‐spined sticklebacks. Amongst multiply infected fish there was a significant negative relationship between L _S‐corrected meal size and the proportion of host mass contributed by S. solidus parasites. This relationship, however, did not hold for singly‐infected fish. Furthermore, the data suggest that multiply‐infected fish that harbour a combined mass of parasites contributing < c . 15% to host body mass might exhibit meal sizes that exceed those of length‐matched uninfected fish. The results suggest that although heavy infections can significantly reduce the meal size of heavily infected three‐spined sticklebacks, in the early stages of multiple S. solidus infections host food intake may increase. The probable causes of these differential effects on meal size and their consequences for the host‐parasite system are discussed.     

Is reduced body growth of cod exposed to the gill parasite Lernaeocera branchialis a cost of resistance?

Three hundred and sixty-nine cod Gadus morhua were individually marked and caged for 19 months. During this period, each cod was inspected several times for Lernaeocera branchialis . Growth in four groups of cod, identified by their infection history, were compared. During the caging, 79% of the cod remained uninfected, 8·5% were infected, but lost the parasite, 8% were infected with one parasite and 4·5% were infected with more than one parasite. The infected fish either harboured the parasite at caging or were infected during the study period. The highest rate of increase, both in body mass and in standard length ( L _S), was recorded in the group of male fish infected with one parasite throughout the experimental period. Conversely, those males free from infection showed significantly lower growth. The observed differences in growth could not be explained by changes in variables related to reproductive strategies. The alternative explanation for these results is that resistance to L. branchialis was associated with costs in terms of reduced growth of body mass and L _S.     

Anguillicola in Dutch Eelfarms; Current State

Anguillicola crassus was introduced into Dutch eelfarms by infected stocking material originating from inland fisheries. Within farms, suitable intermediate hosts for transmission of the parasite are available and uninfected stock becomes rapidly infected. In farming situations, only very heavy infections with the parasite can cause significant damage to fish, mainly by secondary infections. Treatment of fish infected with A. crassus is possible with L-Levamisole as a bath treatment or mixed with the feed, which results in complete immobilisation of the nematode. Transmission of the infection within farms can be controlled by keeping populations of copepods low. This can be accomplished by avoiding accumulations of organic matter within systems and/or control with chemical means. It can be stated that Anguillicola crassus does not pose the threat to intensive eel culture it once seemed to be.     

Distribution of schistosome infections in molluscan hosts at different levels of parasite prevalence

Biomphalaria glabrata snails infected with Schistosoma mansoni were collected during consecutive seasons from a site in Brazil known to have a very high percentage of infected snails. Schistosoma mansoni cercariae from single snails were used to infect individual mice, and the recovered adult worms were genetically assessed using a mtVNTR marker. The number of unique parasite genotypes found per snail was compared to expected abundance values, based on the infection prevalence at the site, to determine the distribution of S. mansoni infections within the snail population. The observed distributions and those from previous studies were used to examine the relationship between schistosome prevalence and aggregation across a wide range of prevalence values. Our analysis showed that prevalence was inversely related to the degree of parasite overdispersion, and at high prevalence, S. mansoni infections were randomly distributed among snails.     

Occurrence of Bucephaloides gracilescens metacercariae in three species of gadoid fish

Bucephaloides gracilescens metacercaria is a common encysted trematode parasite of whiting, Merlangius merlangus (L), haddock, Melanogrammus aeglefinus (L), and hake, Merluccius merluccius (L), in the Irish Sea. The incidence of infection over an 18-month period was uniformly high (whiting, 95%; haddock and hake, 100%). The major site of infection in all three hosts was the cranial fluid surrounding the brain. Large numbers of cysts were also found embedded in the spinal nerves posterior to the anus in haddock and hake and in the auditory capsules in whiting and haddock. Other sites of infection included the spinal canal, cranial nerves (V, VII, VIII, X), eye muscles, orbits and nasal region. Results are discussed in the light of previous records of gasterostome trematodes in the Gadidae.     

Experimental transmission, development, and effects of a parasitic copepod, Lernaeocera branchialis, on Atlantic cod, Gadus morhua

Development and effects of adult Lernaeocera branchialis were studied following experimental transmission to Atlantic cod, Gadus morhua. Growth from the detection of pennella stages to mature adults was approximately 9-10 mo (September-June of the following year) at which time eggs were released and the adult parasites degenerated. Cod from all size groups were susceptible but the prevalence of infection was greater in small fish. Peak mortality, about 30%, occurred within 4 mo after infection and was greatest in young fish with multiple infections. Death was associated with emaciation, blood loss, open lesions, and probable occlusion of branchial blood vessels and/or ventral aorta. Infected fish, especially subadults that survived, consumed less food, gained less weight, had a lower conversion factor, and were substantially smaller than uninfected controls through a 32-wk period. Many of these fish displayed hyperactivity. Large cod that survived the infection and harboured 1 parasite were apparently unaffected but died when stressed. A previous infection conferred no protection against reinfection. Multiple infections delayed gonadal maturation and resulted in significantly lower gonadal somatic indices than in controls. Exposure of infected fish to crude oil fractions or to infection with a hemoprotozoan, Trypanosoma murmanensis, culminated in mortality, weight loss, or low organ somatic indices. It is estimated that considerable losses through mortality and weight gain in young fish occur each year in coastal areas from infections by L. branchialis, particularly in one area where it was estimated that 20% of the population was infected.     

倪氏复口吸虫在稀有鮈鲫体内的移行及对其耳石微结构的影响

倪氏复口吸虫是我国淡水鱼类的一种常见的危害严重的寄生虫。利用稀有鮈鲫作为寄主,研究了倪氏复口吸虫在其体内的移行途径,并观察了复口吸虫的感染是否在寄主耳石上留下标记轮。倪氏复口吸虫尾蚴从稀有鮈鲫体表的各个部位侵入,但主要集中在头部,侵入体内的尾蚴通过肌肉和结缔组织直接进入眼球。感染倪氏复口吸虫的稀有鮈鲫耳石表面微结构发生变化,部分鱼耳石上出现明显的标记轮。     

The population biology of the acanthocephalan Pomphorhynchus laevis (Müller) in the River Avon

Regular samples of Gammarus pulex and dace Leuciscus leuciscus and occasional grayling Thymallus thymallus and chub L.cephalus were examined from the River Avon, Hampshire, for the presence of the acanthocephalan Pomphorhynchus leavis . The parasite only occurred in medium sized Gammarus due to lower probability of contact with small gammarids and stunted growth and selective mortality amongst older infected ones. No cycles in incidence or development of the parasite in G.pulex were observed. The parasite infected gammarids and grew in all months, and cystacanths were available throughout the year. Despite seasonal feeding activity and dietary preferences, fish fed on Gammarus and acquired infections in all months. Dispersion of P.laevis within the fish population was related to host feeding behaviour. No evidence of seasonal cycles in incidence or intensity of infection in fish was found, and observed monthly changes in the parasite population were related to changes in size structure of the host sample. In dace and grayling P.laevis grew little and matured only in summer, but in chub it grew and produced acanthors all year. The parasite population in fish appeared to be in a state of dynamic equilibrium and gain and loss of parasites took place throughout the year with the level of infection at any moment being determined primarily by the feeding behaviour of the host. This relationship between host diet, water temperature and parasite population size is discussed, and P.laevis in the R. Avon compared with other localities and other parasites.     

Impact of a castrating trematode, Neophasis sp., on the common whelk, Buccinum undatum, in the northern Gulf of St. Lawrence

We observed heavy trematode infections of whelks, Buccinum undatum, from the Mingan Islands, eastern Canada, by larval stages of a species of Neophasis. Only sexually mature whelks were infected, 23% of mature females and 15% of mature males, and prevalence increased rapidly with whelk size. In most cases the parasite completely occupied the gonad, causing castration. The digestive gland was also infected, although to a lesser degree (0% to 50% occupation), and a marked reduction in the mass of the penis was associated with the infection. A decrease in the proportion of whelks with a highly infected digestive gland between May and August 1994 suggested mortality of infected individuals. Whelks held for 12 to 15 months in the laboratory retained the infection but did not show significant mortalities (possibly because food was abundant and predators absent). The larval stage of Neophasis sp. found in whelks was a cercaria; however, the tail easily detached. The putative infective stage (metacercaria) was not observed but may be present in whelks in late winter and early spring. Other trematode parasites observed were adult Steringophorus furciger in the stomach and larval Renicola sp. in the digestive gland.     

Host manipulation by Ligula intestinalis: a cause or consequence of parasite aggregation?

Previous investigations suggest that the infection of the cyprinid roach, Rutilus rutilus, with the larval plerocercoid forms of the cestode, Ligula intestinalis, creates behavioural and morphological changes in the fish host, potentially of adaptive significance to the parasite in promoting transmission to definitive avian hosts. Here we consider whether these behavioural changes are important in shaping the distribution of parasite individuals across the fish population. An examination of field data illustrates that fish infected with a single parasite were more scarce than expected under the negative binomial distribution, and in many months were more scarce than burdens of two, three or more, leading to a bimodal distribution of worm counts (peaks at 0 and >1). This scarcity of single-larval worm infections could be accounted for a priori by a predominance of multiple infection. However, experimental infections of roach gave no evidence for the establishment of multiple worms, even when the host was challenged with multiple intermediate crustacean hosts, each multiply infected. A second hypothesis assumes that host manipulation following an initial single infection leads to an increased probability of subsequent infection (thus creating a contagious distribution). If manipulated fish are more likely to encounter infected first-intermediate hosts (through microhabitat change, increased ingestion, or both), then host manipulation could act as a powerful cause of aggregation. A number of scenarios based on contagious distribution models of aggregation are explored, contrasted with alternative compound Poisson models, and compared with the empirical data on L. intestinalis aggregation in their roach intermediate hosts. Our results indicate that parasite-induced host manipulation in this system can function simultaneously as both a consequence and a cause of parasite aggregation. This mutual interaction between host manipulation and parasite aggregation points to a set of ecological interactions that are easily missed in most experimental studies of either phenomenon.     

Further studies on Capillaria philippinensis: development of the parasite in the Mongolian gerbil

Capillaria philippinensis larvae from the digestive tract of a Northern Luzon freshwater fish (Hypselotris bipartita) experimentally exposed to embryonated eggs, were given by stomach tube to Mongolian gerbils (Meriones unguiculatus). The larvae developed into adults within 10 to 11 days and female worms produced larvae within 13 to 14 days. These larvae developed into second generation adults by days 22 to 24 and the second generation females produced eggs that were present in the feces of the animal on the average 26 days after infection. Most females were oviparous but a few larviparous females were always present. The gerbils died on an average of 46 days after infection, with the highest numbers of worms recovered between days 36 and 46. All stages of the parasite were generally found at necropsy. Gerbils developed patent infections after receiving 2 or 3 laeval from fish, and 852 to 5,353 worms were recovered at necropsy. These studies show that autoinfection in an integral part of the life cycle of C. philippinensis, both initially and in maintaining the infection. The natural transmission of the parasite was demonstrated when H. bipartita from a lagoon in the endemic area were fed to gerbils and 3 became infected. The parasite can also be maintained in the laboratory by transfer of worms by stomach tube from the small intestines of an infected gerbil to a clean gerbil.