Eel Swimbladder Research Articles

Infection with swim bladder nematode Anguillicola crassus in relation to European eel growth, age, and habitat along the German Baltic coast.

One possible reason for the European eel (Anguilla anguilla) population decline is the neozoan eel swim bladder nematode Anguillicola crassus. To investigate whether the prevalence of A. crassus and the associated swim bladder pathology is related to eel habitat, growth rate, and age, 728 yellow eels from 6 habitats differing in salinity and located along the German Baltic coast were examined between 2005 and 2009. The prevalence of A. crassus varied between habitats, ranging from 9 to 57%. Infection prevalence and the percentage of eels with a damaged swim bladder were significantly higher in inner coastal waters compared to more saline open coastal water. In infected eels, 1 to 32 adult and preadult individuals of A. crassus were observed. The mean infection intensity varied between habitats from 2 to 7 nematodes per eel but did not significantly differ between inner and open coastal waters. Infection prevalence and intensity decreased significantly with age when all open coastal waters and all habitats were combined. Both the lower prevalence of A. crassus and the swim bladder damage of older eels and of eels originating from open coastal water habitats suggest that these eels have a higher fitness for spawning migrations than eels from inner coastal waters. The present study underlines the importance of eel screening on a sufficiently small geographical scale for the accurate estimation of eel recruitment and the identification of priority areas that are likely to produce healthy silver eels.

PREVALENCE OF THE Anguillicola crassus PARASITE IN THE INTERNATIONAL MINHO RIVER

The European eel, Anguilla anguilla (Linnaeus, 1758), is vulnerable to infections by the parasitic nematode Anguillicola crassus Kuwahara, Niimi & Itagaki, 1974, mainly in freshwater ecosystems. The eel is a bioindicator species due to its benthic behaviour, predator, and life cycle. The parasite feeds on blood from the eel's swim bladder, causing damage to the walls and deterioration of this organ, reducing energy reserves, and affecting its migratory capacity for reproduction. Eels were captured at different sampling points divided into 4 areas of the international section of the Minho River in the following time periods: 1995-96, 2008-2011 and 2017-2021, through fyke nets and electric fishing sampling techniques. The objectives of this work were to analyze the dispersion and prevalence of A. crassus in the Minho River basin over time, infection rates and the eels condition. The prevalence levels found reach values ​​close to 75% in some sampled locations and 99% of eels shown pathological signs of swim bladder infection. The nematode dispersal area increased since the early 1990s when its presence in the Minho River was first recorded.

Aquaporin expression and cholesterol content in eel swimbladder tissue.

Leakiness of the swimbladder wall of teleost fishes must be prevented to avoid diffusional loss of gases out of the swimbladder. Guanine incrustation as well as high concentrations of cholesterol in swimbladder membranes in midwater and deep‐sea fish has been connected to a reduced gas permeability of the swimbladder wall. On the contrary, the swimbladder is filled by diffusion of gases, mainly oxygen and CO2, from the blood and the gas gland cells into the swimbladder lumen. In swimbladder tissue of the zebrafish and the Japanese eel, aquaporin mRNA has been detected, and the aquaporin protein has been considered important for the diffusion of water, which may accidentally be gulped by physostome fish when taking an air breath. In the present study, the expression of two aquaporin 1 genes (Aqp1aa and Aqp1ab) in the swimbladder tissue of the European eel, a functional physoclist fish, was assessed using immunohistochemistry, and the expression of both genes was detected in endothelial cells of swimbladder capillaries as well as in basolateral membranes of gas gland cells. In addition, Aqp1ab was present in apical membranes of swimbladder gas gland cells. The authors also found high concentrations of cholesterol in these membranes, which were several fold higher than in muscle tissue membranes. In yellow eels the cholesterol concentration exceeded the concentration detected in silver eel swimbladder membranes. The authors suggest that aquaporin 1 in swimbladder gas gland cells and endothelial cells facilitates CO2 diffusion into the blood, enhancing the switch‐on of the Root effect, which is essential for the secretion of oxygen into the swimbladder. It may also facilitate CO2 diffusion into the swimbladder lumen along the partial gradient established by CO2 production in gas gland cells. Cholesterol has been shown to reduce the gas permeability of membranes and thus could contribute to the gas tightness of swimbladder membranes, which is essential to avoid diffusional loss of gas out of the swimbladder.

The impact of Anguillicoloides crassus (Nematoda) on European eel swimbladder: histopathology and relationship between neuroendocrine and immune cells.

The swimbladder functions as a hydrostatic organ in most bony fishes, including the European eel, Anguilla anguilla. Infection by the nematode Anguillicoloides crassus impairs swimbladder function, significantly compromising the success of the eel spawning migration. Swimbladders from 32 yellow eels taken from Lake Trasimeno (Central Italy) were analysed by histopathology- and electron microscopy-based techniques. Sixteen eels (50%) harboured A. crassus in their swimbladders and intensity of infection ranged from 2 to 17 adult nematodes per organ (6.9 ± 1.6, mean ± s.e.). Gross observations of heavily infected swimbladders showed opacity and histological analysis found a papillose aspect to the mucosa and hyperplasia of the lamina propria, muscularis mucosae and submucosa. Inflammation, haemorrhages, dilation of blood vessels and epithelial erosion were common in infected swimbladders. In the epithelium of parasitized swimbladders, many empty spaces and lack of apical junctional complexes were frequent among the gas gland cells. In heavily infected swimbladders, we observed hyperplasia, cellular swelling and abundant vacuolization in the apical portion of the gas gland cells. Numerous mast cells and several macrophage aggregates were noticed in the mucosal layer of infected swimbladders. We found more nervous and endocrine elements immunoreactive to a panel of six rabbit polyclonal antibodies in infected swimbladders compared to uninfected.

Long-term ecological analysis of Anguillicola crassus occurrence and impact on the European eel population in a Mediterranean lagoon (North Italy)

Anguillicola crassus, a haematophagous nematode infecting the eel swim bladder, was introduced into Europe from Asia in the early 1980s with imported Anguilla japonica. It spread rapidly after establishment in the native European eel Anguilla anguilla. A long-term dataset shows the dynamics of A. crassus in eels of the Comacchio Lagoon from 1997 to 2019, and reveals the factors that influence its prevalence. A sample of 339 eels showed 19 parasitized by adult A. crassus, with one to five parasites per infected host and a mean abundance of 0.09 ± 0.45. Prevalence ranged from 2.14% (minimum value reached in 2005/06) to 11.9% (maximum reached in 1997). No significant temporal trend in the occurrence of A. crassus was detected over the period of the investigation, which was characterized by low levels of infection compared to that in eel populations from other coastal lagoons or estuaries. No influence of A. crassus on condition factor, hepatosomatic and gonadosomatic index and swim bladder integrity (evaluated through the Swim bladder Degenerative Index) was found, suggesting a minimal impact of the parasite on the eel population health. Anguillicola crassus, although established in Comacchio Lagoon, has not become invasive. The possible reasons for this, among which high salinity, will be discussed. Management of the lagoon for the past 30 years has also contributed to parasite containment through avoidance of restocking the eel population from external sources.

A mechanical approach to understanding the impact of the nematode Anguillicoloides crassus on the European eel swimbladder.

One of the most detrimental factors in the drastic decline of the critically endangered European eel (Anguilla anguilla) was the inadvertent introduction of the invasive nematode Anguillicoloides crassus Infection primarily affects the swimbladder, a gas-filled organ that enables the eel to control its depth in the water. A reduction in swimbladder function may be fatal for eel undergoing their spawning migration to the Sargasso Sea, a journey of over 5000 km. Although the physiological damage caused by this invasive parasite is well studied through the use of quantifiable gross pathological indices, providing a good measure of the swimbladder health status, they cannot separate the role of mechanical and morphological damage. Our study examined the appropriateness of three commonly used indices as a measure of mechanical damage by performing uniaxial tensile tests on swimbladder specimens obtained from an infected eel population. When the test results were compared with the gross pathological indices it was found that thickness correlated most strongly with mechanical damage, both confirming and, more importantly, explaining the counterintuitive findings of earlier work. In a damaged swimbladder, the immune response leads to a trade-off; increasing wall thickness raises the pressure required for organ rupture but decreases strength. The results indicate that for moderate infection the mechanical integrity of the swimbladder can be maintained. For severe infection, however, a reduction in mechanical integrity may reach a tipping point, thereby affecting the successful completion of their oceanic migration.

First evidence for a possible invasional meltdown among invasive fish parasites

Biological invasions are frequently studied topics in ecological research. Unfortunately, within invasion ecology parasite-associated aspects such as parasite impacts on new environments and on local host populations are less well-studied. Round gobies migrating from the Ponto-Caspian region into the Rhine River system are heavily infested with the Ponto-Caspian acanthocephalan parasite Pomphorhynchus laevis. As shown by experimental infestations the acanthocephalans occur as pre-adults in host-encapsulated cysts within the internal organs of the migrating gobies, but remain infective for their definitive host chub. Recently, we described the occurrence of larvae of another parasite, the invasive eel swim bladder nematode Anguillicola crassus, in these Pomphorhynchus cysts. In the present study, we could prove the infectivity of the nematode larvae for European eels for the first time. After experimental inoculation of Pomphorhynchus cysts occasionally infested with A. crassus larvae, the nematodes grow to maturity and reproduce whereas all P. laevis were unviable. We therefore postulate that the nematode larvae behave like immunological hitchhikers that follow a “Trojan horse strategy” in order to avoid the paratenic host’s immune response. Accordingly, the interaction between both invasive parasites gives first evidence that the invasional meltdown hypothesis may also apply to parasites.

Transcript levels of members of the SLC2 and SLC5 families of glucose transport proteins in eel swimbladder tissue: the influence of silvering and the influence of a nematode infection

The rate of glucose metabolism has been shown to be correlated to glucose uptake in swimbladder gas gland cells. Therefore, it is assumed that in the European eel silvering, i.e., the preparation of the eel for the spawning migration to the Sargasso Sea, coincides with an enhanced capacity for glucose uptake. To test this hypothesis expression of all known glucose transport proteins has been assessed at the transcript level in yellow and in silver eels, and we also included Anguillicola crassus infected swimbladders. Glucose uptake by rete mirabile endothelial cells could be crucial for the countercurrent exchange capacity of the rete. Therefore, this tissue was also included in our analysis. The results revealed expression of ten different members of the slc2 family of glucose transporters, of four slc5 family members, and of kiaa1919 in gas gland tissue. Glucose transporters of the slc2 family were expressed at very high level, and slc2a1b made up about 80% of all slc2 family members, irrespective of the developmental state or the infection status of the eel. Overall, the slc5 family contributed to only about 8% of all detected glucose transport transcripts in gas gland tissue, and the slc2 family to more than 85%. In rete capillaries, the contribution of sodium-dependent glucose transporters was significantly higher, leaving only 66% for the slc2 family of glucose transporters. Neither silvering nor the infection status had a significant effect on the expression of glucose transporters in swimbladder gas gland tissue, suggesting that glucose metabolism of eel gas gland cells may not be related to transcriptional changes of glucose transport proteins.

Anguillicola crassus infection affects mRNA expression levels in gas gland tissue of European yellow and silver eel.

Using Illumina sequencing, we investigated transcriptional changes caused by the nematode Anguillicola crassus within yellow and silver eels by comparing swimbladder samples of uninfected yellow with infected yellow eels, and uninfected silver with infected silver eels, respectively. In yellow eel gas gland, the infection caused a modification of steady state mRNA levels of 1675 genes, most of them being upregulated. Functional annotation analysis based on GO terms was used to categorize identified genes with regard to swimbladder metabolism or response to the infection. In yellow eels, the most prominent category was ‘immune response’, including various inflammatory components, complement proteins, and immunoglobulins. The elevated expression of several glucose and monocarboxylate transporters indicated an attempt to maintain the level of glucose metabolism, even in due to the infection thickened swimbladder tissue. In silver eel swimbladder tissue, on the contrary, the mRNA levels of only 291 genes were affected. Genes in the categories ‘glucose metabolism’ and ‘ROS metabolism’ barely responded to the infection and even the reaction of the immune system was much less pronounced compared to infected yellow eels. However, in the category ‘extracellular matrix’, the mRNA levels of several mucin genes were strongly elevated, suggesting increased mucus production as a defense reaction against the parasite. The present study revealed a strong reaction to an Anguillicola crassus infection on mRNA expression levels in swimbladder tissue of yellow eels, whereas in silver eels the changes ware almost negligible. A possible explanation for this difference is that the silvering process requires so much energy that there is not much scope to cope with the additional challenge of a nematode infection. Another possible explanation could be that gas-secreting activity of the silver eel swimbladder was largely reduced, which could coincide with a reduced responsiveness to other challenges, like a nematode infection.

Development ofAnguillicoloides crassusin a Cyclopoid Copepod from theAcanthocyclops robustus–americanus–vernalisComplex in South Carolina, U.S.A.

ABSTRACT: The invasive nematode Anguillicoloides crassus parasitizes the swim bladder of eels, including that of the American eel, Anguilla rostrata. Despite its potential devastating effects on eel populations, however, its intermediate host(s) is/are unknown in North America. The goal of this study was to determine whether An. crassus could infect copepods collected in the wild from the Goose Creek Reservoir in South Carolina, U.S.A., where An. crassus is known to occur. Cyclopoid copepods, identified morphologically as belonging to the Acanthocyclops robustus–americanus–vernalis species complex, were successfully experimentally infected by second-stage larvae (L2s) of An. crassus from eels captured in South Carolina, U.S.A. One infected copepod was identified as Ac. americanus via sequencing of a 251-base pair (bp) portion of mitochondrial cytochrome oxidase I DNA. For each infection experiment, 30 to 60 copepods were exposed for 24 hr to L2s at either 21°C or 26°C and maintained at their respective e...

Anguillicola crassus Infection Significantly Affects the Silvering Related Modifications in Steady State mRNA Levels in Gas Gland Tissue of the European Eel.

Using Illumina sequencing, transcriptional changes occurring during silvering in swimbladder tissue of the European eel have been analyzed by comparison of yellow and silver eel tissue samples. Functional annotation analysis based on GO terms revealed significant expression changes in a number of genes related to the extracellular matrix, important for the control of gas permeability of the swimbladder, and to reactive oxygen species (ROS) defense, important to cope with ROS generated under hyperbaric oxygen partial pressures. Focusing on swimbladder tissue metabolism, levels of several mRNA species encoding glucose transport proteins were several-fold higher in silver eels, while enzymes of the glycolytic pathway were not affected. The significantly higher steady state level of a transcript encoding for membrane bound carbonic anhydrase, however, suggested that CO2 production in the pentose phosphate shunt and diffusion of CO2 was of particular importance in silver eel swimbladder. In addition, the mRNA level of a large number of genes related to immune response and to sexual maturation was significantly modified in the silver eel swimbladder. The modification of several processes related to protein metabolism and transport, cell cycle, and apoptosis suggested that these changes in swimbladder metabolism and permeability were achieved by increasing cell turn-over. The impact of an infection of the swimbladder with the nematode Anguillicola crassus has been assessed by comparing these expression changes with expression changes observed between uninfected yellow eel swimbladder tissue and infected silver eel swimbladder tissue. In contrast to uninfected silver eel swimbladder tissue, in infected tissue the mRNA level of several glycolytic enzymes was significantly elevated, and with respect to extracellular matrix, several mucin genes were many-fold higher in their mRNA level. Modification of many immune related genes and of the functional categories “response to DNA damage stimulus” and “cellular response to stress” illustrated the damaging effect of the nematode infection. This study has identified a range of cellular processes in the swimbladder of silver eels that appear to be altered by nematode infection. These altered cellular processes could contribute to detrimental changes in swimbladder function that, in turn, may lead to impairment of spawning migration.

Influence of adult Anguillicoloides crassus load in European eels swimbladder on macrophage response

Anguillicoloides crassus has become one of the most important threats to the European eel (Anguilla anguilla). Adult parasites colonize the swimbladder leading to an impaired functioning of this organ. The infection is also responsible for an increased in the stress level of infected eels, that could produce an altered immune response as well. Differences in parasite loads and effects in the European and Japanese eel (Anguilla japonica) have been described. We have studied the influence of the number of adult parasites present in the swimbladder of wild eels on the macrophage response (phagocytosis and respiratory burst) as part of the first immune response to pathogens. Our results show an increased phagocytozed bacterial survival 24 h post-infection in macrophages of eels infected with more than ten adult parasites compared to macrophages from eels infected with less than those ten adult parasites. Respiratory burst results also showed a less efficient response in macrophages from eels infected with more than ten adult parasites, although in this case results were not found to be significant.

An evaluation of indices of gross pathology associated with the nematode Anguillicoloides crassus in eels

This study compares two alternative indices for quantifying the gross pathology of the swimbladder of eels, Anguilla anguilla (L.), infected with the nematode Anguillicoloides crassus. Two observers recorded twice the scores obtained by the two indices on the same set of 71 wild caught eels (from elver to silver eels, French Mediterranean lagoons). The Length Ratio Index (LRI), performed better than the Swimbladder Degenerative Index (SDI), in three of four predefined criteria of decision. First, the LRI better correlated with an estimate of the swimbladder volume reduction, a functional consequence of the infection (representativeness). Also, the LRI was less prone to subjectivity (inter-observer variability) and more precise (intra-observer variability), although less easy to generate (time needed for measurement/assessment). Using a sub-sample of 32 unaffected eels (showing minor if any swimbladder damage and no living worms at autopsy), we ascertained a linear relationship between the swimbladder length and the total body length, a prerequisite of isometric growth, to definitively accept the new ratio index as a valid alternative to the SDI. Also, because the LRI can be recorded on live specimens with radio-imagery (non-invasive method), we recommend its use, and provide a graph of correspondence between the SDI scores, the LRI scores and the estimated proportion of gas loss in the swimbladder.

New data on the biology of the introduced exotic nematode Anguillicola crassus Kuwahara, Niimi et Itagaki, 1974 in the eel Anguilla anguilla in Lake Wdzydze (Polish waters)

Abstract Anguillicola crassus Kuwahara, Niimi et Itagaki, 1974 is an Asian parasitic nematode that was introduced to Europe and inhabits the swim bladder of eels. In the 2002-2005 period, 237 eels, Anguilla anguilla (Linnaeus, 1758), from Lake Wdzydze were examined for the occurrence of the nematode. 79.3% of the fish were infected, at a mean intensity of 7.2 nematodes per fish. Morphological measurements of the observed A. crassus are presented. This is the first published report of A. crassus in eels from Lake Wdzydze.

Biased Sex Ratio in the European Eel (Anguilla anguilla) Swim-Bladder Parasite Anguillicola crassus, Experimentally Induced by 11-Ketotestosterone

Parasites are intimately connected to the host in which they live, and some may be affected by the polluted environment of their host. The present study describes the effect of a steroid hormone (11-ketotestosterone) on the sex ratio of the invasive hematophagous nematode Anguillicola crassus Kuwahara, Niimi & Itagaki, 1974, when experimentally injected to European eels, Anguilla anguilla. Our results showed that this steroid induced a significant male-biased ratio in the nematode A. crassus infrapopulations, suggesting that the presence of endocrine disruptors in the environment may lead to skewed sex ratios among parasites.

Element concentrations in the swimbladder parasite Anguillicola crassus (nematoda) and its host the European eel, Anguilla anguilla from Asi River (Hatay-Turkey)

The European eel's swimbladder nematode, Anguillicola crassus, sampled from the Asi River (Orontes River) in Antakya (Hatay, Turkey) in May 2006 were analysed by Inductively Coupled Plasma-Atomic Emission Spectrometry (ICP-AES) for their some heavy metal (Cd, Cr, Cu, Fe, Hg, Mn, Pb and Zn) levels. The metal concentrations of the parasites were compared to different organs (swimbladder, liver, muscle and skin) of the fish hosts. The parasite contained statistically highly significantly amounts of Fe (P < 0.05). The iron level of nematode was up to 25.52 times than the muscle of its host, Anguilla anguilla. However, bioconcentration of Cd, Cr, Cu, Hg, Mn, Pb, Zn were detected in the A. crassus and it contained no statistically differences with the other tissues of its host, the eel (P > 0.05). Furthermore, no significant differences were detected in the heavy metal accumulations between the parasitized and un-parasitized fish tissues. The analysed metals (Cd, Cr, Cu, Fe, Mn, Pb and Zn) were found in fish muscle at mean concentrations under the permissible limits proposed by FAO.

Pathological studies on the swimbladder of egyptian eels (Anguilla anguilla) infected with anguillicola crassus

Pathological studies on the swimbladder of egyptian eels (Anguilla anguilla) infected with anguillicola crassus

Sequential morphological and permeability changes in the rete capillaries during hyperglycaemia.

With the rete model of the eel swimbladder, we have studied the appearance and development of a microangiopathy during a 2-year period of hyperglycaemia. Hyperglycaemia was induced in the eel by chronic exposure to cold water. At 3-5 months, basement membrane thickness was twice the normal value and increased only slightly thereafter. Diffusion coefficients of permeability were measured in counter-current perfusion experiments for a variety of tracers that are believed to use different pathways of transcapillary transport. The permeability to sucrose was the first to significantly increase, at 6-8 months, followed by that of albumin, insulin, and inulin, at 9-11 months and that of sodium, at 18-24 months. The permeability to water and antipyrine remained stable throughout the study. The results indicate that in the rete model, chronic hyperglycaemia induces a rapid thickening of the capillary basement membrane and selective permeability increments in the various paths of transcapillary transport.

The health state of the eel swimbladder as a measure of parasite pressure by Anguillicola crassus.

We have developed an index based on macroscopic criteria to easily assess the health state of the eel swimbladder as a result of infection by the nematode Anguillicola crassus. In the sampling area (brackish lagoons of the French Mediterranean coast), 92% of the host sample (1,251 eels covering all size classes) showed pathological signs of infection. The general trend was for increasing damage as eel size increased, thus suggesting accumulation of pathological effects. We also revealed a non-linear relationship between the swimbladder index and the abundance of living worms. In particular, we showed that severely damaged swimbladders harboured very few living nematodes. We argue that the swimbladder degenerative index more closely reflects the parasite pressure than does classic parasite count. We found seasonal variation in the swimbladder index, with maximum damage occurring in July and thereafter a trend for healthy individuals. We discuss the possibility that the seasonal decrease in the swimbladder index could reflect the death of the more severely affected individuals during the warmest months.

The spread of the eel swimbladder nematode Anguillicola crassus through the Erne system, Ireland

The spread of the eel swimbladder nematode Anguillicola crassus through the Erne system, Ireland