The effect of foraging and ontogeny on the prevalence and intensity of the invasive parasite Anguillicola crassus in the European eel Anguilla anguilla

Infection patterns of the invasive Anguillicola crassus nematode were investigated in a population of the European eel Anguilla anguilla where parasite invasion is very recent, Loch Lomond, Scotland. Intensity levels of the parasite were associated with differences in fish ontogeny and trophic ecology. Although eels foraged on both fish and invertebrates, individuals which were smaller and fed on invertebrates (>70% contribution to diet) were found to contain a greater number of swim bladder parasites compared to larger eel with a predominance of fish (>60% contribution) in their diet. Within affected fish, a significant negative relationship was found between fish length and parasite intensity, with smaller individuals having higher parasite intensity than larger individuals. This study indicates that food intake and infection risk are linked in this recently infected host–parasite system. From a management perspective increasing our understanding of how infection intensity and repeated exposure is linked to resource use in an ecosystem is important for the future management of this endangered species in Europe.     

Freshwater eels: A symbol of the effects of global change

Temperate eels Anguilla anguilla (European eel), A. rostrata (American eel) and A. japonica (Japanese eel) are three catadromous species which have been declining since the 1970s/1980s despite their remarkable adaptive capacity. Because of their specific life cycles, which share distant oceanic spawning grounds and continental growth stage, eels are affected by five components of the global change: (a) climate change affecting larval survival and drift, (b) an increase in pollution leading to high levels of contamination exacerbated by their high lipid levels, (c) increasing fragmentation and habitat loss that reduce dramatically the amount of available habitats and induce increased spawner mortality, (d) the appearance of Anguillicola crassus a parasitic alien nematode that impairs spawning success, and (e) the impact of commercial and recreational fisheries for all life stages of eel. In this context, the rapid increases of pressures during the “Great Acceleration” have surpassed the adaptive capacity of eels. This illustrates that cumulative effects of global change can lead to the collapse of species, even in species that have amazingly high adaptive capacities.     

The pathogenic helminth parasites of eels

Although 63 and 55 species of helminths have been reported from each species of Atlantic eel and from 29 to 19 for each species of Pacific eel only the monogeneans Pseudodactylogyrus bini and P. anguillae and the nematode Anguillicola crassus, originally specific to species of Pacific eels, can be considered serious pathogens. None of the three are normally pathogenic to their preferred natural eel host species in the wild. Pseudodactylogyrus spp. only cause serious local gill damage when present on a host in large numbers under optimal conditions that facilitate transmission. This is the case in eel aquaculture, where infections can be controlled by drugs. Anguillicola crassus is only pathogenic to Anguilla anguilla and A. rostrata when Atlantic eels are introduced to the far east or when the parasites have been introduced to Europe. Here the parasite life cycle differs in that A. crassus can infect a wide range of intermediate hosts, employ paratenic hosts and survive as larvae for months in the swimbladder wall. This makes it an excellent colonizer. Its major pathogenic effects on eels result from haemorrhaging in, and thickening of, the swimbladder wall. It reduces the oxygen concentration in the swimbladder, reducing its ability to function as a hydrostatic organ, and increases the stress response of eels. In shallow lakes at warm temperatures this can result in mass mortalities. It is also feared that the parasite affects the ability of eels to migrate to the Sargasso Sea and so contributes to the decline in eel populations. Control by drug treatment is possible in culture, but not in the wild.     

Infection by Anguillicoloides crassus in a riverine stock of European eel,Anguilla anguilla

Abstract Infection by the parasitic nematode Anguillicoloides crassus Kuwahara, Niimi & Itagaki, in a wild riverine stock of European eel, Anguilla anguilla (L.), in a near pristine river was investigated. Samples were collected on a seasonal basis in distinct habitats along the river gradient. This study highlighted the presence of the parasite and completion of the whole life cycle in eels from the Río Esva. Infection levels by A. crassus were high at three sites between the mid river to the estuary and also varied among seasons. Condition of eels was lower at upstream sites compared with downstream locations. Although high‐quality, environmental conditions in the Río Esva may buffer the effects of A. crassus on eels, potential impacts and limiting factors for the parasite are discussed.     

Long‐term records (1781–2013) of European eel (Anguilla anguilla L.) production in the Comacchio Lagoon (Italy): evaluation of local and global factors as causes of the population collapse

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Effects of vasoactive intestinal polypeptide,substance P, 5-hydroxytryptamine,met-enkephalin and neurotensin on the swimbladder smooth muscle of two teleost species,Gadus morhua andAnguilla anguilla

The effects of vasoactive intestinal polypeptide (VIP), substance P (SP), 5-hydroxytryptamine (5-HT), neurotensin (NT) and met-enkephalin (mEnk) on the smooth muscles of the teleost swimbladder were studied in two teleost species, the Atlantic cod (Gadus morhua) and the eel (Anguilla anguilla). The study was made on isolated strip preparations of the muscularis mucosae, using putative transmitters corresponding to the immunoreactive materials that have previously been localized by immunohistochemical methods in nerves or endocrine/paracrine cells of the teleost swimbladder and/or the gastrointestinal canal. VIP was relaxatory on both cod and eel swimbladder smooth muscle, SP and 5-HT were constrictory in both species, and mEnk was excitatory on the eel swimbladder smooth muscle. Clear effects of these agents were usually seen at a concentration ofca. 10 nM in cumulative concentration/effect experiments. NT had no effect in either species. In the eel, the effects on the pneumatic duct were generally greater than on the swimbladder proper. The study indicates that the 5-HT and peptides previously observed by immunohistochemistry have physiological functions in the swimbladder.     

The phylogeny of Anguillicola crassus and A. globiceps based on partial 18S ribosomal RNA sequences

The parasitic nematodes Anguillicola crassus and A. globiceps infect the swimbladder of eels. To investigate the relationship of these species at the molecular level, the small subunit ribosomal RNA (18S rRNA) genes of A. crassus and A. globiceps were cloned and their nucleotide sequences determined. The 18S rRNA gene of A. crassus and A. globiceps were found to have similar lengths (886 and 888 base pairs, respectively) and demonstrated extensive similarity in their nucleotide sequences, showing 98.8% homology. However, the sequence homology of the 18S rRNA gene of A. crassus with that of other nematodes was found to be in the range of 72.7–89.0% homology, whilst that of A. globiceps was in the range of 73.1–89.4% homology. A phylogenetic reconstruction showed A. crassus to be closely related to A. globiceps. The analysis of nucleotide sequences of the 18S rRNA gene of fish parasites has proven useful in supporting species status and phylogenetic relationships.     

Comparative imaging of European eels (Anguilla anguilla) for the evaluation of swimbladder nematode (Anguillicoloides crassus) infestation

This study compares diagnostic imaging tools in detecting the parasitic swimbladder nematode Anguillicoloides crassus in Anguilla anguilla (L.) and focuses on ultrasound in an attempt to develop a non‐destructive, field diagnostic test. Ultrasound use could allow the parasite to be diagnosed without decreasing the number of critically endangered European eels through post‐mortem. In the preliminary study, eels were examined with computed radiography, computed tomography, magnetic resonance imaging, 14 MHz high‐end ultrasound and 5 MHz low‐end portable ultrasound, and the results were compared with post‐mortem findings. This ultrasound scanning technique did not produce any promising results. A second batch of eels was examined using the same high‐end and low‐end ultrasounds, but employing a different scanning technique and comparing the results with post‐mortem. This second study, scanning along the midline from below, allowed for the detection of anomalies associated with moderately infected animals. None of the eels used in this study were severely infected; thus, no conclusions can be made regarding the use of ultrasound in those animals. Overall, it was found that none of the techniques were useful in diagnosing mildly infected individuals; therefore, no single diagnostic imaging tool is sensitive enough to replace post‐mortem for definite diagnosis.     

Ecology and conservation of the American eel in the Caribbean region

The majority of American eel, Anguilla rostrata LeSueur, knowledge is derived from temperate regions in the United States and Canada, with little known from its tropical Caribbean distribution. Findings of original research on American eel distribution, abundance, population biology, habitat ecology and threats from the Caribbean island of Puerto Rico were synthesised. American eel were captured from 48 of 116 sites (41.4%) in 26 of 49 river basins (53.1%) during 2005–2016, and it was extirpated upstream of dams and migration barriers >3.0 m high (38.9% of habitat). Mean density and biomass were 438.9 fish/ha and 23.44 kg/ha, respectively. Upstream habitats favoured larger individuals, and females were larger than males. The swim‐bladder parasite Anguillicoloides crassus Kuwahara, Niimi & Hagaki was not found in 120 eels examined. Realised threats include dams and other migratory barriers, habitat loss and alteration and pollution; exotic species and commercial fishing are impending threats; and the least understood is climate change.     

Is European catfish a threat to eels in southern France?

• 1. European eel (Anguilla anguilla) is recognized as a critically endangered species in the northern hemisphere. Threats such as overfishing or pollution are well known as risks for eel populations. However, much less is known about the impact of introduced fish on European eels. In particular, introduced large‐bodied predators could become new predators to eels.
• 2. The potential impact of European catfish (Silurus glanis L) on an eel population in the Camargue, southern France was studied using a combination of stable isotope and gut content analyses.
• 3. Only large‐bodied catfish (>500 mm) can consume numerous fish prey. However, catfish mostly consumed crayfish (Procambarus clarkii), these prey items being found in 79% of the guts of the largest individuals. Eel was absent from the dissected catfish guts. A mixing model based on Bayesian inference revealed that catfish diet included only 5% (0–8.5%) of marine sources (both eel and mullet).
• 4. While local economic interests prompted ecological studies to assess whether catfish exerted a new and strong predatory pressure on eel, this study found that European catfish behaved as an opportunistic omnivore, and as such was not a direct threat as a predator on eel populations in the Camargue. Copyright © 2011 John Wiley & Sons, Ltd.

     

Is there a role of ocean environment in American and European eel decline?

American eel (Anguilla rostrata) recruitment has declined dramatically, in parallel with that of European eel (Anguilla anguilla). Since both species spawn in the Sargasso Sea and migrate as larvae to continental waters, the coincidence in recruitment failure implies an Atlantic-wide cause, due perhaps to ocean climate. There is indirect evidence that the Gulf Stream has weakened in the 1980s. A slower Gulf Stream could interfere with larval transport and generate observed patterns of declining abundance of American eel only in northern North America and relatively uniform declines of European eel throughout Europe. While specific causes are still unclear, these data indicate a threat to both species and to their commercial fisheries.     

Anthropogenic spreading of anguillid herpesvirus 1 by stocking of infected farmed European eels,Anguilla anguilla (L.), in the Schlei fjord in northern Germany

The Schlei fjord in northern Germany is the recipient water of a comprehensive eel, Anguilla anguilla (L.), stocking programme. Since 2015, stocked eels become alizarin red S marked, but to date no control mechanism is implemented in this stock enhancement measure to prevent anthropogenic spreading of diseases. Consequentially, it was possible that farmed stocking cohorts of 2015 and 2016 (in total ca. 1040 kg) were subsequently tested positive for anguillid herpesvirus 1 (AngHV 1). For this study, 100 eels [total length (TL) 24.3–72.9 cm, age ca. 1–6 years] were caught in 2016 and investigated with regard to AngHV 1 infection, parasite load (Anguillicoloides crassus) and body conditions. 68% of the eels were found to be virus positive while larger specimens were more often infected. In addition, a fitted generalized linear model (area under the curve = 0.741) demonstrated that an increase in individual TL is accompanied with an increased risk of clinically relevant virus loads. Anguillicoloides crassus turned out to be an important stressor for eels, because parasite and virus load revealed a significant positive correlation. The results of this study evidently show the urgent need of a disease containment strategy for eel stocking programmes.     

Increased abundance of European eel (Anguilla anguilla) in acidified Norwegian rivers after liming

The prevalence and abundance (density 100 m^?2) of European eel (Anguilla anguilla) were studied by means of electrofishing in 13 acidified rivers in Norway that had been limed to restore acceptable water quality for Atlantic salmon (Salmo salar). Status of Atlantic salmon in these rivers varied prior to liming, from being entirely lost in six highly acidified rivers and in different stages of decline in seven less acidified rivers. Four of the rivers are heavily affected by hydropower development. The abundance and prevalence of European eel increased significantly during the study period. The best model for predicting eel abundance was that with four explanatory variables: time after liming, time after liming squared, status of salmon stocks and hydropower regulation. The eel density was expected to increase by a factor of almost 5 after 10 years of liming. The model also predicts that a river with a formerly reduced Atlantic salmon stock has a 2.8 times higher density of eel than rivers with formerly lost salmon stocks. Before liming, European eel were on average recorded at 15 and 41% of the sampling stations in rivers with formerly lost and reduced Atlantic salmon populations, respectively, increasing to 49 and 68% in individual rivers, respectively, after 10 years of liming. The recovery of European eel in these formerly acidified rivers by means of liming took place during the same period as their abundance declined in other parts of their distribution area in Norway and elsewhere in Europe.     

Virus infections of the European Eel in North Rhine Westphalian rivers

Viral infections have been suggested to play a role in the decline of the panmictic population of the European eel (Anguilla anguilla). However, despite the importance of knowledge about pathogenic eel viruses, little is known about their spread in the wild European eel population and only a few eel pathogenic viruses have been described so far. In this study, we aimed to investigate the health status of the A. anguilla stock in North Rhine Westphalia (NRW) State of Germany. For this purpose, we examined tissue samples of 16 elvers, 100 yellow eels and 6 silver eels, sampled from the rivers Rhine, Lippe and Ems. Virus detection was performed via a combination of cell culture and PCR. Next to the detection of frequently encountered pathogenic eel viruses (anguillid herpesvirus 1 and eel virus European X (EVEX)), we isolated the eel picornavirus 1 (EPV-1) from tissue of yellow eels and elvers and demonstrate the distribution of EPV-1 in wild eel population in NRW.     

Mortality of European eel after downstream migration through two types of pumping stations

Although numerous pumping stations (PS) have been used by water managers for numerous applications on rivers, canals and other water bodies, their impact on fish populations is poorly understood. This study investigates European eel, Anguilla anguilla (L.), mortality after natural downstream passage through a propeller pump and two Archimedes screw pumps at two PSs on two lowland canals in Belgium. Fyke nets were mounted permanently on the outflow of the pumps during the silver eel migration periods. Based on the condition and injuries, maximum eel mortality rates were assessed. Mortality rates ranged from 97 ± 5% for the propeller pump to 17 ± 7% for the large Archimedes screw pump and 19 ± 11% for the small Archimedes screw pump. Most injuries were caused by striking or grinding. The results demonstrate that PSs may significantly threaten escapement targets set in eel management plans.     

PARASITES AND PARASITOSIS IN FISH CULTURE IN PORTUGAL

This paper deals with research work covering the period from May 1979 up to May 1981 and presents results of parasites and parasitosis diagnosed in a total of 195 complete dissections of six fish species from cultured and feral populations in Portugal: European eel (Anguilla anguilla) (49); mirror carp (Cyprinus carpio specularis) (29); common grey mullet (Mugil cephalus) (18); European plaice (Pleuronectes platessa) (11); rainbow trout (Salmo gairdneri) (42); common sole (Solea solea) (46). A list of protozoans and helminths identified with respective incidence is given: A) Feral fish: 1) European eel (17)—Echinorhynchus clavula 11.8% and Rhabdochona anguilla 5.9%; 2) common grey mullet (18)—Haploporus benedenii 16.7%, Neoechinorhynchus sp. 5.6%, and Raphidascaris sp. 5.6%; 3) European plaice (11)—Bothriocephalus sp. larvae 9.1%, Contracaecum aduncum 9.1%, and Cryptocotyle lingua 9.1%; 4) common sole (46)—Cucullanellus minutus 8.7%, Gyrodactylus elegans 4.3%, and Cestodes larvae 2.2%. B) Cultured fish: 1) European eel (32)—Trichodina anguillae 3.1% and Ichthyophthirius multifiliis 18.8%; 2) rainbow trout (42)—Eimeria truttae 2.4%, Hexamita intestinalis 4.8%, Holophrya simplex 2.4%, and Trichodina truttae 4.8%. The results show that feral fish harbor predominantly indirect life cycle helminths, in contrast with cultured fish only affected with protozoans, due mainly to overcrowding and deficient management, which propitiate a significant background infection. It was in these specimens that some lesions characteristic of protozoosis were found.     

Development and validation of a real‐time PCR assay for the detection of anguillid herpesvirus 1

Anguillid herpesvirus 1 (AngHV1) causes a haemorrhagic disease with increased mortality in wild and farmed European eel, Anguilla anguilla (L.) and Japanese eel Anguilla japonica, Temminck & Schlegel). Detection of AngHV1 is currently based on virus isolation in cell culture, antibody‐based typing assays or conventional PCR. We developed, optimized and concisely validated a diagnostic TaqMan probe based real‐time PCR assay for the detection of AngHV1. The primers and probe target AngHV1 open reading frame 57, encoding the capsid protease and scaffold protein. Compared to conventional PCR, the developed real‐time PCR is faster, less labour‐intensive and has a reduced risk of cross‐contamination. The real‐time PCR assay was shown to be analytically sensitive and specific and has a high repeatability, efficiency and r²‐value. The diagnostic performance of the assay was determined by testing 10% w/v organ suspensions and virus cultures from wild and farmed European eels from the Netherlands by conventional and real‐time PCR. The developed real‐time PCR assay is a useful tool for the rapid and sensitive detection of AngHV1 in 10% w/v organ suspensions from wild and farmed European eels.     

Movements of the European eel (Anguilla anguilla) in a chalk stream

Abstract – The movements of wild European eels (Anguilla anguilla L.) were monitored continuously over a 2‐year period in a tributary of the River Itchen, Hampshire, UK, using a passive integrated transponder (PIT) antenna system. The time of these movements was then related to a number of monitored and calculated environmental parameters. No eel movements were recorded in the winter months when mean stream temperature was below 10 °C. The numbers of movements peaked in May, when mean water temperatures and day length were increasing. The movement of eels was significantly (P < 0.001, R² = 0.45, N = 72) correlated with the time of sunset, with the majority (72%) recorded during the hours of darkness. The results of this investigation have implications for the design/timing of surveys of yellow eel populations and their habitat associations and suggest that successfully determining the microhabitat preferences of active resident eels will require remote monitoring throughout the 24‐h period.     

Management issues relating to the European eel, Anguilla anguilla

In many European countries there is growing concern over reduced recruitment and catches of the European eel, Anguilla anguilla (L.). Evidence of the decline, together with possible reasons for the changes as detailed by various authors, are reviewed. It is suggested that the problems need to be addressed now and on various levels. Proposals for management actions, as outlined by the Environment Agency for England and Wales, are summarized by way of example.