Effect of concurrent infections of Lernaeocera Branchialis (Copepoda) and Trypanosoma murmanensis (Protozoa) on Atlantic cod, Gadus morhua

A study was initiated to ascertain the prevalence, effect and interaction of the adult stages of the parasitic copepod, Lernaeocera branchialis, on Atlantic cod concurrently infected with a hematozoan, Trypanosoma murmanensis, by comparing condition (K) factor, organ somatic indices, hematological values and lipid concentrations of the liver from infected and uninfected fish of comparable length. Prevalence of the copepod varied from 9 to 21% and was highest in fish examined on the southern coast of Newfoundland. Body condition and blood values were significantly lower in young cod infected with two parasites whereas only K-factor was altered in two size classes parasitized by one copepod. Although lipid concentrations were similar in three length groups of fish without and infected with L. branchialis, the pooled values were significantly greater among the infected group. Mortality occurred only in juvenile cod infected with the copepod and T. murmanensis concurrently. Cod which survived dual infections had lower K-factor and blood values than controls or fish harboring single, parasitic infections. It is concluded that an infection with an adult L. branchialis does not impair the health of fish in this area of the northwestern Atlantic Ocean, but the presence of T. murmanensis concurrently can potentiate its effect.     

Influence of Lernaeocera branchialis (Crustacea: Copepoda) on growth rate of Atlantic cod, Gadus morhua

Influence of Lernaeocera branchialis, a hematophagous copepod, on the growth rate of Atlantic cod, Gadus morhua, was investigated in fish of various sizes. Initially, it appeared that growth, over a 16-mo period, was reduced when single or multiple infections were present. We then examined growth rate by comparing food consumption, weight gain, food conversion efficiency, and condition (k) factor over a 2-mo period and subsequently over a 4 wk in control and experimentally infected fish. Total body weight and length of each fish, controls and infected were determined before and after feeding known weights of food. Adults infected with young parasites consumed more food and gained more weight than controls, especially in the first month, but food conversion efficiency and k-factor were greater than those of controls after 2 mo, but food efficiency was still lower than in controls. In 2 groups of young infected fish, all values were consistently lower than those of uninfected fish of comparable size during the 2-mo period. Three additional trials on immature cod confirmed that infected fish consumed less food and exhibited less growth than infected controls. Our results suggest that only adult cod infected with immature parasites compensate for the infections by increasing food consumption, thus resulting in a transitory weight gain. Additionally, parasites that have completed their reproductive activities still produce subtle effects in the form of low food conversion efficiency in their hosts.     

Lernaeocera branchialis: a potential pathogen to cod ranching

A study was carried out to determine the effect of Lernaeocera branchialis on Atlantic cod infected in the laboratory and in the field and also to ascertain its effect on cod-ranching. Sixty-four percent (308) of 481 cod acquired infections in the laboratory and 33% (159) of the infected fish died over a 4-yr period. About 74% of the deaths occurred within 4 mo of the infection. Monthly samples of cod collected adjacent to a cod-ranching operation showed an initial prevalence of 30% that subsequently decreased in the following 2 mo to 15%. Prevalence of the infection also decreased among the initial field sample of cod that were kept alive, from 30 to 17% during the same 2-mo period and to 9% after 8 mo and was associated with death caused by the parasite. Cod examined at intervals after infection showed evidence of reduced weight gain, lower liver somatic index, liver lipid, and blood values than controls. A field sample taken from the same area during the summer of the following year indicated a prevalence of 12%. This higher than usual prevalence (4-6%) was associated with retention of the intermediate host, Cyclopterus lumpus, that provided an additional source of infective stages. It is likely that increased parasitism could affect the success of the cod-ranching operation in view of the parasite's devastating effects on its hosts.     

Prevalence and influence of Loma branchialis (Microspora) on growth and mortality in Atlantic cod (Gadus morhua) in coastal Newfoundland

A study was conducted to determine the prevalence, geographical distribution, and effects of a microsporan parasite, Loma branchialis, in Atlantic cod in coastal Newfoundland. The parasite was identified microscopically as opaque, ovoid xenomas, primarily in the gills, heart, and spleen. Although widely distributed in young fish inhabiting 7 coastal localities, prevalence was 1-7% in general, <0.01% in older and large fish, but 78% in market-size cod from a commercial farm. Some of the latter fish were emaciated, and approximately 2 mo after the parasite was detected, 63% succumbed with a massive infection. Condition factor and blood values were significantly lower than those in reference fish. An experimental study conducted over 2 yr revealed that mass gained and condition factor were significantly lower in infected cod than in controls at the termination of the study. Feed consumption, mass gained, feed conversion efficiency, and condition factor also were significantly lower in another group of infected cod of marketable size studied over 12 wk. Xenomas also were observed in the heart and gills of year class II cod reared in a hatchery. Loma branchialis is considered to be a potential pathogen in both hatchery-reared and net pen-cultured cod in Newfoundland.     

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.     

Changes in numbers and growth of Ligula intestinalis in the spottail shiner (Notropis hudsonius), and their roles in transmission

Eighteen species of fishes were collected during the open water (1985-1987) and winter seasons (1985-1986) from Dauphin Lake, Manitoba, Canada (51 degrees 17'N, 99 degrees 48'W) and examined for plerocercoids of Ligula intestinalis (L.). Plerocercoids were most prevalent (5.3%) in spottail shiners (Notropis hudsonius), the major fish host for Ligula in Dauphin Lake. Detailed analysis of the spottail shiner-Ligula host-parasite system revealed that the number of plerocercoids differed between years and among habitats but there was no statistically significant seasonal pattern; recruitment of new worms was highest in young fish and decreased with age, and infected spottails had reduced gonad development. Analysis of host and parasite growth revealed that the soma of male spottails infected with Ligula weighed more but had a reduced growth rate. Growth rate of females was unaffected by Ligula but somatic weight was slightly increased. This appears to be related to the greater metabolic stress on infected males. Based on increased mean somatic weight and skewness of the weight distribution for infected fish, we propose that infected spottails are subjected to size-selective mortality. Some of the contradictions in the literature may be attributed to underestimated prevalence due to increased numbers of spawning fish in the spring, mixed age-classes of Ligula in separate age-classes of fish, and differential effects on growth due to infection in male versus female hosts.     

The effects of Lernaeocera branchialis on the Merlangius merlangus population in the Medway Estuary

Whiting entering estuarine waters during autumn are largely free from the copepod Lernaeocera branchialis (L.). Infection soon follows and, between 1973 and 1975, an average 40.4% whiting were infected. The parasite's effects on fish weight over this period are assessed and, in a separate study, its effects on the host's lipid biochemistry determined. Mature adults of L. branchialis caused a significant reduction in body weight. Liver lipid content was also lower in these individuals, by more than 50%. Phospholipid levels were lower but cholesterol readings were greater in infected fish. Fatty acid composition of liver lipids appeared unaffected.     

Seasonal changes in energy and the energy cost of spawning in Gulf of Alaska Pacific cod

In the Gulf of Alaska, adult Pacific cod exhibited an annual cycle of condition, gonad index and liver index in which maximum values occurred in ripe fish in March and minima in July. About 30–31 % of prespawning stored energy was expended during the spawning effort. The energy associated with spawning derived from liver (24% and 18%), somatic tissue (22% and 33%) and gonad (53% and 48%) for females and males, respectively. Liver index and gonad index at the time of sampling were directly related in females, but in males gonad index was best related to liver index 1–3 months earlier.
The Pacific cod is very similar to the Atlantic cod in terms of energy cycling, maximum gonad sizes, energy expended during spawning and gonadal contribution to energy expenditure. However, in Pacific cod, somatic tissue contributes markedly to energy expended during reproduction. The Pacific cod cod differs from the walleye pollock with respect to gonad index (13% and 20%ν. 20% and 8% for females and males, respectively), spawning weight loss (25%ν. 38%), liver energy loss during spawning (71%ν. 55%) and energy cost of spawning.     

The dynamics of Baltic fish stocks based on a multispecies stock production model

The multispecies stock‐production model of Horbowy developed in 1996 was further extended to include the unexploited part of a stock. The model was then applied to simulate stock dynamics and species interactions of cod, herring, and sprat in the Baltic from 1982 to 2001. The model indicates that there have been large declines in cod and herring biomass over the past two decades and a strong increase in sprat biomass in the 1990s. Using the extended stock‐production model, the relative changes in stock biomass were similar to the changes derived using the age‐structured multispecies model, the multispecies virtual population analysis (MSVPA). However, the production model estimates of the average predation mortality of young cod and young sprat are much lower than those derived from MSVPA, although the estimates for young and adult herring and adult sprat are similar in both approaches. The estimates of food suitability show that the preferred food of adult cod is adult sprat and young herring, while the suitability of young sprat, young cod, and adult herring is much smaller. The simulations performed show that the multispecies production model, which is less data‐demanding than age‐structured MSVPA, can provide estimates of stock dynamics and species interactions that are largely consistent with those estimated by MSVPA. The quality of input data in terms of recruitment and fishing‐effort indices strongly impacts the reliability of the model's results.     

Impacts of an endoparasitic copepod, Ismaila belciki, on the reproduction,growth and survivorship of its nudibranch host, Janolus fuscus

Copepods from the genus Ismaila are large endoparasites that inhabit the main body cavity and/or cerata of opisthobranch molluscs. These parasites exhibit many life history characteristics typically found in parasitic castrators, yet the actual impact of infection on reproduction, growth or survivorship of the hosts are unknown. On the Oregon (USA) coast, Ismaila belciki can infect over 80% of their hermaphroditic hosts, Janolus fuscus. In laboratory mating experiments, we compared the reproductive output (egg mass weight, number of egg capsules, number of viable embryos) and the gonadal somatic index of infected versus uninfected J. fuscus. Infected J. fuscus could produce viable sperm and copulate. Mating with an infected individual did not limit a sea slug’s reproductive output. However, infected J. fuscus had significantly lower reproductive output (by 34–54%), producing smaller egg masses with fewer capsules and viable embryos. Infected hosts had significantly lower gonadal somatic index than their uninfected counterparts, although there was no significant difference in gonadal somatic index between hosts with single and double infections. By collecting the egg sacs produced by the copepod parasite during experiments, we estimated that 25–34% of the host’s reproductive output is usurped by the parasite and re-directed to the parasite’s own reproduction. In the laboratory, infection did not alter growth in J. fuscus. However, infection significantly decreased survivorship in mature (but not immature) nudibranch hosts. These results suggest that I. belciki is not a true castrator, but it does reduce the reproductive output of its host and may therefore limit the natural population size of J. fuscus.     

Susceptibility of juvenile Atlantic cod Gadus morhua to viral haemorrhagic septicaemia virus isolated from wild-caught Atlantic cod

A European strain of viral haemorrhagic septicaemia virus (VHSV) isolated from wild-caught cod Gadus morhua (H16/7/95) was shown to cause clinical disease and mortality in excess of 80% in juvenile Atlantic cod when administered by the intra-peritoneal (i.p.) route. No virus was recovered from cod cohabiting with experimentally infected fish at a ratio of 1:1, and no VHSV-associated mortality was demonstrated following immersion infection. External signs of disease in cod were the presence of exophthalmia and ascites. Virus was identified as VHSV by enzyme-linked immunosorbent assay (ELISA) and was recovered from both brain and organ pools (kidney, liver and spleen) of 100% of i.p. infected cod mortalities. Virus was also detected using an indirect immunofluorescence test on tissue imprints of kidney, liver, spleen and brain taken from moribund fish. The fact that cod were not susceptible to VHSV following waterborne exposure raises important questions surrounding the propagation, maintenance and impact of a naturally occurring reservoir of virus in the marine environment.     

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.     

Copepod ectoparasites of Merlangius merlangus and Platichthys flesus

Seasonal changes in the levels of copepod ectoparasitic infections from Merlangius merlangus and Platichthys flesus were examined and related to the annual migrations of young fish into an estuary. Lernaeocera branchialis (L.) was the only parasite common to both fish species; its life-cycle stages infected the branchial chambers of 96·7% flounders ( P. flesus ) and 40·4% whiting ( M. merlangus ). Infection in the two fish species exhibited similar seasonal fluctuations and a temporal relationship between the parasite's occurrence on its two hosts was apparent. Whiting were also parasitized by Clavella uncinata (Milller); 26·9 % fish were affected. The copepods' distribution was highly localized with the majority restricted to the long gill rakers of the first gill arch. Infection was related to size of whiting up to 12·5 cm; there was little increase beyond this length. In addition to L. branchialis , flounder was also host to Acanthochondria depressa (T. Scott) and Lepeophtheirus pectoralis (Müller). A. depressa showed a preference for the ocular side of the body with its developing stages attached mainly to the second gill arch and the adults located in the posterior pocket of the branchial chamber. L. pectoralis was associated with the paired fins. Factors which could result in such localized distributions are discussed.     

Cryptobia salmositica: susceptibility of infected rainbow trout, Salmo gairdneri, to environmental hypoxia

Using the sealed jar technique (also called residual oxygen bioassay), rainbow trout fry infected with Cryptobia salmositica were more susceptible than non-infected fish to environmental hypoxia. The Winkler technique (azide modification) was used to determine the residual dissolved oxygen in the water. Susceptibility of infected fish increased with 1) time after infection and was most evident in 3-7 wk infections, 2) the severity of anemia, and 3) increasing parasitemia. In prolonged infections, susceptibility was reduced when there were decreases in anemia and parasitemia; however, these infected fish were still more susceptible than non-infected fish. The increase in susceptibility of infected fish to hypoxia may be an important contributing factor to mortality of fish in hatcheries where there is inadequate water flow and overcrowding. The sealed jar technique is recommended in future studies on the pathogenesis of parasitic fish diseases, especially if the metabolic and/or respiratory systems are affected by the infection.     

Occurrence of the tuna nematode <Emphasis Type="Italic">Hysterothylacium cornutum</Emphasis> (Stossich, 1904) in farmed Atlantic cod <Emphasis Type="Italic">Gadus morhua</Emphasis> L. in North Norway

Adult and fourth-stage larval nematodes found in the stomachs of farmed cod in North Norway in October 2006 were identified as Hysterothylacium cornutum (Stossich, 1904), a nematode considered to be specific at the adult stage to tunas of the genus Thunnus. As far as we are aware, this is the first report of an adult form of this nematode from any host other than members of the genus Thunnus, and is also the first report from a polar region. The two infected cod, one with one large adult worm and another with six larvae, were in a sample of 17 that had been captured from the wild about 1 year before sampling and held in floating sea cages in Øksfjord, Finnmark County, North Norway, where the examinations took place. No further infections were found in any other samples of wild and farmed cod, totalling 261 fish, examined by us during the period 2006 and 2007 from five locations distributed along the coast of Norway from Øksfjord in the north to Ålesund in the south. Possible sources of this unusual infection are discussed, but no firm conclusion could be reached.     

Experimental evidence for parasite‐induced over‐winter mortality in juvenile Rhodeus amarus

In this study, the effects of the eye fluke Diplostomum pseudospathaceum (Trematoda) infection on over‐winter survival of young‐of‐the‐year (YOY) European bitterling Rhodeus amarus (Cyprinidae) were examined between September 2010 and April 2011. The fish were reared in semi‐natural conditions to ensure that results were not confounded by other parasite infections. The cumulative mortality of R. amarus from November until April was significantly higher in D. pseudospathaceum‐infected fish (57·3%) compared to controls (42·1%). Infection of the parental generation did not have any effect on the mortality of juveniles. The results indicate that D. pseudospathaceum infection increases over‐winter mortality of YOY R. amarus. The possible mechanisms causing mortality are discussed.     

Flow cytometry detection of infectious pancreatic necrosis virus (IPNV) within subpopulations of Atlantic salmon (Salmo salar L.) leucocytes after vaccination and during the time course of experimental infection

In the present study, intracellular infectious pancreatic necrosis virus (IPNV) in salmon leucocytes was detected by flow cytometry after experimental cohabitant challenge. IPNV vaccinated, non-vaccinated and intraperitoneally (i.p.) infected salmon (virus shedders) were analysed at different times throughout the period when mortality occurred. Fish that had survived 61 days post challenge (carriers) were also analysed. In particular, we analysed the presence of IPNV in B-cells (C7G7+cells) and in neutrophils (E3D9+ cells) in head kidney leucocytes (HKL) and in peripheral blood leucocytes (PBL).IPNV was present in HKL and PBL from all challenged fish groups at all samplings, including carriers. IPNV was also found intracellular in other leucocytes than B-cells and neutrophils. During the time course of infection there were changes in proportion of B-cells and neutrophils and in proportions of IPNV+ cells. In vaccinated fish, a delay in the changes observed in the proportion of IPNV+ cells and in the proportions of the two subpopulations was identified. The vaccinated fish were protected against disease as no fish died compared to 30.8% of non-vaccinated cohabitant fish. All i.p. infected fish, except one, survived the challenge. This is consistent with previous studies and confirmed that the routes of infection can influence mortality. The analyses in this study could not identify any factors enlightening this absence of mortality in i.p. infected fish, but both flow cytometry and qRT-PCR showed that i.p. infected fish were carriers of IPNV. The present study also found that IPNV was present in both B-cells and neutrophils as well as in other leucocytes in all carriers after cohabitant challenge. These fish had survived 9 weeks post challenge and 4 weeks after mortality has ceased. The fish harbouring virus within their leucocytes might become life long carriers and represent a risk for disease outbreaks, being virus shedders. Such fish are protected from later infections if the virus exposure has resulted in protective immunity. Flow cytometry was found to be very suitable for detection of intracellular virus after in vivo challenge and the sensitivity was demonstrated by the detection of virus in carriers.     

Head morphology and piscivory of European eels,Anguilla anguilla,predict their probability of infection by the invasive parasitic nematode Anguillicoloides crassus

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Francisella noatunensis subsp. noatunensis is the aetiological agent of visceral granulomatosis in wild Atlantic cod Gadus morhua

During the 1980s and 1990s wild-caught cod displaying visceral granulomatosis were sporadically identified from the southern North Sea. Presumptive diagnoses at the time included mycobacterial infection, although mycobacteria were never cultivated or observed histologically from these fish. Farmed cod in Norway displaying gross pathology similar to that identified previously in cod from the southern North Sea were recently discovered to be infected with the bacterium Francisella noatunensis subsp, noatunensis. Archived formalin-fixed paraffin-embedded tissues from the original North Sea cases were investigated for the presence of Mycobacterium spp. and Francisella spp. using real-time polymerase chain reaction, DNA sequencing and immunohistochemistry. Whilst no evidence of mycobacterial infection was found, F. noatunensis subsp. noatunensis was identified in association with pathological changes consistent with Francisella infections described from farmed cod in recent years. This study shows that francisellosis occurred in wild-caught cod in the southern North Sea in the 1980s and 1990s and demonstrates that this disease predates intensive aquaculture of cod.