Effects of temperature on fecundity in vitro, egg hatching and reproductive development of Benedenia seriolae and Zeuxapta seriolae (Monogenea) parasitic on yellowtail kingfish Seriola lalandi

Globally, aquaculture industries involved with commercial culture of kingfish (Seriola spp.) experience outbreaks of monogenean parasites, which can cause heavy stock losses. In Australia and New Zealand, aquaculturists of kingfish Seriola lalandi incur financial losses caused by two monogenean species: Benedenia seriolae and Zeuxapta seriolae which parasitise the skin and gills, respectively. This study provides information on some basic temperature-dependent life-cycle parameters of these problematic monogeneans on S. lalandi. Hatching times and age at maturity were inversely related to water temperature within the range experienced by wild kingfish in New Zealand (13-21 degrees C). Mature B. seriolae in vitro laid on average 37 eggs/day that hatched over approximately 4 days; peak hatching occurred 9, 11 and 22 days post-deposition at temperatures of 21, 17.5 and 13+/-1.0 degrees C, respectively. Z. seriolae in vitro laid on average 246 eggs/day that hatched over 2 days; peak hatching occurred 7, 9 and 15 days post-deposition at these respective temperatures. B. seriolae matured within 20, 25 and 48 days p.i. at 21, 18 and 13 degrees C. Z. seriolae matured within 25, 37 and >52 days p.i. at the same temperatures. This research describes stages in the reproductive development of B. seriolae and Z. seriolae and discusses the inclusion of basic parasitic life-cycle parameters into management strategies designed to maximise treatment efficacy and limit monogenean epizootics in sea-cage kingfish culture.     

Metabolism of praziquantel in kingfish Seriola lalandi

Investigations into the metabolism of drugs used in aquatic animal therapy are useful for understanding the mechanisms of xenobiotic transformation systems and can aid the development of dosing regimens. This study investigated the metabolism of the synthetic anthelmintic praziquantel, which has application in helminthiasis treatment for several fish species including kingfish Seriola lalandi, a commercial aquaculture finfish species. At least 7 mono- or dihydroxylated derivatives of the parent compound were identified in kingfish after administration of a 150 mg kg(-1) oral praziquantel dose, paralleling findings in mammals. The structure of one representative mono-hydroxylated species that was prominent in the skin, muscle, liver, kidney and plasma of kingfish was investigated using fragmentation experiments; this revealed that hydroxylation of the parent molecule occurred in the tetrahydroisoquinoline region of praziquantel, analogous with mammalian metabolites, but different to that of the active mammalian metabolite (trans-4-OH-praziquantel). The implications of these findings with regard to biotransformation systems for this drug in mammals and fish are discussed.     

Effect of water temperature on reproductive development of Benedenia seriolae (Monogenea: Capsalidae) from Seriola lalandi in Australia

The monogenean Benedenia seriolae (Yamaguti, 1934) Meserve, 1938 is a major pathogen of farmed yellowtail kingfish Seriola lalandi in South Australia. To control parasite populations in commercial farms, an understanding of the effect of water temperature on parasite development is vital. This study investigated the effect of water temperature (14, 18, 22 and 26 +/- 0.5 degrees C) on development, growth rates and age at sexual maturity of B. seriolae. Five distinct developmental stages, defined by the progressive development of reproductive organs, were used to describe development of B. seriolae from recently invaded larvae to sexually mature adults. Parasite age at the first sign of sexual maturity (ability to lay eggs) was strongly influenced by water temperature and was attained at 41, 24, 16 and 14 d post infection (p.i.) at 14, 18, 22 and 26 +/- 0.5 degrees C respectively. Four parameters (parasite total length, maximum parasite width, accessory sclerite length and anterior hamulus length) were examined for suitability as an index of parasite age. Growth rates for each parameter increased with water temperature; however, mean anterior hamulus length was identified as the most reliable index of parasite age. Equations derived from these data can be used to estimate parasite age and time to sexual maturity at water temperatures ranging from 14 to 26 degrees C. The equations provide a simple tool to assist implementation of strategic treatment plans for B. seriolae infections in commercial kingfish farms, not only in South Australia but in other localities worldwide where S. lalandi is farmed.     

Bioavailability and pharmacokinetics of a praziquantel bolus in kingfish Seriola lalandi

Oral praziquantel (PZQ) preparations have recently been investigated for the treatment of monogeneans that infect the skin and gills of kingfish Seriola lalandi cultured in sea-cages. To evaluate an oral PZQ dosing strategy, the pharmacokinetics of a dissolved and in feed oral PZQ preparation (40 mg kg(-1) body weight) were compared with an intravenous bolus in kingfish plasma and skin using HPLC. Compared with intravenous administration, PZQ bioavailability (area under curve, AUC0-24h) was slightly improved when the drug was administered with food in both kingfish plasma (56.8% in feed vs. 50.8% in solution) and skin (55.5% in feed vs. 50.3% in solution). After oral dosing, maximum drug concentrations in skin were approximately one-third of those achieved in plasma and higher when the drug was administered in solution (5.26 microg ml(-1)) than in feed (3.96 microg ml(-1)); additionally, the time to achieve maximum PZQ concentration was similar in plasma and skin, although markedly reduced when the drug was administered in solution (1 h) than in feed (6 h). However, clearance of the drug was delayed in skin; administered as an oral formulation, PZQ concentrations in the systemic circulation fell below the limit of quantification after 24 h, but remained quantifiable (0.3 microg g(-1)) in skin at this time. These initial studies indicate that a daily treatment interval will lead to the exposure of parasites to highly variable anthelmintic concentrations, which may be sub-optimal for the treatment of monogeneans in this finfish species.     

Ontogeny of body density and the swimbladder in yellowtail kingfish Seriola lalandi larvae

The ontogeny of larval body density and the morphological and histological events during swimbladder development were investigated in two cohorts of yellowtail kingfish Seriola lalandi larvae to understand the relationship between larval morphology and body density. Larvae <3 days post hatch (dph) were positively buoyant with a mean ± s.d . body density of 1·023 ± 0·001 g cm^?3. Histological evidence demonstrated that S. lalandi larvae are initially transient physostomes with the primordial swimbladder derived from the evagination of the gut ventral to the notochord and seen at 2 dph. A pneumatic duct connected the swimbladder to the oesophagus, but degenerated after 5 dph. Initial swimbladder (SB) inflation occurred on 3 dph, and the inflation window was 3–5 dph when the pneumatic duct was still connected to the gut. The swimbladder volume increased with larval age and the epithelial lining on the swimbladder became flattened squamous cells after initial inflation. Seriola lalandi developed into a physoclist with the formation of the rete mirabile and the gas‐secreting gland comprised low‐columnar epithelial cells. Larvae with successfully inflated swimbladders remained positively buoyant, whereas larvae without SB inflation became negatively buoyant and their body density gradually reached 1·030 ± 0·001 g cm^?3 by 10 dph. Diel density changes were observed after 5 dph, owing to day time deflation and night‐time inflation of the swimbladder. These results show that SB inflation has a direct effect on body density in larval S. lalandi and environmental factors should be further investigated to enhance the rate of SB inflation to prevent the sinking death syndrome in the early life stage of the fish larvae.     

Dietary fish oil replacement with canola oil up-regulates glutathione peroxidase 1 gene expression in yellowtail kingfish (Seriola lalandi)

The marine carnivore yellowtail kingfish (YTK, Seriola lalandi) was fed diets containing 5% residual fish oil (from the dietary fish meal) plus either 20% fish oil (FO), 20% canola oil (CO), 20% poultry oil (PO), 10% fish oil plus 10% canola oil (FO/CO) or 10% fish oil plus 10% poultry oil (FO/PO) and the effects on fish growth and hepatic expression of two glutathione peroxidase (GPx 1 and GPx 4) and two peroxiredoxin (Prx 1 and Prx 4) antioxidant genes were investigated. Partial (50%) replacement of the added dietary fish oil with poultry oil significantly improved fish growth whereas 100% replacement with canola oil significantly depressed fish growth. The fatty acid profiles of the fish fillets generally reflected those of the dietary oils except that there was apparent selective utilization of palmitic acid (16:0) and oleic acid (18:1n-9) and apparent selective retention of eicospentaenoic acid (EPA, 20:5n-3) and docosahexaenoic acid (DHA, 22:6n-3). The Prx 1 and 4 genes were expressed at 10- and 100-fold the level of the GPx 4 and 1 genes, respectively, and at one-tenth the level of the highly expressed β-actin reference gene. Dietary fish oil replacement with canola oil significantly up-regulated GPx 1 gene expression and there was a non-significant tendency towards down-regulation of Prx 1 and Prx 4. The results are discussed in terms of the effects of fish oil replacement on the peroxidation index of the diets and the resulting effects on the target antioxidant enzymes.     

Unilateral ablation of trunk superficial neuromasts increases directional instability during steady swimming in the yellowtail kingfish Seriola lalandi

Detailed swimming kinematics of the yellowtail kingfish Seriola lalandi were investigated after unilateral ablation of superficial neuromasts (SNs). Most kinematic variables, such as tail‐beat frequency, stride length, caudal fin‐beat amplitude and propulsive wavelength, were unaffected but lateral amplitude at the tip of the snout (A₀) was significantly increased in SN‐disrupted fish compared with sham‐operated controls. In addition, the orientation of caudal fin‐tip relative to the overall swimming direction of SN‐disrupted fish was significantly deflected (two‐fold) in comparison with sham‐operated control fish. In some fish, SN disruption also led to a phase distortion of the propulsive body‐wave. These changes would be expected to increase both hydrodynamic drag and thrust production which is consistent with the finding that SN‐disrupted fish had to generate significantly greater thrust power when swimming at ≥1·3 fork lengths (L_F) s^?1. In particular, hydrodynamic drag would increase as a result of any increase in rotational (yaw) perturbation and sideways slip resulting from the sensory disturbance. In conclusion, unilateral SN ablation produced directional instability of steady swimming and altered propulsive movements, suggesting a role for sensory feedback in correcting yaw and slip disturbances to maintain efficient locomotion.     

Egg-laying patterns and in vivo egg production in the monogenean parasites Heteraxine heterocerca and Benedenia seriolae from Japanese yellowtail Seriola quinqueradiata

Egg-laying patterns and egg production in Heteraxine heterocerca from the gills and Benedenia seriolae from the skin of Japanese yellowtail Seriola quinqueradiata in Japan were investigated in vivo. Eggs were collected every 3 h from sexually mature H. heterocerca and B. seriolae infecting 3 S. quinqueradiata kept individually over 3 consecutive days and exposed to alternating periods of illumination and darkness (LD 12:12; light on 06.00, light off 18.00) and maintained at 23.8 +/- 0.1 degrees C and 35 ppt salinity. A well-defined egg-laying rhythm was demonstrated for H. heterocerca while B. seriolae was shown torelease eggs continuously. A total of 114,000 H. heterocerca eggs was collected and of these, 45.4 (42.5-49.9)% were collected during the first 3 h period following dark at 18.00 h. A total of 662,857 B. seriolae eggs was collected and these were distributed over each 3 h period ranging from 11.1 to 14.1% of the daily egg output. All eggs extracted from the uterus of each H. heterocerca were joined together forming an 'egg-string'. The contrasting egg-laying patterns of H. heterocerca and B. seriolae suggest that each species makes use of a different infection strategy to infect the same host species, S. quinqueradiata.     

Attachment-inducing capacities of fish skin epithelial extracts on oncomiracidia of Benedenia seriolae (Monogenea: Capsalidae)

Attachment-inducing capacities of skin epithelial extracts of yellowtail, Japanese flounder and red sea bream on oncomiracidia of the monogenean Benedenia seriolae were examined. Clear differences were not detected in the capacity among the fish species, although B. seriolae infects only yellowtail and its congeners in Seriola. This suggests that either the capacity is not host specific or host-specific attachment-inducing capacity cannot be detected by the assay method. Further, the attachment-inducing capacities were suppressed by wheat-germ lectin and concanavalin A in skin epithelial extracts of Japanese flounder and yellowtail, respectively. This suggests that some sugar-related chemical substances existing in fish epithelia induce the attachment of B. seriolae oncomiracidia.     

Unicapsula seriolae n. sp. (Myxosporea,Multivalvulida) from Australian Yellowtail Kingfish Seriola lalandi1

Unicapsula seriolae n. sp. forms long plasmodia within the striated muscle fibers of Seriola lalandi off eastern Australia. Its spores are composed of three valves, only one of which contains a developed polar capsule. Within the capsule, the filament makes 2 1/2–3 turns, and this criterion can be used to separate U. seriolae from the two other members of the genus. The flesh of infected fish disintegrates during slow cooking.     

Quantitative Trait Loci (QTL) Associated with Resistance to a Monogenean Parasite (Benedenia seriolae) in Yellowtail (Seriola quinqueradiata) through Genome Wide Analysis

Benedenia infections caused by the monogenean fluke ectoparasite Benedenia seriolae seriously impact marine finfish aquaculture. Genetic variation has been inferred to play a significant role in determining the susceptibility to this parasitic disease. To evaluate the genetic basis of Benedenia disease resistance in yellowtail (Seriola quinqueradiata), a genome-wide and chromosome-wide linkage analyses were initiated using F₁ yellowtail families (n = 90 per family) based on a high-density linkage map with 860 microsatellite and 142 single nucleotide polymorphism (SNP) markers. Two major quantitative trait loci (QTL) regions on linkage groups Squ2 (BDR-1) and Squ20 (BDR-2) were identified. These QTL regions explained 32.9–35.5% of the phenotypic variance. On the other hand, we investigated the relationship between QTL for susceptibility to B. seriolae and QTL for fish body size. The QTL related to growth was found on another linkage group (Squ7). As a result, this is the first genetic evidence that contributes to detailing phenotypic resistance to Benedenia disease, and the results will help resolve the mechanism of resistance to this important parasitic infection of yellowtail.     

Drug resistance and pulsed-field gel electrophoresis patterns of Lactococcus garvieae isolates from cultured Seriola (yellowtail, amberjack and kingfish) in Japan

AIMS: To investigate the existing antimicrobial susceptibility and genetic characteristics of Lactococcus garvieae isolates from cultured Seriola in Japan. METHODS AND RESULTS: Minimum inhibitory concentrations (MICs) of 14 antimicrobial agents for 170 isolates were determined using the agar dilution method. Seventy-five isolates (44.1%) were simultaneously resistant to erythromycin (EM) (MIC>or=2 microg ml-1), lincomycin (LCM) (MIC>or=128 microg ml-1) and oxytetracycline (OTC) (MIC>or=4 microg ml-1). Resistance to EM was grouped as intermediate- and high-level resistant by MIC values. All resistant isolates possessed ermB and tet(S) genes. The number of different bands between pulsed-field gel electrophoresis patterns of 25 isolates and two ATCC strains (isolated in 1974), determined using two enzymes (ApaI and SmaI), did not exceed 3. CONCLUSIONS: The present resistance pattern observed with ermB and tet(S) is similar to that observed in previous reports. Moreover, the genetic characteristics of L. garvieae isolates from a wide area in Japan in 2002 and ATCC strains were closely related. SIGNIFICANCE AND IMPACT OF THE STUDY: This study suggests that EM-, LCM- and OTC-resistant isolates have been present for 15 years and that L. garvieae strains with same origin have spread among Seriola spp. in Japan since 1974.     

Spatio‐temporal patterns of genetic variations in populations of yellowtail kingfish Seriola lalandi from the south‐eastern Pacific Ocean and potential implications for its fishery management

The genetic population structure and genetic diversity of yellowtail kingfish Seriola lalandi from the coastal south‐eastern Pacific Ocean (SEP) were evaluated at spatiotemporal scale in order to understand the ecology of this species. Between 2012 and 2015, temporal and spatial population genetic structure and a low genetic diversity were detected in S. lalandi from SEP. These results suggest that S. lalandi specimens arriving annually from offshore to the SEP coast could come from at least two genetically distinct populations, revealing a particular life strategy (i.e. reproductive or habitat segregation) for this fish species. Therefore, the SEP coast might constitute a point of population mixing for this species. Additionally, the low genetic diversity of S. lalandi in the SEP could be a result of a founder effect or overfishing. Regardless of the process explaining the genetic diversity and structure of S. lalandi in this geographical area, this new information should be considered in order to implement successful fishery management of this resource in the South Pacific.     

Drug resistance and random amplified polymorphic DNA analysis of Photobacterium damselae ssp. piscicida isolates from cultured Seriola (yellowtail, amberjack and kingfish) in Japan

AIMS: To investigate the antimicrobial susceptibility and genetic characteristics of Photobacterium damselae ssp. piscicida isolates obtained from cultured Seriola in Japan. METHODS AND RESULTS: Minimal inhibitory concentrations of 14 antimicrobials for 74 isolates from Seriola in Japan in 2002 were determined. Isolates showed high frequencies of resistance to sulfamonomethoxine (SMMX) (97.3%), oxytetracycline (OTC) (77.0%), flumequine (FMQ) (77.0%), chloramphenicol (CP) (75.7%), kanamycin (KM) (63.5%) and oxolinic acid (OA) (62.0%), but low to ampicillin (ABPC) (2.8%). All isolates were susceptible to bicozamycin (BCM), fosfomycin (FOM) and florfenicol (FF). Of these isolates, 45 (60.8%) showed same resistance pattern (SMMX-OTC-FMQ-OA-CP-KM). In random amplified polymorphic DNA (RAPD) analysis, no difference was observed among our 74 field isolates and ATCC51736 isolated from Seriola in 1974 in Japan, but different from ATCC 17911 isolated from white perch in USA. CONCLUSIONS: FF, BCM, FOM and ABPC were useful antimicrobials for treating pseudotuberculosis. However, the frequency of multidrug resistance was high. RAPD analysis showed homogeneity of isolates from Seriola in Japan. SIGNIFICANCE AND IMPACT OF THE STUDY: This study demonstrates that some antimicrobials were still useful for treating pseudotuberculosis and that P. damselae ssp. piscicida strains of same origin might have spread among Seriola in Japan since 1974.     

Ceratomyxa seriolae n. sp. and C. buri n. sp. (Myxozoa: Myxosporea) from the gall-bladder of cultured yellowtail Seriola quinqueradiata

Ceratomyxa seriolae n. sp. and C. buri n. sp. (Myxozoa: Myxosporea) were found in the gall-bladder of cultured yellowtail Seriola quinqueradiata Temminck & Schlegel (Carangidae) in Japan. Mature spores of C. seriolae n. sp. were elongate and 6.5 (6.0-7.5) m long and 33.7 (28.0-41.5) m thick. Disporous plasmodia of C. seriolae n. sp., 40-100 m in size, were amoeboid to spherical. C. buri n. sp. were elliptical with a flattened posterior end, 6.5 (5.5-7.5) m long and 14.3 (11.0-16.5) m thick. Spherical plasmodia of C. buri n. sp., 15-20 m in diameter, were disporous. In periodical sampling of yellowtail bile from August, 1999 to February, 2000, the two new species of Ceratomyxa, as well as Myxobolus spirosulcatus Maeno, Sorimachi, Ogawa & Kearn 1995, first appeared in October, and the prevalences were very variable (20-100%) during the study period.     

Diet and diet-associated bacteria shape early microbiome development in Yellowtail Kingfish (Seriola lalandi)

The supply of quality juveniles via land-based larviculture represents a major bottleneck to the growing finfish aquaculture industry. As the microbiome plays a key role in animal health, this study aimed to assess the microbial community associated with early larval development of commercially raised Yellowtail Kingfish (Seriola lalandi). We used qPCR and 16S rRNA gene amplicon sequencing to monitor changes in the microbiome associated with the development of S. lalandi from larvae to juveniles. We observed an increase in the bacterial load during larval development, which consisted of a small but abundant core microbiota including taxa belonging to the families Rhodobacteraceae, Lactobacillaceae and Vibrionaceae. The greatest change in the microbiome occurred as larvae moved from a diet of live feeds to formulated pellets, characterized by a transition from Proteobacteria to Firmicutes as the dominant phylum. A prediction of bacterial gene functions found lipid metabolism and secondary metabolite production were abundant in the early larval stages, with carbohydrate and thiamine metabolism functions increasing in abundance as the larvae age and are fed formulated diets. Together, these results suggest that diet is a major contributor to the early microbiome development of commercially raised S. lalandi.     

Metazoan parasite assemblages of wild Seriola lalandi (Carangidae) from eastern and southern Australia

Yellowtail kingfish, Seriola lalandi support significant commercial and recreational fisheries as well as aquaculture operations throughout the world. Metazoan parasite infections of S. lalandi are of considerable economic and ecological importance, yet very little is known about wild parasite assemblages. S. lalandi were collected from the east coast and south coast of Australia and examined for metazoan parasites. Forty-three parasite taxa were identified, including 26 new host records. Four of the parasite species recovered have been previously associated with disease or mortality in Seriola aquaculture. Comparisons are made between ectoparasite and endoparasite prevalence and intensity of S. lalandi from New South Wales and Victoria. S. lalandi sampled from the east coast of Australia shared ectoparasites previously documented from this species in New Zealand, providing support that S. lalandi in the Tasman Sea comprise a single stock. Based on previously used criteria to evaluate the suitability of parasites as biological tags, the monogenean Paramicrocotyloides reticularis Rohde and the copepod Parabrachiella seriolae Yamaguti and Yamasu may be potentially useful for stock discrimination.