The infection dynamics and dispersion pattern of Lernaeocera branchialis L. on 0+ whiting (Merlangius merlangus L.) in the Oosterschelde (SW Netherlands)

Size and structure of the Lernaeocera branchialis population infecting 0+ whiting in the Oosterschelde were studied during 1989. Two periods of successful transmission were distinguished. The first transmission wave occurs in late spring when the post-larval whiting enter the Oosterschelde. A second wave occurs in autumn. This pattern in the infection dynamics is possibly related to seasonal variations in spatial overlap of the intermediate ( Platichthysflesus ) and the final host ( Merlangius merlangus ). The dispersion pattern of Lernaeocera branchialis within the whiting population can be described by the Poisson distribution. Possible explanations for the observed dispersion pattern are given. Evidence is presented that the rejection of pennella larvae is a key mechanism determining the abundance of L. branchialis in whiting. The potential impact of parasite-induced host mortality on population size and dispersion pattern of the parasite is discussed.     

The diet of whiting Merlangius merlangus in the western Baltic Sea

The diet of whiting Merlangius merlangus in the western Baltic Sea was investigated and compared to the diet in the southern North Sea. Clupeids were important prey in both areas, but especially in the western Baltic Sea where they constituted up to 90% of the diet of larger individuals. Gobies, brown shrimps and polychaetes were the main prey of juveniles in the western Baltic Sea, while a wider range of species were consumed in the North Sea. The shift to piscivory occurred at smaller sizes in the western Baltic Sea and the fish prey consumed was proportionately larger than in the southern North Sea. Estimates of prey abundance and food intake of M. merlangus are required to evaluate its predatory significance in the western Baltic Sea, but its diet suggests that it could be just as significant a fish predator here as in the southern North Sea.     

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.     

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.     

Growth and food consumption of whiting Merlangius merlangus

In the western Baltic Sea (WBS), whiting Merlangius merlangus is the main piscivorous fish together with cod Gadus morhua. In the present study, we investigate the growth and food consumption rates of WBS M. merlangus and compare the growth rates of males and females with those of M. merlangus in the North Sea (NS). Food consumption rates are estimated directly from sampled stomach contents in the WBS using a gastric evacuation rate model and indirectly by using a static energy‐budget model together with the growth rates. The results indicate that male and female M. merlangus in the WBS have similar feeding and growth strategies, while in the NS M. merlangus show more pronounced differences in food consumption and growth dynamics between the sexes. Female WBS M. merlangus grow significantly slower than their conspecifics in the NS, but there is no significant difference for males. Sexual size dimorphism is seen in both areas, but for M. merlangus in the WBS the difference is less pronounced. Food consumption rates in the WBS differ between seasons, with the lowest food intake in the first 2 quarters of the year and the highest in the 3rd quarter. No differences in consumption rates were seen between males and females, which could be related to the more similar growth pattern seen for M. merlangus in the WBS.     

Lernaeocera branchialis (L., 1767) on cod in Baltic waters

Field surveys have shown a limited distribution ofL. branchialis in Baltic waters due to heterogenic salinity. The parasite is not suited as “natural” tagging of the cod population in these waters.     

The appearance of accessory growth centres in adult whiting Merlangius merlangus otoliths

The appearance of accessory growth centres (AGCs) in the otoliths of adult whiting Merlangius merlangus reared in the laboratory for 2 years is reported. The causes and implications of AGCs appearing in otoliths of adult fish are discussed.     

Sex‐specific food intake in whiting Merlangius merlangus

In this study, the topic of sexual growth dimorphism in whiting Merlangius merlangus is examined. To understand the magnitude and underlying mechanisms, North Sea International Bottom Trawl Survey (IBTS) data and two additional datasets from the third quarter of 2007 and the first quarter of 2012 were analysed. Merlangius merlangus displays distinct differences in growth parameters between males and females, with females reaching a higher asymptotic length (L_∞) than males. To identify the mechanisms which lead to higher growth in females, the quantity and the quality of the diet of M. merlangus in the North Sea were investigated to compare the sex‐specific energy uptake levels. The diet composition did not differ between the sexes, but females had higher stomach content masses than males of the same total length (L_T), and showed lower proportions of empty stomachs. Moreover, female M. merlangus had higher liver and empty stomach masses compared with males of the same size, which indicates additional sex‐specific differences in the metabolic costs and energy allocation patterns. Finally, interannual differences were found in the stomach contents, the share of empty stomachs and liver masses of M. merlangus in the North Sea.     

The common dab as definitive host for the Pennellid copepods Lernaeocera branchialis and Haemobaphes cyclopterina

Seven (0.039%) and five (0·028%) of 18 163 common dab from the east coast of Scotland were definitive hosts to Lernaeocera branchialis and to Haemobaphes cyclopterina , respectively. Both represent new host records. Muscle necrosis and localized haemorrhage were associated with H. cyclopterina infestation and as described from other definitive hosts.     

Mitochondrial DNA sequence variation in whiting Merlangius merlangus in the North East Atlantic

Genetic variation in whiting Merlangius merlangus was examined using a 621 base pair fragment of the cytochrome c oxidase subunit I mitochondrial gene in 138 individuals sampled from Iceland, Norway and the North Sea. In total 10 segregating sites were observed defining 12 haplotypes. Three of the haplotypes were found at high frequencies (>5 %). All but one mutations were synonymous and the nonsynonymous mutation was found as a singleton. This suggests weak or no natural selection acting on the observed polymorphism making it useful for examination of population breeding structure. The genetic variation suggests that the whiting population has undergone sudden expansion in the past, estimated to have started 70 Kyr ago, during the last glacial period. Spatial genetic analysis reveals genetic uniformity across long geographic distances suggesting high level of gene flow. The long pelagic phase at early age, allowing for high dispersal rate, may partly explain the observed pattern.     

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.     

Gastric digestion and evacuation in whiting, Merlangius merlangus (L.)

Three meal sizes of sandeels were fed to whiting in order to monitor the evacuation of food out of the stomach. The stomach contents were sampled at intervals after feeding, using a stomach pump. In such experiments, the proportion of fish with empty stomachs tends to increase with time and, since stomach contents are limited to zero or positive values, the variance of the stomach contents becomes censored at zero. This tends to produce a curved relationship between mean stomach content and time, which gives the impression that evacuation rate slows down at low levels of stomach fullness. By taking account of censoring, it was shown that the evacuation curve generated for whiting was consistent with and could be generated from a linear model in which the rate of gastric evacuation exhibited by the fish was constant and independent of meal size, level of stomach fullness and time after feeding. The parameters of the linear model were estimated by maximum likelihood and then applied in a second model to predict the observed mean stomach content. The average gastric evacuation rate of whiting of mean weight 268 g at 10°C was 0.31 g h⁻¹.     

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.     

Dietary habits of fish populations in the Lower Medway Estuary

Populations of mainly first-year fish overwinter in the Medway Estuary, an area offering shelter and a rich and varied food supply. In the absence of previous investigations, the present study examines the dietary habits of four fish species; gadoids Merlangius merlangus and Trisopterus luscus , and pleuronectids Platichthys flesus and Pleuronectes platessa .
Gadoids fed predominantly on fast moving nektonic organisms such as brown shrimps, mysids and fish while pleuronectids preferred the slower moving tubificid and polychaete worms. Seasonal fluctuations of the dietary constituents are considered in relation to changes within the populations of both prey and predator organisms.     

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

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

Assessment of egg quality and realised fecundity of whiting Merlangius merlangus L. in captivity

Potential predictors of egg quality were assessed in whiting Merlangius merlangus L. permitted to spawn in a tank from which eggs were collected. These included fertilisation rate, the proportion of viable buoyant eggs, egg diameter, and egg wet and dry weights; all were influenced by temporal effects and were negatively correlated with days from start of spawning. The spawning period was protracted, from February to June. Mean daily egg production per female was 2.74 ± 2.43 g and 2338 ± 2075 eggs, equivalent to 14.6 ± 13.1 g kg^?1 day^?1 female^?1. Egg diameter was 1.21 ± 0.04 mm, egg wet weight 1.20 ± 0.21 mg, dry weight 0.10 ± 0.02 mg, and mean fertilisation rate and hatching rates were 76.8 and 73.3%, respectively. The incubation period ranged from 72 to 80 degree days and was dependent on temperature (x) and described by the equation y = 25.92 e^?0.1219x. Realised fecundity was also assessed to determine if this gave a more accurate measure of reproductive potential, and this was compared with potential fecundity estimated from predictive regressions on fish length from fisheries data. Realised egg production of 20 females of 185 g mean weight and 256 mm fork length was 4 444 360 (95% CL 4 093 961–4 743 018), similar to predicted seasonal egg production based on gravimetric fecundity measurements of wild caught fish.     

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.     

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.     

PCR amplification of a polymorphic minisatellite VNTR locus in whiting [Merlangius merlangus L.)

An approach has been developed for the screening of allelic variation at minisatellite DNA loci that substantially reduces the time and hazards involved. Primers were designed for a minisatellite region isolated from a gadoid fish species [Merlangius merlangus L.), enabling amplification by polymerase chain reaction, so that differences in the number of minisatellite repeat units (allelic variability) were detectable by ethidium bromide fluorescence (over UV light) following separation by agarose gel electrophoresis. This amplifiable minisatellite variable number tandem repeat region, the first non-primate marker of its kind, can be used successfully with DNA extracted by a rapid Chelex® protocol. From a sample of 97 individuals, 24 alleles were resolved (750–2200 kb) and heterozygosity was estimated at 0–94.     

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).