Parasites of flounder (Platichthys flesus L.) from the German Bight, North Sea, and their potential use in biological effects monitoring

In the frame of an integrated biological effect monitoring programme, the parasite community of flounder (Platichthys flesus) was investigated at different locations in the German Bight from 1995 to 2000. In order to assess the impact of environmental contamination caused by anthropogenic activities on the parasite community, selected parasitological parameters that displayed significant differences between the sampling sites were subjected to correlation analyses with site-specific contamination and individual pollution loads of their fish hosts. In addition, correlation analyses were conducted with the responses of selected genetic, biochemical, histopathological, physiological and immunological parameters of fish, used as potential biomarkers. In total, 802 flounder were analysed for these parameters. Information on the chemical background at the sampling sites was derived from sediment samples and from 120 samples of blue mussel (Mytilus edulis) tissue, collected at each of the sampling sites. Based on chemical data available from the sediment and blue mussel samples, a pollution gradient could be established between the sampling sites for individual contaminants. The relative abundance of Acanthochondria cornuta, Cucullanus heterochrous and Zoogonoides viviparus, and the community measures species richness and number of heteroxenous species decreased with increasing concentrations of individual heavy metals or hydrocarbons in sediment and blue mussel samples. Most of the parasitological parameters significantly reflected the established site-specific contamination gradient, when data were pooled over all sampling campaigns. Significant correlations were also found with the contamination level of individual flounder. The parasitological parameters included the parasite species Lepeophtheirus pectoralis and Lernaeocera branchialis, which were not correlated to site-specific contamination. Several biomarkers were significantly correlated to the abundance of parasitic copepods A. cornuta, Lernaeocera branchialis and Lepeophtheirus pectoralis and to parasite community parameters. The results showed that the abundance of several metazoan parasite species, species richness and parasite diversity were reduced in contaminated habitats, and that differences between sites were not only related to natural factors, such as salinity, but also to pollution-induced stress. Thus, it can be concluded that the parasite community of fish responds to the level of pollution at a specific site as well as to residues of xenobiotics in individual fish. These findings give indications that the parasite community of fish is a valuable parameter for the assessment of ecological consequences of chemical contamination in aquatic habitats.     

Parasites of flounder Platichthys flesus (L.) from the German Bight, North Sea, and their potential use in ecosystem monitoring

The analysis of fish-parasite community structure and the use of ecological richness and diversity measurements are commonly used for the evaluation of environmental stress in aquatic ecosystems. As part of an integrated biological-effect monitoring, the parasite community of flounder Platichthys flesus (L.) was investigated for various locations in the German Bight during spring and autumn of 1995–2000, using established ecological methods. Although the parasite-community composition was very similar at the component-community level, the number of component species as well as the species accumulation curves showed clear differences among the sites. On the infra-community level, all of the ecological measurements showed significantly lower values in flounder from the Elbe estuary, the most polluted site, than in flounder from Helgoland. This was seen during a single season or during both seasons. When the data were pooled over the years, gradual differences between the sites, which were seldom detected at individual sampling periods, became evident for different measurements of species richness and species diversity and corresponded to a contamination gradient established between Elbe > Inner Eider, Outer Eider > Helgoland. Despite seasonal variations, which were observed in almost all measurements, these gradual differences were found in both seasons.     

The population dynamics ofLernaeocera lusci andL. branchialis on intermediate hosts

The metapopulation dynamics ofLernaeocera lusci andL. branchialis on soleSolea solea and flounderPleuronects flesus were studied in the Dutch coastal area. Both fish species harboured large numbers of parasites when they arrived in the coastal area in the spring. Between April and June all parasites detached from the intermediate hosts and infected the definitive hosts (0+ whitingMerlangius merlangus forL. branchialis, and possibly sand gobyPomatoschistus minutus forL. lusci). Thereafter, flounder remained almost parasite-free until autumn. This suggests thatL. branchialis has only 1 generation per year. However, soles were infested again withL. lusci (in June and July), which detached to infest 0+bibTrisopterus luscus, the typical definitive host for this parasite species. Thus, it appears thatL. lusci has 2 generations per year. The flounder length and the infection intensity ofL. branchialis were not correlated throughout the study period. Significant positive correlations were found between the sole length and infection intensity ofL. lusci in late spring, but not in the summer or autumn. Throughout the year, bothL. lusci andL. branchialis were aggregated within their intermediate host populations (variance ≫ ≫ abundance).     

The parasitic copepod Lernaeocera branchialis negatively affects cardiorespiratory function in Gadus morhua

The parasitic copepod Lernaeocera branchialis had a negative effect on cardiorespiratory function in Atlantic cod Gadus morhua such that it caused pronounced cardiac dysfunction with irregular rhythm and reduced stroke amplitude compared with uninfected fish. In addition, parasite infection depressed the postprandial cardiac output and oxygen consumption.     

Survey of the metazoan ectoparasites of the European flounder Platichthys flesus (Linnaeus, 1758) along the north-central Portuguese coast

A survey was undertaken to identify metazoan ectoparasite species on the European flounder, Platichthys flesus (Linnaeus, 1758), in 4 different locations off the north-central Portuguese coast. Parasites of 7 different taxa were found: Caligus diaphanus, Caligus sp., and Lepeophtheirus pectoralis (Copepoda: Caligidae); Acanthochondria cornuta (Copepoda: Chondracanthidae); Holobomolochus confusus (Copepoda: Bomolochidae); Nerocila orbignyi (Isopoda: Cymotholdae); and praniza larvae (Isopoda: Gnathiidae). Lernaeocera branchialis, a common European flounder parasite in the North and Baltic Seas, was not observed among the surveyed fish. Caligus diaphanus, Caligus sp., and Nerocila orbignyi are new host records. The high prevalence and intensity values recorded for L. pectoralis and A. cornuta suggest that both parasite species are common to the European flounder along the north-central Portuguese coast. In contrast, infection levels with respect to the other parasite taxa were, in most cases, comparatively lower, thereby indicating that they only occur occasionally among flounders in the surveyed area.     

Genomic Resources for Sea Lice: Analysis of ESTs and Mitochondrial Genomes

Sea lice are common parasites of both farmed and wild salmon. Salmon farming constitutes an important economic market in North America, South America, and Northern Europe. Infections with sea lice can result in significant production losses. A compilation of genomic information on different genera of sea lice is an important resource for understanding their biology as well as for the study of population genetics and control strategies. We report on over 150,000 expressed sequence tags (ESTs) from five different species (Pacific Lepeophtheirus salmonis (49,672 new ESTs in addition to 14,994 previously reported ESTs), Atlantic L. salmonis (57,349 ESTs), Caligus clemensi (14,821 ESTs), Caligus rogercresseyi (32,135 ESTs), and Lernaeocera branchialis (16,441 ESTs)). For each species, ESTs were assembled into complete or partial genes and annotated by comparisons to known proteins in public databases. In addition, whole mitochondrial (mt) genome sequences of C. clemensi (13,440 bp) and C. rogercresseyi (13,468 bp) were determined and compared to L. salmonis. Both nuclear and mtDNA genes show very high levels of sequence divergence between these ectoparastic copepods suggesting that the different species of sea lice have been in existence for 37–113 million years and that parasitic association with salmonids is also quite ancient. Our ESTs and mtDNA data provide a novel resource for the study of sea louse biology, population genetics, and control strategies. This genomic information provides the material basis for the development of a 38K sea louse microarray that can be used in conjunction with our existing 44K salmon microarray to study host–parasite interactions at the molecular level. This report represents the largest genomic resource for any copepod species to date.     

The use of fish metabolic, pathological and parasitological indices in pollution monitoring

  An integrated biological effect monitoring concept has been tested in flounder (Platichthys flesus L.) from four locations with different anthropogenic impact in the German Bight. During 3 years of sampling, biomarkers at all levels of biological organisation from the molecular to the ecosystem level were applied and tested on 742 individual fish of body lengths between 18 and 25 cm. At the ecosystem level, the fish were taken as a habitat for the parasite assemblage. The hypothesis was that changes in the environment might lead to changes in the species diversity of parasites and in the infection intensity of single species, as well as between heteroxenic and monoxenic parasite species (H/M ratio). At the molecular level, activity of the CYP1A-dependent monooxygenase ethoxyresorufin O-deethylase (EROD) was used as a biomarker of exposure. At the subcellular level, the integrity of lysosomal membranes in hepatocytes was taken as an indicator of non-specific acute and chronic toxic effects. Both biomarkers are recommended by the ICES Advisory Committee on the Marine Environment for the application in biological effects monitoring programmes. In addition, neutral lipid content in the liver was used as a marker for pathologically induced fat accumulation. In the same individual fish, a new method for the measurement of macrophage aggregate activity in the liver was tested for its application and reliability in reflecting immunosuppression. Tests were accompanied by chemical analysis of standard organochlorine and heavy metal residues in flounder tissue. A total of 33 parasite species were found. As an indicator species, the mean abundance of Trichodina sp. reflected best the pollution gradient observed with highest infection intensity at the most polluted location. Species diversity was significantly higher in fish caught near the reference site and significantly lower in fish from the polluted Elbe estuary. The use of the heteroxenous/monoxenous species ratio as a marker was not useful at the locations investigated because of the dominance of heteroxenous species at all habitats. Since EROD activity and macrophage aggregate activity were dependent on sex and maturity of female flounder, only male fish were taken into consideration for the integrated evaluation of data. All biochemical and histochemical tests were able to reflect accurately the site-specific differences, as well as an observed pollution event at the end of 1995 as determined by chemical analyses. The correlation analysis revealed a connection not only between the single parasitological and biochemical parameters but also within these groups. The non-specific immune response and Trichodina infection intensity were correlated with all other parameters, leading to the assumption that these may serve as links between the lowest and the highest levels of biological organisation. The simultaneous use of metabolic and parasitological results facilitated the interpretation of the observed variations of the data and the distinction between natural variation and pollution-mediated effects. Received: 1 March 1999 / Received in revised form: 25 May 1999 / Accepted: 7 June 1999     

Maintenance of two genetic entities by habitat selection

Summary In the laboratory, the two species of copepodsLepeophtheirus thompsoni andLepeophtheirus europaensis, ectoparasites of flatfishes, can meet and mate on at least one host species. In the wild however, these two species are found isolated on their sympatric hosts. Habitat selection theoretically represents a powerful enough mechanism to explain the maintenance of genetic heterogeneity in the wide sense. In this paper, the host colonization process is studied for both parasite species. It is shown that each parasite can develop and reach adult age on each host species. However,L. thompsoni is highly selective; it almost totally refuses to colonize hosts other than its natural one.Lepeophtheirus europaensis, on the contrary, readily infests turbot and brill in single-host experiments, but strongly prefers the brill when it has a choice. It appears that these two genetic entities are sympatrically maintained due to strong habitat selection. Such a pattern could theoretically only occur in a soft-selection context (density dependence). This point is discussed with respect to the different patterns in host use found in the geographical distribution of these parasites.     

Regional differences in the infection of wild Japanese macaques by gastrointestinal helminth parasites

A coprological survey of gastrointestinal parasites in wild Japanese macaques (Macaca fuscata), from 14 natural habitats was done. Ova of five nematode species (Trichuris trichiura, Strongyloides fuelleborni, Streptopharagus pigmentatus, Oesophagostomum aculeatum, andGongylonema species) and a worm of the cestode species,Bertiella studieri, were detected. Some differences found in rates of infection by sex were observed in the 14 areas. Differences based on age were found in only troops in which the infection rates ofStrongyloides fuelleborni, Streptopharagus pigmentatus, andTrichuris trichiura were higher in the juvenile monkeys. The number of parasite species was related to the geographical and climatic conditions of the habitat of the troop: troops living in areas cold in winter were infected by fewer parasite species than those in southern warmer areas.     

Chemical monitoring in the Dutch Wadden Sea by means of benthic invertebrates and fish

In monitoring, it is of utmost importance to carefully define the purpose, the sampling strategy, as well as the analytical chemical and statistical requirements. Surveys are appropriate for describing the geographical variation in environmental contaminant levels. Repeated surveys and recurrentdata collection at permanent locations provide means of detecting temporal trends. Results are presented here of surveys on pollution by trace metals, polychlorinated biphenyls and organochlorine pesticides in the Ems Estuary and Dutch Wadden Sea usingMytilus edulis, Mya arenaria, Arenicoia marina, Nereis diversicolor andCrangon crangon as test organisms. Trends towards decreasing pollution by mercury are illustrated by monitoring data onMytilus edulis andZoarces viviparus. It is stressed that the results of chemical monitoring in organisms may be interpreted only in termser the biological effects on the basis of relevant toxicological knowledge and/or additional bio-assays. Presented at the VI International Wadden Sea Symposium (Biologische Anstalt Helgoland Wattenmeerstation Sylt, D-2282 List, FRG, 1–4 November 1988)     

Ultrastructural studies on the early cuticular metamorphosis of adult female Lernaeocera branchialis (L.) (Copepoda,Pennellidae)

After its final moult and fertilization an adult female of the marine fish-parasitic copepod, Lernaeocera branchialis, begins an extensive metamorphosis. This commences while the parasite is still on the flounder intermediate host and is completed once the female has established itself on the whiting final host. One early component of the metamorphosis is a considerable elongation of the parasite's abdominal region. S.e.m. and t.e.m. studies have revealed that part of the mechanism of the elongation consists of a straightening out of a highly folded abdominal cuticle. Before fertilization, the epicuticle and outer procuticular layers of this integument are thrown into a series of transverse, 4–6 µm deep pleats or folds with a density of 1–1.2 folds/µm of abdominal length. Straightening these folds can generate an approximately 6-fold length increase. The folds are already present beneath the female chalimus IV cuticle when the epidermis of this development stage starts to secrete the adult cuticle. Immediately before the final moult, the adult cuticle is super-folded with the whole cuticle displaying second-order folds, 8–10 µm deep.The capacity of Lernaeocera to engage in extensive cuticular modifications without recourse to a moult is compared with similar abilities shown by some insect species.     

Multi-annual changes in the parasite communities of rabbitfish Siganus rivulatus (Siganidae) in the Gulf of Aqaba, Red Sea

The parasite communities of the rabbitfish, Siganus rivulatus, were used to track multi-annual changes in the northern Gulf of Aqaba, Red Sea, in an environment subjected to ongoing anthropogenic impact. Parasitological data from these fish were collected from 1998 to 2000, with spring and fall samplings at three locations: at a coral reef (OBS), at a sandy beach area (NB) and at a mariculture cage farm (FF). These data were compared with data from 1995–1997 as well as data collected during 1981–1985 at the coral reef sampling site. The data analyses indicate that the ratio between heteroxenous and monoxenous parasite species declined significantly at all sites between 1995–1997 and 1998–2000. During the same period, the species richness of monoxenous parasites increased significantly at all sites. The species richness of heteroxenous parasites decreased significantly at the coral reef site, but remained steady at the other two sites. This coincided with a significant increase in the prevalence of monogeneans at the OBS and FF sites and a significant decrease in the prevalence of digeneans at the FF and NB sites. The decline in the abundance of the latter, specifically of Opisthogonoporoides sp. and Gyliauchen sp., was even more significant when compared with the 1981–1985 data. The prevalence of other gut helminths, namely the digenean Hexangium sigani and the nematodes Cucullanus sigani and Procamallanus elatensis, however, showed a significant increase over the same period. Analysis of the species richness and diversity indices of the parasite communities did not reveal conspicuous differences. These, however, did become apparent when heteroxenous and monoxenous members of particular taxa were analyzed separately. Therefore, when using parasite assemblages to detect ecological changes, it is essential to analyze not only at the community level, but also to consider separate components of particular parasitic groups. Communicated by H. von Westernhagen, A. Diamant     

The ultrastructure of the spermatozoon of Lernaeocera branchialis (Copepoda : Pennellidae)

Spermatozoa are produced by males of the fish-parasitic copepod, Lernaeocera branchialis, on the flounder (Platichthys flesus) host and packaged into spermatophores. Mature spermatozoa from spermatophores have been investigated with light microscopy and t.e.m. and s.e.m. techniques. Each is a filiform cell up to 30 µm long and 1 µm in diameter, being symmetrically tapered at each end to produce a javelin-shaped configuration. Surface s.e.m. appearances suggest that the cell is helically twisted. The spermatozoon possesses no flagellum, no nuclear envelope, no mitochondria and no orthodox acrosome. For most of its length the cell has a four-lobed appearance in transverse section and contains little more than a cylindrical sleeve of pseudomembranous material with which is associated finely filamentous or granular material which is assumed to be nuclear chromatin. The spermatozoon is immobile in seawater.The ultrastructure of L. branchialis spermatozoa has been compared with that of eight other copepod species.     

Trichodinid ectoparasites (Ciliophora: Peritrichida) of freshwater fishes of the Zambesi River System,with a reappraisal of host specificity

Over a period of five years parasitological surveys were carried out on the freshwater fish fauna in the eastern Caprivi which included the upper Zambesi River, a section of the Chobe and Kwando Rivers, and vast swampy areas. This area is well known for its wide variety of indigenous fish and has so far not been influenced in any way by introduced alien fish species. In these surveys 45 different fish species of 12 families were examined. This paper reports on the parasites of the generaTrichodina andHemitrichodina of the eastern Caprivi. A total of 15 species of parasites were recorded of which nine are new species described here-in. The list of host records of known species are expanded and an evaluation of host specificity based on information recorded in this survey as well as previously published data from southern Africa is provided.     

Experimental studies on the development of Lernaeocera branchialis (Copepoda: Pennellidae): population processes from egg production to maturation on the flatfish host

Quantitative population dynamical information derived from laboratory- and field-based experiments is provided for the fish-parasitic copepod, Lernaeocera branchialis, infecting flounder (Platichthys flesus) and whiting (Merlangius merlangus). Adult, post-metamorphosis females from whiting can produce more than one set of egg-strings. The mean number of eggs in each egg-string pair was 1445. At 10 °C these eggs took about 12.7 d after extrusion before hatching of NI nauplii began. Hatching took up to 12 days to be completed with an exponentially declining pattern of output over this period. In the laboratory about 44% of the egg-string egg population successfully passed through the NI to NII nauplius moult and the NII to copepodid moult to produce infective copepodids, a process lasting about 2 d. The non-feeding copepodids had a maximum survival time at 10 °C of 18 d, with a time to 50% survival of 7.5 d. In laboratory infection experiments at 10 °C, copepodids infected flounder and passed through all their developmental stages to adulthood and copulation in a minimum of 25 d. Field experiments on the seabed off Lowestoft in June 1987 with a sea temperature of about 16 °C suggested that the developmental period in those conditions could be as short as 11 d. Previously uninfected flounder in the field experiments became naturally infected with copepodids at a mean rate of not less than 30 parasites per fish d^–1.     

The parasite community infecting flounders, Platichthys flesus, in the tidal Thames.

The composition of the parasite fauna of the flounder, Platichthys flesus, retrieved from two locations in the tidal Thames is described in detail for the first time. The combined parasite species list of the flounders from Lots Road in the upper tideway and West Thurrock in the middle tideway consisted of one protozoan (Glugea stephani), one monogenean (Gyrodactylus sp.), four larval digeneans (Cryptocotyle concava, Timoniella imbutiforme, T. praeterita, and Labratrema minimus), five adult digeneans (Derogenes varicus, Lecithaster gibbosus, Podocotyle sp., Plagioporus varius, and Zoogonoides viviparus), one larval cestode (unidentified tetraphyllidean), one or possibly more larval nematodes (unidentified) plus five adult nematodes (Capillaria sp., Cucullanus heterochrous, C. minutus, Contracaecum sp. and Goezia sp.), two acanthocephalans (Pomphorhynchus laevis and Acanthocephalus anguillae), three copepods (Lepeophtheirus pectoralis, Acanthochondria sp. and Lernaeocera branchialis), and one mollusc (unidentified glochidia). The overall parasite community of flounders from Lots Road and West Thurrock were compared in terms of species richness and diversity. The parasite community in flounders from the former location in the upper tideway was found to be less diverse than that of its counterpart at West Thurrock in the middle estuary. The component community of Lots Road flounders was dominated by the acanthocephalan Pomphorhynchus laevis.     

The population dynamics of the parasitic copepodeLernaeocera lusci (Bassett-Smith, 1896) on its definitive host

The mesoparasitic copepodLernaeocera lusci (Bassett-Smith, 1896) was recovered from first-year bib (Trisopterus luscus L.) in the Voordelta (Southern Bight of the North Sea) from May until December 1989. Analysis of the seasonal abundance and of the population structure showed that transmission of infective stages to bib mainly occurred from June to September. From September to December the overall prevalence fluctuated around 70%. Maximum parasite population size (47/10⁴m²) and the highest total egg number were recorded in September and October, respectively. It was found that total parasite mortality was significantly influenced by mortality of hosts carrying parasites. Natural mortality probably contributed a small percentage to total parasite mortality. Calculation of the temporal mean-variance regression equation revealed that the parasites were aggregated within the definitive host population.     

Assessment of Epinephelus coioides (Hamilton, 1822) aquaculture systems in the Gulf of Tonkin,Vietnam, by using fish parasites

The parasite fauna of Epinephelus coioides can be used as an indicator to assess different aquaculture systems. A total of 133 E. coioides were collected from fishermen (wild fish) and marine fish farms (net cages, pond farms) in the Gulf of Tonkin (Ha Long, Cat Ba and Nghia Hung), Vietnam in 2013 and 2014, and examined for the presence of protozoan and metazoan parasites. Different patterns of parasite infections were found. The monogenean Pseudorhabdosynochus spp. was predominant in the net cage system; and the protozoans Trichodina spp. and Cryptocaryon irritans were found exclusively in pond and net cage cultivation sites in Nghia Hung and Cat Ba. These three species were assessed in addition to seven further indicator species and two dominance indices, to visualize the potential of assessing different aquaculture systems in Vietnam. This suggests the use of former shrimp ponds for grouper cultivation, reducing the pressure to further extend net cage cultivation in already highly influenced mariculture regions in Vietnam.     

Hematological values and parasite fauna in free-rangingMacaca hecki and theM. hecki/M. tonkeana hybrid group of Sulawesi Island, Indonesia

Hematological values and parasitological fauna of free-rangingMacaca hecki and the hybrid group betweenM. hecki/M. tonkeana of Sulawesi Island, Indonesia, were investigated. The hematological values, especially the red cell number (RBC), were lower than those of other macaque species, indicating that Sulawesi macaques are slightly anemic. Several parasites including Plasmodium sp., trombiculid mites, andTrichuris trichiura were identified. Although infection by Plasmodium was observed with considerable frequency, no clear relationship between its infection and the occurrence of anemia was found. Trombiculid mites and eggs ofAnatrichosoma sp. were detected in foci of the ears of most monkeys. The infection with a trombiculid mite is the first recorded occurrence in free-ranging wild Sulawesi macaques. Gastrointestinal parasites were identified from their eggs in fecal samples, where five species of nematoda and one trematoda species were found.