Movements and spatiotemporal distribution of escaped farmed and local wild Atlantic cod (Gadus morhua L.)

Commercial farming of Atlantic cod (Gadus morhua L.) is now being developed in several countries. The ecological consequences of cod culture are poorly understood, but recent research suggests that Atlantic cod are more prone to escape from net pens than Atlantic salmon. Here, we describe the movements and the spatiotemporal distribution of farmed cod after escape relative to wild cod, both during and outside the natural spawning season. The experimental design included simulating escape incidents of farmed cod tagged with acoustic transmitters and using an array of automatic listening stations to monitor their dispersal and distribution. For comparison, local wild cod were monitored using the same array of receivers. The farmed cod dispersed rapidly after a simulated escape, they randomly distributed over large areas and their distribution overlapped with local wild cod. Moreover, escaped farmed fish were found at local cod spawning areas during the spawning season. The study also indicated that the recapture rate of escaped farmed cod was high compared with that of escaped farmed salmon. Thus, while our results showed that there is a considerable potential for ecosystem effects caused by escaped farmed cod, mitigating actions such as an efficient recapture fishery for escapees may be possible.     

Impact of stocked Atlantic salmon (Salmo salar L.) on habitat use by the wild population

Laffaille P. Impact of stocked Atlantic salmon (Salmo salar L.) on habitat use by the wild population.
Ecology of Freshwater Fish 2011: 20: 67–73. © 2010 John Wiley & Sons A/S Abstract – We investigated the summer habitat occupied by populations of young‐of‐the‐year wild and stocked (farmed populations released into the native range) Atlantic salmon under allopatric and sympatric conditions. Under allopatric conditions, farmed and wild salmon occupied habitats with the same characteristics. The salmon preferentially occupied the riffle areas. However, under sympatric conditions, the fish occupied meso‐ and micro‐habitats with different characteristics. Wild salmon avoided habitats used by farmed salmon and preferred glide areas with considerable vegetation cover. This study suggests that differences in the pattern of habitats used by young Atlantic salmon were both size‐ and origin‐dependent and may result from intra‐species competition between farmed and wild populations. Given that stocking with farmed Atlantic salmon is carried out intensively to enhance recreational angling or to conserve salmon populations, this study warns that this can have a negative impact on the extant wild Atlantic salmon population.     

Experimental mycobacteriosis in Atlantic cod, Gadus morhua L

Piscine mycobacteriosis causes losses in a number of fish species both in the wild and in aquaculture worldwide. Mycobacterium salmoniphilum infections have on several occasions been reported in farmed Atlantic salmon, Salmo salar L. The present study tested and confirmed the susceptibility of Atlantic cod, Gadus morhua L., an important yet relatively novel aquaculture species, to infection with M. salmoniphilum. Atlantic cod injected intraperitoneally with a suspension of this bacterium were maintained together with cohabitant (COH) fish in a flow-through marine water system at 10-11 °C. The fish were supervised daily and samples taken at 2, 7, 14, 23, 34 and 53 weeks post-infection and examined pathologically, bacteriologically and using molecular biology. Injected mycobacteria were re-isolated in high concentrations from both injected and COH fish groups. Death attributable to mycobacterial infection was observed in both injected (47%) and COH (28%) fish groups. Extensive development of granuloma in visceral organs, mainly the mesenteries, spleen, kidney and liver (lesser extent) and at later stages of the infection in heart tissues and gills, was observed in both injected and COH fish. Granulomas underwent a temporal progression of distinct morphological stages, culminating in well-circumscribed lesions surrounded by normal or healing tissue. Acid-fast bacilli were detected in both granulomas and non-granulomatous tissues. This study confirms that Atlantic cod is highly susceptible to M. salmoniphilum infection and that this bacterial species may be a threat to cod both in the wild and in the aquaculture.     

Behavioural responses in wild cod (Gadus morhua L.) exposed to fish holding water

Local fishermen in several areas of Norway assert that salmon farms have caused the wild migrating cod to change their migratory behaviour, so that they no longer enter their natural spawning grounds in the fjords. If the asserted changes in behaviour of wild cod populations can be linked to establishment of salmon farms, water-soluble odorants are then possible candidates to explain such a connection. Chemical stimulants are important to the individual fish's conception of the surrounding environment. High density stocks of fish in a farm are expected to release large amounts of waterborne information. The present laboratory experiments were conducted to test behavioural responses in Atlantic cod exposed to water containing metabolites and waste from farmed salmon. The trials were conducted on single fish in a multiple chamber preference system. The results show that migrating wild Atlantic cod chose to spend more time in chambers without addition of water from the salmon tank, regardless of their maturation status, and even at very low concentrations (0.2%). The avoidance is probably due to presence of chemical compounds with olfactory properties from salmon, since anosmic cod did not elicit such response. Farmed cod, on the other hand, does not avoid water from the salmon tank, and stationary wild cod caught nearby a fish farm had a less pronounced response as compared to wild migrating cod. The response seen is not species specific, as wild migrating cod responded similar to water from a tank holding farmed cod as to water from salmon. These results do not preclude fishermen's observations that cod change their behaviour in areas with fish farming activity. Such a change in behaviour could be a response to water-soluble odorants, but needs to be validated and detailed in further laboratory experiments as well as in nature before any conclusions can be made.     

Calanus oil as a natural source for flesh pigmentation in Atlantic salmon (Salmo salar L.)

The present study was to understand how efficiently the astaxanthin in Calanus oil is utilized for flesh colouration in Atlantic salmon ( Salmo salar ). Postsmolts of the fish (309 g) were held at 7.9 °C and they were fed diets containing 20 or 60 mg astaxanthin per kilogram feed derived from a synthetic source or from Calanus oil for 181 days. Besides growth and feed intake assessments, at day 81 and 181, fish flesh were subjected to colour analysis and astaxanthin determination. Growth and feed performance did not vary between the groups. There were significant differences in the amount of astaxanthin in muscle between almost all groups both at day 81 ( P  < 0.05) and at day 181 ( P  < 0.001). However, a notable similarity between fish receiving 20 mg astaxanthin from the synthetic source and those receiving 60 mg astaxanthin from Calanus oil ( P  > 0.05) at day 181 indicated that comparable amounts were deposited only with the greater level of the natural source. Tristimuli colorimeter a* values support the analytical results at day 181. Although Calanus oil did serve as a natural dietary pigment source for farmed salmon, its inclusion level should provide more than 60 mg astaxanthin per kilogram feed to achieve colouration preferred by the market.     

Evaluation of sea lice abundance levels on farmed Atlantic salmon (Salmo salar L.) located in the Broughton Archipelago of British Columbia from 2003 to 2005

Salmon farming began in British Columbia (BC) in the 1970s and in 2006, aquaculture represented BC's largest agricultural export. Along with this growth in production has been a growth in controversy, including the concern that sea lice originating from Atlantic salmon farms negatively impact wild juvenile pink salmon in the Broughton Archipelago. To understand the dynamic interaction between wild and farmed fish, data for on‐farm abundance of sea lice are required. In this study, 33 000 Atlantic salmon from 20 active farms were examined over 3 years. Two species of lice were found: Lepeophtheirus salmonis and Caligus clemensi. Inter‐annual and seasonal variations in abundance levels occurred with lower levels of L. salmonis in 2003 compared with 2004 and 2005, while C. clemensi levels were highest in 2003. The abundance of L. salmonis was greater on older farmed fish. The findings are compared with European and eastern Canadian sea lice reports, and possible sources of sea lice on farmed salmon are discussed.     

Genetic comparison of experimental farmed strains and wild Icelandic populations of Atlantic cod (Gadus morhua L.)

Microsatellite DNA loci and the Pantophysin locus (Pan I) were used to investigate levels of genetic diversity within farmed strains of Atlantic cod Gadus morhua and to compare them with the wild source population. A total of 282 farmed samples originating from a spawning ground off the south-west coast of Iceland were sampled in the years 2002 and 2003, and 258 wild cod were collected at the same spawning ground in the same years. The farmed strains exhibited a lower mean number of alleles and allelic diversity than the wild samples at the microsatellite loci. Significant differences were observed between wild and farmed samples both in allele and genotype frequencies at the Pan I locus. We argue that the genetic divergence of wild and farmed samples of Atlantic cod may be due to a small number of effective founding breeders contributing to the genetic variation of the farmed strains, inducing a reduction in allelic diversity. We discuss the potential effect of breeding practices on the genetic diversity of Atlantic cod.     

Growth, feed conversion and chemical composition of Atlantic salmon (Salmo salar L.) and Atlantic halibut (Hippoglossus hippoglossus L.) fed diets supplemented with krill or amphipods

The effects of partial replacement of fish meal (FM) with meal made from northern krill (Thysanoessa inermis), Antarctic krill (Euphausia superba) or Arctic amphipod (Themsto libellula) as protein source in the diets for Atlantic salmon (Salmo salar L.) and Atlantic halibut (Hippoglossus hippoglossus L.) on growth, feed conversion, macro‐nutrient utilization, muscle chemical composition and fish welfare were studied. Six experimental diets were prepared using a low‐temperature FM diet as control. The other diets included northern krill where 20, 40 or 60% of the dietary FM protein was replaced with protein from northern krill, and two diets where the FM protein was replaced with protein from Antarctic krill or Arctic amphipod at 40% protein replacement level. All diets were iso‐nitrogenous and iso‐caloric. Atlantic salmon grew from 410 g to approximately 1500 g during the 160 day experiment, and Atlantic halibut grew from 345 g to 500–600 g during the 150 day experiment. Inclusion of krill in the diets enhanced specific growth rate in salmon, especially during the first 100 days (P < 0.01), and in a dose–response manner in halibut for over the 150 day feeding period (P < 0.05). Feed conversion ratio did not differ between dietary treatments, and no difference was found in dry matter digestibility, protein digestibility and fish muscle composition. Good growth rates, blood parameters within normal ranges and low mortalities in all experimental treatments indicted that fish health was not affected either Atlantic salmon or Atlantic halibut fed the various zooplankton diets.     

Content of synthetic astaxanthin in escaped farmed Atlantic salmon, Salmo salar L., ascending Norwegian rivers

Abstract  Isomeric ratios of astaxanthin in eggs and alevins of Atlantic salmon, Salmo salar L., have proven useful in identifying female spawners of farmed origin, but the method underestimates the proportion of fish of farmed origin. The rate of underestimation was studied by analysing astaxanthin content in tissue of 55 farmed Atlantic salmon ascending two Norwegian rivers in the autumn of 1991. The astaxanthin content fell into two distinct classes. Fifty-one per cent of the adult escaped salmon had isomeric ratios similar to salmon fed synthetic astaxanthin, whereas all the remaining fish had ratios similar to wild fish. Discriminant analysis classified 96.4% of the fish with known astaxanthin content into the correct astaxanthin class on basis of tail-fin erosion, length, weight and gill-cover damage. This discriminant function was used to estimate the astaxanthin classification of 1017 farmed salmon caught in nine rivers during 1989–1991. The classification success varied among years from 52 to 64%. Corresponding numbers for females and males were 45–48% and 54–70%, respectively. Thus, estimates of spawning rates of farmed female salmon via astaxanthin content in eggs or alevins from redds should be adjusted accordingly. The observed isomeric ratios of astaxanthin in the escaped farmed salmon and the relationship with morphology indicates that a significant proportion of the escapees ascending rivers have spent more than 1 year in the wild after escape.     

Incidence and timing of wild and escaped farmed Atlantic salmon (Salmo salar) in Norwegian rivers inferred from video surveillance monitoring

Run timing of escaped farmed Atlantic salmon Salmo salar vs. wild fish was compared by the use of video camera surveillance in 15 rivers over several years, covering 1600 km of the Norwegian coastline (from 58°N to 69°N). Annual runs of wild salmon varied among rivers from <200 fish to more than 10 000. During the surveillance period that for most rivers extended from late May to early October, larger‐sized salmon (fish ≥ 65 cm) generally entered the rivers earlier than small fish. The percentage of salmon identified as escaped farmed fish ranged from 0.1% to 17% across rivers with an average of 4.3%. Estimates of escapees are, however, assumed to represent minimum values because an unknown number of farmed fish passing the video cameras may have been misclassified as wild fish. By the use of a linear mixed model and generalised additive mixed models, it was found that the relationship between run timing and fish length differed significantly between farmed and wild salmon. While small‐sized farmed and wild fish (<65 cm) entered the river at about the same time, wild large salmon returned on average 1–2 weeks earlier than similarly sized escapees. The proportion of large‐sized farmed escapees also increased until late August and decreased thereafter. In contrast, there was a relatively constant and lower proportion of small‐sized escapees throughout the season. Within the surveillance period, there was no evidence of any exceptionally late runs of fish classified as escaped farmed salmon.     

Effect of Antarctic krillmeal on quality of farmed Atlantic cod (Gadus morhua L.)

Farmed Atlantic cod with a mean weight of 4.8 kg were maintained for 9 weeks in sea cages and fed diets where the dietary fishmeal component was substituted with increasing proportions (0%, 22%, 63% and 100%) of meal from Antarctic krill, Euphausia superba. Wild‐caught cod were included in the study as external control. At termination of feeding, all fish were slaughtered and muscle pH was immediately recorded. The fish were then stored on ice for three days and assessed for muscle pH and objective (skin and fillet colour, and fillet texture) and subjective (sensory evaluation) quality criteria. Replacement of fishmeal with krillmeal in the diets resulted in the skin colour above and below the lateral line to be more red than the control group without krillmeal substitutions, even though this difference was not significant, and with more yellow hue. Additions of krillmeal increased the muscle whiteness and yellow hue compared with the control group and wild fish. There was no difference in red hue between the groups. Muscle pH, texture or sensory attributes were unaffected by dietary inclusion level of krillmeal. Wild‐caught cod deviated in several aspects from the farmed cod. It is concluded that the replacement of fishmeal with Antarctic krillmeal in the diets two months before slaughter did not move the sensory attributes more towards wild fish.     

Anisakid larva in the viscera of a farmed Atlantic salmon (Salmo salar)

Parasitic nematodes of the family Anisakidae occur in the visceral cavity and surrounding tissues of many marine fish species at a prevalence as high as 100% in wild salmon samples. Human consumption of fish products containing these parasites can result in the zoonotic disease anisakiasis, and Anisakis simplex is most commonly associated with human disease. Previous studies of farmed salmon have found no anisakids in viscera or muscle, presumably because formulated feed production renders parasite larvae nonviable. However, among farmed Atlantic salmon (Salmo salar) examined by histopathology as part of a provincial government auditing program in British Columbia, Canada, 1 of 894 (0.11%) had an anisakid larva partly embedded in the wall of an intestinal cecum. Skeletal muscle is not examined as part of the government's program, but other studies have correlated anisakids in the viscera and muscle. Using anisakid prevalence in viscera as an estimate of its prevalence in muscle, the risk ratio of anisakid parasites in commercial product is 570 times less in farmed than in wild Atlantic salmon.     

Egg quality determinants in cod (Gadus morhua L.): egg performance and lipids in eggs from farmed and wild broodstock

Lipids and essential fatty acids, particularly the highly unsaturated fatty acids, 20:5n‐3 (eicosapentaenoic acid; EPA), 22:6n‐3 (docosahexaenoic acid; DHA) and 20:4n‐6 (arachidonic acid, AA) have been shown to be crucial determinants of marine fish reproduction directly affecting fecundity, egg quality, hatching success, larval malformation and pigmentation. In Atlantic cod (Gadus morhua L.) culture, eggs from farmed broodstock can have much lower fertilization and hatching rates than eggs from wild broodstock. The present study aimed to test the hypothesis that potential quality and performance differences between eggs from different cod broodstock would be reflected in differences in lipid and fatty acid composition. Thus eggs were obtained from three broodstock, farmed, wild/fed and wild/unfed, and lipid content, lipid class composition, fatty acid composition and pigment content were determined and related to performance parameters including fertilization rate, symmetry of cell division and survival to hatching. Eggs from farmed broodstock showed significantly lower fertilization rates, cell symmetry and survival to hatching rates than eggs from wild broodstock. There were no differences in total lipid content or the proportions of the major lipid classes between eggs from the different broodstock. However, eggs from farmed broodstock were characterized by having significantly lower levels of some quantitatively minor phospholipid classes, particularly phosphatidylinositol. There were no differences between eggs from farmed and wild broodstock in the proportions of saturated, monounsaturated and total polyunsaturated fatty acids. The DHA content was also similar. However, eggs from farmed broodstock had significantly lower levels of AA, and consequently significantly higher EPA/AA ratios than eggs from wild broodstock. Total pigment and astaxanthin levels were significantly higher in eggs from wild broodstock. Therefore, the levels of AA and phosphatidylinositol, the predominant AA‐containing lipid class, and egg pigment content were positively related to egg quality or performance parameters such as fertilization and hatching success rates, and cell symmetry.     

Energy and nutrient utilization of Atlantic cod, Atlantic salmon and rainbow trout fed diets differing in energy content

The growth and feed utilization of Atlantic cod (Gadus morhua) (437 g), Atlantic salmon (Salmo salar) (485 g) and rainbow trout (Oncorhynchus mykiss) (413 g) fed a diet (170 g kg⁻¹ fat, 600 g kg⁻¹ crude protein; LE) similar to that used in commercial cod production or one that was top dressed with additional fat (280 g kg⁻¹ fat, 530 g kg⁻¹ crude protein; HE), were compared in an 11‐week trial. In the cod, relative feed intake was 41–58% and thermal growth coefficient 63% of that in the salmonids, but the feed efficiency ratio (FER) was 38% better (P ≤ 0.05). In contrast to the cod where there was no effect of diet on feed intake, growth or FER, both the salmon and trout fed the HE diet had greater feed intake than those fed the LE diet, but the effect of this was only positive for growth in the salmon. The cod retained more of the digested nitrogen (44.9 ± 2.7%) than the salmon (39.4 ± 0.8%), and both of these species retained more than the trout (33.6 ± 1.1%) (P ≤ 0.05). The retention of digested energy was significantly higher in the salmon (52.2 ± 0.9%) than in the trout (44.8 ± 1.1%), with the cod (44.9 ± 4.9%) not different from either of the other species. There were no differences between the species in the retention of absorbed phosphorus (65.9 ± 3.6%). There were very few dietary effects on nutrient utilization in this trial and, for the cod, this indicates that higher energy diets may be feasible for use in production.     

Occurrence of Francisella piscicida in farmed and wild Atlantic cod, Gadus morhua L., in Norway

Francisellosis, caused by the bacterium Francisella piscicida , has become one of the most serious diseases in Atlantic cod production in Norway. The major aim of this study was to determine the distribution of F. piscicida in farmed and wild fish in areas with cod farming along the Norwegian coast, and its occurrence in cod from areas without cod farming. Two real-time PCR assays, targeting the 16S rRNA gene and the FopA gene of F. piscicida , were developed since sensitive and specific diagnostic tools are required for detecting asymptomatic carriers of the bacterium. A total of 422 wild cod from 13 sampling areas and 955 farmed cod from 10 areas along the coast of Norway were examined. Using the real-time polymerase chain reaction (PCR) assays, F. piscicida was detected in wild populations of cod from all counties examined south of Sogn og Fjordane in southern Norway (overall prevalence 13%, n  = 221). Wild cod north of Sogn og Fjordane were negative for the bacterium ( n  = 201). Farmed cod from most parts of Norway were F. piscicida positive. The apparent absence of the bacterium in wild populations of cod in the northern parts of Norway and its widespread occurrence in wild cod from southern parts of Norway is believed to relate to differences in seawater temperatures.     

Host tropism of infectious salmon anaemia virus in marine and freshwater fish species

The aquatic orthomyxovirus infectious salmon anaemia virus (ISAV) causes a severe disease in farmed Atlantic salmon, Salmo salar L. Although some ISA outbreaks are caused by horizontal transmission of virus between farms, the source and reservoir of the virus is largely unknown and a wild host has been hypothesized. Atlantic salmon are farmed in open net‐pens, allowing transmission of pathogens from wild fish and the surrounding environment to the farmed fish. In this study, a large number of fish species were investigated for ISAV host potential. For orthomyxoviruses, a specific receptor binding is the first requirement for infection; thus, the fish species were investigated for the presence of the ISAV receptor. The receptor was found to be widely distributed across the fish species. All salmonids expressed the receptor. However, only some of the cod‐like and perch‐like fish did, and all flat fish were negative. In the majority of the positive species, the receptor was found on endothelial cells and/or on red blood cells. The study forms a basis for further investigations and opens up the possibility for screening species to determine whether a wild host of ISAV exists.     

Maintenance ration, protein synthesis capacity, plasma insulin and growth of Atlantic salmon (Salmo salar L.) with genetically different trypsin isozymes

Growth was found to be associated with the changes of trypsin activity in the pyloric caecal tissues and the level of plasma insulin in Atlantic salmon (Salmo salar L.). A decrease in trypsin activity accompanied by an increase in plasma insulin was detected one month before an enhanced growth was observed. There were significant relationships between weight specific consumption rate, plasma insulin levels and fish growth. The correlation of weight specific consumption rate was higher with growth rate (R²=0.7, p<0.0001) than with plasma insulin concentration (R²=0.4, p<0.0001).When the comparison was made between Atlantic salmon carrying and lacking the trypsin variant TRP-2*92, the fish with the variant had lower maintenance ration (p<0.05), higher capacity for protein synthesis in the white muscle (p<0.02), and a greater ability to utilize the feed at a restricted ration than the fish without the variant. In Atlantic salmon lacking the variant, both plasma insulin concentrations and growth rates were significantly lower (p<0.05) in the fish fed 0.5% bw day^–1 than those fed 1% bw day^–1. Whilst the growth rates of TRP-2*92 salmon fed the different rations became similar one month after similar levels of plasma insulin were observed between them. The TRP-2*92 salmon may be defined as a high protein growth efficiency fish with low protein turnover rate.Genetic variation in trypsin isozyme pattern affects feed utilization, plasma insulin levels and growth in Atlantic salmon.     

Sarcoma of the swim bladder of Atlantic salmon (Salmo salar L.)

A neoplastic disease of the swim bladder of farmed Atlantic salmon (Salmo salar L.) was investigated. The tumour was classified as a leiomyosarcoma and had a detected prevalence of 4.6% of a population of 500 second-year sea fish.     

Piscine reovirus (PRV) in wild Atlantic salmon,Salmo salar L., and sea‐trout,Salmo trutta L., in Norway

This is the first comprehensive study on the occurrence and distribution of piscine reovirus (PRV) in Atlantic salmon, Salmo salar L., caught in Norwegian rivers. PRV is a newly discovered reovirus associated with heart and skeletal muscle inflammation (HSMI), a serious and commercially important disease affecting farmed Atlantic salmon in Norway. A cross‐sectional survey based on real‐time RT‐PCR screening of head kidney samples from wild, cultivated and escaped farmed Atlantic salmon caught from 2007 to 2009 in Norwegian rivers has been conducted. In addition, anadromous trout (sea‐trout), Salmo trutta L., caught from 2007 to 2010, and anadromous Arctic char, Salvelinus alpinus (L.), caught from 2007 to 2009, were tested. PRV was detected in Atlantic salmon from all counties included in the study and in 31 of 36 examined rivers. PRV was also detected in sea‐trout but not in anadromous Arctic char. In this study, the mean proportion of PRV positives was 13.4% in wild Atlantic salmon, 24.0% in salmon released for stock enhancement purposes and 55.2% in escaped farmed salmon. Histopathological examination of hearts from 21 PRV‐positive wild and one cultivated salmon (Ct values ranging from 17.0 to 39.8) revealed no HSMI‐related lesions. Thus, it seems that PRV is widespread in Atlantic salmon returning to Norwegian rivers, and that the virus can be present in high titres without causing lesions traditionally associated with HSMI.     

Prevalence of piscine orthoreovirus and salmonid alphavirus in sea‐caught returning adult Atlantic salmon (Salmo salar L.) in northern Norway

Heart and skeletal muscle inflammation (HSMI) caused by piscine orthoreovirus (PRV) and pancreas disease (PD) caused by salmonid alphavirus (SAV) are among the most prevalent viral diseases of Atlantic salmon farmed in Norway. There are limited data about the impact of disease in farmed salmon on wild salmon populations. Therefore, the prevalence of PRV and SAV in returning salmon caught in six sea sites was determined using real‐time RT‐PCR analyses. Of 419 salmon tested, 15.8% tested positive for PRV, while none were positive for SAV. However, scale reading revealed that 10% of the salmon had escaped from farms. The prevalence of PRV in wild salmon (8%) was significantly lower than in farm escapees (86%), and increased with fish length (proxy for age). Sequencing of the S1 gene of PRV from 39 infected fish revealed a mix of genotypes. The observed increase in PRV prevalence with fish age and the lack of phylogeographic structure of the virus could be explained by virus transmission in the feeding areas. Our results highlight the need for studies about the prevalence of PRV and other pathogens in Atlantic salmon in its oceanic phase.