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Effects of laboratory salmon louse infection on Arctic char osmoregulation, growth and survival.

ABSTRACT: High salmon lice (Lepeophtheirus salmonis) infestation levels resulting from intensive salmonid sea-cage aquaculture can threaten populations of wild salmonid hosts. This includes anadromous Arctic char (Salvelinus alpinus), which rely on short migrations into more productive seawater environments to build energy stores for maturation, spawning and over-wintering in freshwater. Elevated salmon lice burdens may limit the benefits of migration by constraining osmoregulation, growth, survival and reproduction. To test for these effects, we simulated anadromous migration in tanks by transferring individually tagged Arctic char smolts (n?=?352, averaging 133 g) to seawater where they were infected with salmon lice or left as uninfected controls for 1 month, and then transferring them back to freshwater for 2 months. After the seawater phase, infected post-smolts had a mean of 0.33 (range of 0.09-0.91) mobile lice g-1 fish weight. At this point, specific growth rates (SGRs) dropped in infected compared to control fish (0.1% vs. 1.6% day-1). Higher plasma Na+ and osmolality in infected fish also indicate osmoregulatory impairment. Throughout the study, mortality was 18.2% and 1.7% in infected and control groups, but sexual maturation was low and comparable between groups. Infection intensity correlated positively with mortality rate and plasma Cl-, and correlated negatively with SGR and condition factor (CF). CF dropped (?CF?0.09 lice g-1 fish weight, and intensities of >0.3 causing zero or negative SGRs and increased mortality were particularly concerning. If infection intensities reach these levels in the wild, char could be impacted by growth restrictions and increased mortality rates, which potentially cause shorter migration durations, lowered reproductive success and possibly also selection against anadromy. This study provides vital information for conservation practitioners wanting to understand the physiologically derived burden salmon lice can have on Arctic char populations, and can be used to define thresholds in the monitoring and conservation of Arctic char populations affected by aquaculture-driven salmon lice infestations.

SUBMITTER: Fjelldal PG

PROVIDER: S-EPMC6839430 | biostudies-literature | 2019

REPOSITORIES: biostudies-literature

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Effects of laboratory salmon louse infection on Arctic char osmoregulation, growth and survival.

Fjelldal P G PG Hansen T J TJ Karlsen Ø Ø Wright D W DW

Conservation physiology 20191107 1

High salmon lice (<i>Lepeophtheirus salmonis</i>) infestation levels resulting from intensive salmonid sea-cage aquaculture can threaten populations of wild salmonid hosts. This includes anadromous Arctic char (<i>Salvelinus alpinus</i>), which rely on short migrations into more productive seawater environments to build energy stores for maturation, spawning and over-wintering in freshwater. Elevated salmon lice burdens may limit the benefits of migration by constraining osmoregulation, growth, ...[more]

PMID: 31723431

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Project description:Northern populations of Arctic char (Salvelinus alpinus) can be anadromous, migrating annually from the ocean to freshwater lakes and rivers in order to escape sub-zero temperatures. Such seasonal behavior demands that these fish and their associated microbiomes adapt to changes in salinity, temperature, and other environmental challenges. We characterized the microbial community composition of anadromous S. alpinus, netted by Inuit fishermen at freshwater and seawater fishing sites in the high Arctic, both under ice and in open water. Bacterial profiles were generated by DNA extraction and high-throughput sequencing of PCR-amplified 16S ribosomal RNA genes. Results showed that microbial communities on the skin and intestine of Arctic char were statistically different when sampled from freshwater or saline water sites. This association was tested using hierarchical Ward's linkage clustering, showing eight distinct clusters in each of the skin and intestinal microbiomes, with the clusters reflecting sampling location between fresh and saline environments, confirming a salinity-linked turnover. This analysis also provided evidence for a core composition of skin and intestinal bacteria, with the phyla Proteobacteria, Firmicutes, and Cyanobacteria presenting as major phyla within the skin-associated microbiomes. The intestine-associated microbiome was characterized by unidentified genera from families Fusobacteriaceae, Comamonadaceae, Pseudomonadaceae, and Vibrionaceae. The salinity-linked turnover was further tested through ordinations that showed samples grouping based on environment for both skin- and intestine-associated microbiomes. This finding implies that core microbiomes between fresh and saline conditions could be used to assist in regulating optimal fish health in aquaculture practices. Furthermore, identified taxa from known psychrophiles and with nitrogen cycling properties suggest that there is additional potential for biotechnological applications for fish farm and waste management practices.

Project description:BACKGROUND: The salmon louse (SL) is an ectoparasitic caligid crustacean infecting salmonid fishes in the marine environment. SL represents one of the major challenges for farming of salmonids, and veterinary intervention is necessary to combat infection. This study addressed gene expression responses of Atlantic salmon infected with SL, which may account for its high susceptibility. RESULTS: The effects of SL infection on gene expression in Atlantic salmon were studied throughout the infection period from copepodids at 3 days post infection (dpi) to adult lice (33 dpi). Gene expression was analyzed at three developmental stages in damaged and intact skin, spleen, head kidney and liver, using real-time qPCR and a salmonid cDNA microarray (SFA2). Rapid detection of parasites was indicated by the up-regulation of immunoglobulins in the spleen and head kidney and IL-1 receptor type 1, CD4, beta-2-microglobulin, IL-12beta, CD8alpha and arginase 1 in the intact skin of infected fish. Most immune responses decreased at 22 dpi, however, a second activation was observed at 33 dpi. The observed pattern of gene expression in damaged skin suggested the development of inflammation with signs of Th2-like responses. Involvement of T cells in responses to SL was witnessed with up-regulation of CD4, CD8alpha and programmed death ligand 1. Signs of hyporesponsive immune cells were seen. Cellular stress was prevalent in damaged skin as seen by highly significant up-regulation of heat shock proteins, other chaperones and mitochondrial proteins. Induction of the major components of extracellular matrix, TGF-beta and IL-10 was observed only at the adult stage of SL. Taken together with up-regulation of matrix metalloproteinases (MMP), this classifies the wounds afflicted by SL as chronic. Overall, the gene expression changes suggest a combination of chronic stress, impaired healing and immunomodulation. Steady increase of MMP expression in all tissues except liver was a remarkable feature of SL infected fish. CONCLUSION: SL infection in Atlantic salmon is associated with a rapid induction of mixed inflammatory responses, followed by a period of hyporesponsiveness and delayed healing of injuries. Persistent infection may lead to compromised host immunity and tissue self-destruction.

Project description:Lepeophtheirus salmonis (sea lice) and bacterial co-infection threatens wild and farmed Atlantic salmon performance and welfare. In the present study, pre-adult L. salmonis-infected and non-infected salmon were intraperitoneally injected with either formalin-killed Aeromonas salmonicida bacterin (ASAL) or phosphate-buffered saline (PBS). Dorsal skin samples from each injection/infection group (PBS/no lice, PBS/lice, ASAL/no lice, and ASAL/lice) were collected at 24 h post-injection and used for transcriptome profiling using a 44K salmonid microarray platform. Microarray results showed no clear inflammation gene expression signatures and revealed extensive gene repression effects by pre-adult lice (2,189 down and 345 up-regulated probes) in the PBS-injected salmon (PBS/lice vs. PBS/no lice), which involved basic cellular (e.g., RNA and protein metabolism) processes. Lice repressive effects were not observed within the group of ASAL-injected salmon (ASAL/lice vs. ASAL/no lice); on the contrary, the observed skin transcriptome changes -albeit of lesser magnitude (82 up and 1 down-regulated probes)- suggested the activation in key immune and wound healing processes (e.g., neutrophil degranulation, keratinocyte differentiation). The molecular skin response to ASAL was more intense in the lice-infected (ASAL/lice vs. PBS/lice; 272 up and 11 down-regulated probes) than in the non-infected fish (ASAL/no lice vs. PBS/no lice; 27 up-regulated probes). Regardless of lice infection, the skin's response to ASAL was characterized by the putative activation of both antibacterial and wound healing pathways. The transcriptomic changes prompted by ASAL+lice co-stimulation (ASAL/lice vs. PBS/no lice; 1878 up and 3120 down-regulated probes) confirmed partial mitigation of lice repressive effects on fundamental cellular processes and the activation of pathways involved in innate (e.g., neutrophil degranulation) and adaptive immunity (e.g., antibody formation), as well as endothelial cell migration. The qPCR analyses evidenced immune-relevant genes co-stimulated by ASAL and lice in an additive (e.g., mbl2b, bcl6) and synergistic (e.g., hampa, il4r) manner. These results provided insight on the physiological response of the skin of L. salmonis-infected salmon 24 h after ASAL stimulation, which revealed immunostimulatory properties by the bacterin with potential applications in anti-lice treatments for aquaculture. As a simulated co-infection model, the present study also serves as a source of candidate gene biomarkers for sea lice and bacterial co-infection.

Dataset Information

Effects of laboratory salmon louse infection on Arctic char osmoregulation, growth and survival.

Publications

Effects of laboratory salmon louse infection on Arctic char osmoregulation, growth and survival.

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