Effects of host migration, diversity and aquaculture on sea lice threats to Pacific salmon populations

Animal migrations can affect disease dynamics. One consequence of migration common to marine fish and invertebrates is migratory allopatry-a period of spatial separation between adult and juvenile hosts, which is caused by host migration and which prevents parasite transmission from adult to juvenile hosts. We studied this characteristic for sea lice (Lepeophtheirus salmonis and Caligus clemensi) and pink salmon (Oncorhynchus gorbuscha) from one of the Canada's largest salmon stocks. Migratory allopatry protects juvenile salmon from L. salmonis for two to three months of early marine life (2-3% prevalence). In contrast, host diversity facilitates access for C. clemensi to juvenile salmon (8-20% prevalence) but infections appear ephemeral. Aquaculture can augment host abundance and diversity and increase parasite exposure of wild juvenile fish. An empirically parametrized model shows high sensitivity of salmon populations to increased L. salmonis exposure, predicting population collapse at one to five motile L. salmonis per juvenile pink salmon. These results characterize parasite threats of salmon aquaculture to wild salmon populations and show how host migration and diversity are important factors affecting parasite transmission in the oceans.     

Residence time of the sea louse, Lepeophtheirus salmonis K., on Atlantic salmon, Salmo salar L., after immersion in fresh water

Returning adult salmon caught at the mouth of the River Dee, Aberdeenshire, were transferred to tanks in the laboratory. For fish placed in fresh water, sea lice remained attached for up to 6 days, though most lice were lost in the first 48 hours. Few lice were lost from salmon maintained in sea water. The experiments were conducted in water within a temperature range of 12·8 to 16° C, equivalent to summer river temperatures in the Aberdeenshire Dee.     

Sea lice and salmon population dynamics: effects of exposure time for migratory fish

The ecological impact of parasite transmission from fish farms is probably mediated by the migration of wild fishes, which determines the period of exposure to parasites. For Pacific salmon and the parasitic sea louse, Lepeophtheirus salmonis, analysis of the exposure period may resolve conflicting observations of epizootic mortality in field studies and parasite rejection in experiments. This is because exposure periods can differ by 2–3 orders of magnitude, ranging from months in the field to hours in experiments. We developed a mathematical model of salmon–louse population dynamics, parametrized by a study that monitored naturally infected juvenile salmon held in ocean enclosures. Analysis of replicated trials indicates that lice suffer high mortality, particularly during pre-adult stages. The model suggests louse populations rapidly decline following brief exposure of juvenile salmon, similar to laboratory study designs and data. However, when the exposure period lasts for several weeks, as occurs when juvenile salmon migrate past salmon farms, the model predicts that lice accumulate to abundances that can elevate salmon mortality and depress salmon populations. The duration of parasite exposure is probably critical to salmon–louse population dynamics, and should therefore be accommodated in coastal planning and management where fish farms are situated on wild fish migration routes.     

Migration speeds and orientation of Atlantic salmon and sea trout post-smolts in a Norwegian fjord system

We recorded the observed and actual swimming speeds of Atlantic salmon and sea trout post-smolts in a Norwegian fjord system, and initiated studies on the orientation mechanisms of the post-smolts. We tracked Atlantic salmon and sea trout with acoustic transmitters for up to 14 h after release. The actual swimming speed and direction of a fish relative to the ground is the vector sum of the observed movements of the fish and the movements of the water. We determined actual swimming speeds and directions of the post-smolts, which reflect their real swimming capacities and orientation, by corrections for the speed and direction of the water current. The post-smolts were actively swimming. The observed direction of movement was dependent on the actual movement of the fish and not the water current. Water currents were not systematically used as an orientation cue either in Atlantic salmon or sea trout, as the actual movements were random compared to the direction of the water current. The actual movement of sea trout were in all compass directions, with no systematic pattern. The Atlantic salmon also moved in all compass directions, but with the lowest frequency of actual movement towards the fjord.     

Changes in Atlantic salmon (Salmo salar) epidermal mucus protein composition profiles following infection with sea lice (Lepeophtheirus salmonis)

The mucus protein profile of Atlantic salmon (Salmo salar) and changes due to infection with sea lice (Lepeophtheirus salmonis) were examined. Two-dimensional gel electrophoresis was performed on salmon skin mucus and comparisons between control and infected fish mucus were made. LC MS/MS identified intracellular proteins, calmodulin, actin, and hemopexin and plasma proteins, such as apolipoproteins, lectin, plasminogen and transferrin. Plasma proteins in the mucus may result from either direct expression by epidermal cells, leakage of plasma or via a secondary circulation system. Therefore, RT-PCR was used to measure mRNA of transferrin and lectin in Atlantic salmon skin. Transferrin expression was observed suggesting direct expression by the epidermis. Lectin expression was not detected suggesting another mechanism of entry into mucus, either leakage from plasma or secondary circulation. The lack of observable albumin on 2D gels, suggests that mucus lectin may arise from the secondary circulation route. Interestingly, β-actin was a significant component of Atlantic salmon mucus. Cleaved actin and transferrin fragments were observed and positively correlated with sea lice infection suggestive of proteolytic activity. Increased levels of cleaved transferrin during sea lice infection may activate the nitrous oxide response of salmon macrophages, as part of the fish's immune response to sea lice infection.     

Akirins in sea lice: First steps towards a deeper understanding

Sea lice (Copepoda, Caligidae) are the most widely distributed marine pathogens in the salmon industry. Vaccination could be an environmentally friendly alternative for sea lice control; however, research on the development of such vaccines is still at an early stage of development. Recent results have suggested that subolesin/akirin/my32 are good candidate antigens for the control of arthropod infestations, including sea lice, but background knowledge about these genes in crustaceans is limited. Herein, we characterize the my32 gene/protein from two important sea lice species, Caligus rogercresseyi and Lepeophtheirus salmonis, based on cDNA sequence isolation, phylogenetic relationships, three dimensional structure prediction and expression analysis. The results show that these genes/proteins have the main characteristics of akirins from invertebrates. In addition, immunization with purified recombinant my32 from L. salmonis elicited a specific antibody response in mice and fish. These results provide an improvement to our current knowledge about my32 proteins and their potential use as vaccine candidates against sea lice in fish.     

Fragmented mitochondrial genomes are present in both major clades of the blood-sucking lice (suborder Anoplura): evidence from two Hoplopleura rodent lice (family Hoplopleuridae)

Background

The suborder Anoplura contains 540 species of blood-sucking lice that parasitize over 840 species of eutherian mammals. Fragmented mitochondrial (mt) genomes have been found in the lice of humans, pigs, horses and rats from four families: Pediculidae, Pthiridae, Haematopinidae and Polyplacidae. These lice, eight species in total, are from the same major clade of the Anoplura. The mt genomes of these lice consist of 9–20 minichromosomes; each minichromosome is 1.5–4 kb in size and has 1–8 genes. To understand mt genome fragmentation in the other major clade of the Anoplura, we sequenced the mt genomes of two species of rodent lice in the genus Hoplopleura (family Hoplopleuridae).

Results

We identified 28 mt genes on 10 minichromosomes in the mouse louse, Ho. akanezumi; each minichromosome is 1.7–2.7 kb long and has 1–6 genes. We identified 34 mt genes on 11 minichromosomes in the rat louse, Ho. kitti; each minichromosome is 1.8–2.8 kb long and has 1–5 genes. Ho. akanezumi also has a chimeric minichromosome with parts of two rRNA genes and a full-length tRNA gene for tyrosine. These two rodent lice share the same pattern for the distribution of all of the protein-coding and rRNA genes but differ in tRNA gene content and gene arrangement in four minichromosomes. Like the four genera of blood-sucking lice that have been investigated in previous studies, the Hoplopleura species have four minichromosomes that are only found in this genus.

Conclusions

Our results indicate that fragmented mt genomes were present in the most recent common ancestor of the two major clades of the blood-sucking lice, which lived ~75 million years ago. Intra-genus variation in the pattern of mt genome fragmentation is common in the blood-sucking lice (suborder Anoplura) and genus-specific minichromosomes are potential synapomorphies. Future studies should expand into more species, genera and families of blood-sucking lice to explore further the phylogenetic utility of the novel features associated with fragmented mt genomes.

Electronic supplementary material

The online version of this article (doi:10.1186/1471-2164-15-751) contains supplementary material, which is available to authorized users.     

Stochastic multitype epidemics in a community of households: estimation and form of optimal vaccination schemes

This paper treats a stochastic model for an SIR (susceptible-->infective-->removed) multitype household epidemic. The community is assumed to be closed, individuals are of different types and each individual belongs to a household. Previously obtained probabilistic and inferential results for the model are used to derive the optimal vaccination scheme. By this is meant the scheme that vaccinates the fewest among all vaccination schemes that reduce the threshold parameter below 1. This is done for the situation where all model parameters are known and also for the case where parameters are estimated from an outbreak in the community prior to vaccination. It is shown that the algorithm which chooses vaccines sequentially, at each step selecting the individual which reduces the threshold parameter the most, is not in general an optimal scheme. As a consequence, explicit characterisation of the optimal scheme is only possible in certain special cases. Two different types of vaccine responses, leaky and all-or-nothing, are considered and compared for the problems mentioned above. The methods are illustrated with some numerical examples.     

Salmon lice, Lepeophtheirus salmonis, infestation as a causal agent of premature return to rivers and estuaries by sea trout, Salmo trutta, juveniles

A field experiment conducted in the River Lønningdalselven in spring 1992 supports the hypothesis that salmon lice, Lepeophtheirus salmonis, infestations may cause premature return of sea trout, Salmo trutta, juveniles, either to estuaries or to rivers. When lice infested (exposed) and uninfested (control) sea trout juveniles (post smolts) were released simultaneously into the sea, exposed fish returned to the estuarine area earlier compared with controls. Within the following two days, exposed sea trout migrated further into freshwater. At that time they were infested with a median of 62.5 lice, dominated by chalimus larvae and late juveniles. Exposed sea trout suffered from an osmoregulatory failure in sea water and this is considered one reason for infested fish returning to brackish water. While only a few control fish returned to the estuary on the day of release, some more returned to freshwater the following four days. During this time they had become heavily infested with copepodids, and carried a median of 150.0 lice. It is suggested that physiological stress and high infection pressure in the sea results in sea trout juveniles returning to estuaries and freshwater.     

Speed of action and in vitro efficacy of spinosad against sheep body lice, Bovicola ovis (Schrank) (Phthiraptera: Trichodectidae), resistant to pyrethroid, organophosphate or insect growth regulator insecticides

Abstract  Results of laboratory bioassays indicated that spinosad was equally effective against sheep lice populations that were susceptible to insecticides or resistant to pyrethroid, organophosphorus or insect growth regulator (IGR) insecticides. Spinosad had similar toxicity against susceptible strains of lice to that previously reported for diazinon, but lower toxicity than cypermethrin. Lethal concentrations of spinosad and diazinon caused knock down of lice within 6 h of exposure and death within 24 h. Prior to the current phasing out of diazinon as a sheep dip, most wool producers, needing to control pyrethroid- or IGR-resistant lice infestations in short-wool, would have chosen to use diazinon. Our results suggest that spinosad is an effective alternative for treatment of lice resistant to other chemical groups.     

The critical-period concept for juvenile survival and its relevance for population regulation in young sea trout, Salmo trutta

An example of density-dependent regulation is provided by a long-term investigation (1966-present) of a population of migratory trout (estuarine and sea trout), Salmo trutta L., in a Lake District stream. Evidence for the concept of a critical period for the survival of young fish is briefly reviewed and found to be rather equivocal. The concept is, however, relevant to the trout population. Loss rates were high before but low after a critical survival time ( t_c days after fry emergence) that varied between year-classes (range 33-70 days) and was inversely density-dependent on egg density. Survivor density and loss rates were strongly density-dependent on egg density before t _c, but proportionate survival with stable loss-rates occurred after t _c. Some trout established feeding territories soon after emergence and the number of fish without territories decreased from a high initial value to a negligible value at t _c. Fish size at t_c was not constant but increased as t _c increased. The range of t _c for the different year-classes was similar to that for survival times of unfed fry in the laboratory. A new stock-recruitment model, incorporating t _c, has been developed for the trout population and shown to be related to the model (Ricker curve) used in the long-term study. The critical time can also be regarded as the critical age for survival in young trout; this concept may be relevant to other fish species.     

Feedbacks, thresholds and synergies in global change: population as a dynamic factor

The role of feedbacks, thresholds, and synergies in environmental science, and their implications for environmental degradation under a growing human population, are reviewed. A detailed analysis of the impacts of climate change on water resources is used to elucidate mechanisms by which nonlinearities arise in environmental science. Additional examples are drawn from analysis of soil degradation and non-climate related degradation of water resources. The often-assumed notion that impacts will grow in proportion to population size is shown to be overly optimistic. In particular, feedbacks, thresholds, and synergies among multiple threats, tend to amplify risk and cause environmental impacts to grow considerably faster than linearly in population size, even when the per-capita living standard and the technological systems deployed to achieve that living standard are assumed to remain constant.     

QTL for body weight,morphometric traits and stress response in European sea bass Dicentrarchus labrax

Natural mating and mass spawning in the European sea bass (Dicentrarchus labrax L., Moronidae, Teleostei) complicate genetic studies and the implementation of selective breeding schemes. We utilized a two‐step experimental design for detecting QTL in mass‐spawning species: 2122 offspring from natural mating between 57 parents (22 males, 34 females and one missing) phenotyped for body weight, eight morphometric traits and cortisol levels, had been previously assigned to parents based on genotypes of 31 DNA microsatellite markers. Five large full‐sib families (five sires and two dams) were selected from the offspring (570 animals), which were genotyped with 67 additional markers. A new genetic map was compiled, specific to our population, but based on the previously published map. QTL mapping was performed with two methods: half‐sib regression analysis (paternal and maternal) and variance component analysis accounting for all family relationships. Two significant QTL were found for body weight on linkage group 4 and 6, six significant QTL for morphometric traits on linkage groups 1B, 4, 6, 7, 15 and 23 and three suggestive QTL for stress response on linkage groups 3, 14 and 23. The QTL explained between 8% and 38% of phenotypic variance. The results are the first step towards identifying genes involved in economically important traits like body weight and stress response in European sea bass.     

Islands in the sea: extreme female natal site fidelity in the Australian sea lion, Neophoca cinerea

Pinnipeds (seals, fur seals, sea lions and walrus) form large breeding aggregations with females often remaining faithful to a natal site or area. In these cases, females are philopatric to regional areas on broad geographical scales of hundreds to thousands of kilometers. An investigation of variation in a control region sequence of mtDNA in the Australian sea lion (Neophoca cinerea) has shown a case of extreme female natal site fidelity that has resulted in almost fixed population differentiation across its range (PhiST=0.93). This high level of population subdivision over short geographical distances (approx. 60 km) is unparalleled in any social marine mammal and reflects the unique life-history traits of this rare species. The high level of population subdivision and exclusive female natal site fidelity has important ramifications for conservation management, and poses many interesting questions of both academic and applied interest.     

How sea lice from salmon farms may cause wild salmonid declines in Europe and North America and be a threat to fishes elsewhere

Fishes farmed in sea pens may become infested by parasites from wild fishes and in turn become point sources for parasites. Sea lice, copepods of the family Caligidae, are the best-studied example of this risk. Sea lice are the most significant parasitic pathogen in salmon farming in Europe and the Americas, are estimated to cost the world industry €300 million a year and may also be pathogenic to wild fishes under natural conditions.Epizootics, characteristically dominated by juvenile (copepodite and chalimus) stages, have repeatedly occurred on juvenile wild salmonids in areas where farms have sea lice infestations, but have not been recorded elsewhere. This paper synthesizes the literature, including modelling studies, to provide an understanding of how one species, the salmon louse, Lepeophtheirus salmonis, can infest wild salmonids from farm sources. Three-dimensional hydrographic models predicted the distribution of the planktonic salmon lice larvae best when they accounted for wind-driven surface currents and larval behaviour. Caligus species can also cause problems on farms and transfer from farms to wild fishes, and this genus is cosmopolitan. Sea lice thus threaten finfish farming worldwide, but with the possible exception of L. salmonis, their host relationships and transmission adaptations are unknown. The increasing evidence that lice from farms can be a significant cause of mortality on nearby wild fish populations provides an additional challenge to controlling lice on the farms and also raises conservation, economic and political issues about how to balance aquaculture and fisheries resource management.     

Novel procedures for collection of sea urchin egg cortical granule exudate: Partial characterization and evidence for postsecretion processing

We have developed two procedures to collect total cortical granule exudate in a soluble form from eggs of the sea urchin Strongylocentrotus purpuratus. Egg suspensions were either treated with dithiothreitol to disrupt the vitelline envelope or divalent cations were removed postinsemination to prevent the normal vitelline-to-fertilization envelope transition. Rapid acidification of the insemination mixture (dithiothreitol-treated eggs) to pH 6.0 prevented precipitation of the paracrystalline protein fraction described by Bryan [1970a]. Exudate was partitioned into three fractions. The pH 8.0-insoluble fraction appeared to be identical to the paracrystalline protein fraction. The pH 8.0-soluble fraction was separated into pH 4.0-soluble and-insoluble fractions. Analysis for peroxidase and protease activities showed that peroxidase activity was localized in all three fractions whereas protease activity was restricted to the pH 4.0 insoluble fraction as reported [Carroll and Epel, 1975]. A minimum of six major proteins were detected on native polyacrylamide gels of total exudate. Under reducing and denaturing conditions, 12 polypeptides ranging from 19,000 to 165,000 in molecular weight were detected in total exudate; six polypeptides were recovered in the pH 8.0-insoluble fraction. To test the hypothesis that protease and peroxidase activities process cortical granule proteins after secretion, we inseminated eggs in solutions containing peroxidase and protease inhibitors. The paracrystalline protein fraction crystallized slowly from insemination mixtures containing both inhibitors compared to controls and there were dramatic differences in exudate electrophoretic patterns. We suggest that cortical granule protease and peroxidase activities process the exudate so that the paracrystalline protein fraction rapidly crystallizes during normal fertilization.