The importance of porosity and thickness in terms of oxygen supply to embryonic salmonids is analogous to the egg membranes of oviparous organisms. Indeed, studies have shown that other species demonstrate inter-population variability of egg architecture in response to oxygen availability [ 16 ]. Thus, we hypothesize egg architecture will vary among Atlantic salmon populations according to the frequency and degree of oxygen stress that they face during incubation as part of an adaptive compensatory response. Population variation in the response of Atlantic salmon eggs to hypoxia has been observed and attributed to differences in the physiological response of the embryo [ 17 ].
However, the authors did not consider inter-population differences in oxygen uptake rates, which could be driven by structural variance of the egg membrane. If structural differences among populations are present and affect tolerance to oxygen stress, then there would be important implications for stock enhancement programmes that rear eggs of wild fish in a hatchery environment. In addition, deterministic models such as the mass transfer theory [ 7 ] and the sediment intrusion and dissolved oxygen transport model SIDO [ 18 ] that predict ova survival based on incubation conditions assume uniform membrane permeability across populations.
If structural differences exist, the application of such models to a range of populations may need to be re-visited, as they can play an important role in guiding catchment and hydrological management practices [ 19 , 20 ]. This study aimed to determine whether Atlantic salmon populations exhibit distinct egg architecture and whether egg structure varies alongside embryonic sensitivity to hypoxia.
These aims were achieved through three specific objectives: 1 determine inter-population variability of egg architecture of five Atlantic salmon populations, with a particular focus on permeability to oxygen by using scanning electron microscopy to measure key structural features; 2 determine the effect of differences in egg architecture on estimated in-redd conditions required to support ova respiration by applying the measurements obtained from objective 1 to the mass transfer model; and 3 determine whether there was a difference in egg architecture between eggs of a single population that survived extended periods of hypoxia, and those that died.
Four of these River Dochart, River Tilt, River South Tyne, River North Tyne were taken from conservation hatcheries where reproductively mature wild caught Atlantic salmon were captured from their natal streams during peak spawning season. The fifth population was sourced from a commercial hatchery that supports the aquaculture industry. Eggs of the farmed population were originally sourced from adults of Norwegian origin, but have been bred entirely in captivity for more than 10 generations.
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Figure 1. Map of United Kingdom with rivers hosting Atlantic salmon shown in blue. The locations of the egg sources used in this study are labelled and displayed in heavy red. Following extraction, eggs and milt were placed in well-oxygenated plastic bags eggs submerged in coelomic fluid and transported to the University of Southampton in chilled polystyrene containers where they were fertilized within 24 h of the gamete extraction procedure.
Details of the rivers and hatcheries from which eggs were sourced for the current investigation in order to meet all research objectives. The date of fertilization indicates the time at which incubation of each population began in the University of Southampton research facility. Note: Unless otherwise stated, information is based on the hatchery from which eggs were sourced.
Gametes were crossed using a full-factorial breeding design [ 21 ] for each population wherein milt from each male was paired with eggs from each female, resulting in 40 unique families per population. To create each family, the eggs of each female were divided into four groups of Each group of 30 eggs was combined with 0. Fertilized eggs were subsequently washed and allowed to harden for 1 h using water from the experimental facility [ 22 ]. While the process of combining eggs from each maternal fish into a single group per population was necessary due to space constraints, the process had the potential to give rise to pseudo-replication whereby individual parent fish could be over-represented in the data.
This risk was limited by ensuring eggs were well-mixed within the egg chamber and a high number of replicates per population 36 were sampled to maximize the spread of data sources. Before entering the egg chambers, the water was exposed to chemical, biological and physical treatment to ensure it was suitable for rearing of Atlantic salmon ova [ 24 ]. Ambient temperature plays a key role in determining developmental rate of incubating salmonids [ 10 ]. The optodes recorded temperature at 1 min intervals and the 10 min mean was stored on the data logger.
The above calculation was conducted every 24 h and a cumulative value calculated to provide the developmental state of embryos on a daily basis.
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Subsequently, eggs from each population were sampled at DDs. Sampling at the same developmental state for each population ensured that possible changes in structure during development [ 21 ] did not unequally affect samples. The mass transfer theory [ 7 ] enables theoretical estimation of the oxygen supply requirements of incubating ova according to key variables of oxygen concentration, water velocity past the egg surface and egg architecture. Figure 2. An area where the film is missing, revealing the membrane itself can be observed in the centre of the image. Previous application of the mass transfer model relied on porosity and thickness estimates of Chinook salmon Oncorhynchus tshawytscha and brown trout Salmo trutta eggs presented in [ 7 ] and [ 25 ] respectively.
These eggs were subsequently split into two treatment groups control and hypoxic of The control treatment received oxygen-saturated mean: Oxygen levels were controlled through a process of nitrogen sparging following methods described elsewhere [ 24 ]. Only farmed eggs were studied to ensure possible inter-population differences in factors that influence tolerance to oxygen stress [ 27 ] were excluded. Space constraints meant that it was unfortunately not possible to replicate this investigation with all populations. Egg chambers were checked every 24 h and dead eggs counted and removed.
When the number of dead eggs in the hypoxic treatment was greater than the control, enough live eggs of the control were extracted to ensure the daily number of eggs removed from each treatment was the same. This ensured that stocking density did not affect treatments unequally. To determine whether membrane structure changed when eggs died, a separate group of farmed eggs were incubated under control conditions.
This showed membrane structure does not change within 24 h of egg mortality, so validated the methodology.
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To account for measurement error, eggs were re-measured and were within less than 1. Diameter values were used to calculate the surface area of the egg sphere. Egg membranes were then prepared for scanning electron microscope SEM observation using methods described elsewhere [ 13 ], before they were dehydrated in a Balzers Critical Point Drier.
These were affixed to a 12 mm carbon tab on an aluminium stub and sputter coated with gold for 30 s, before inspection under the SEM Jeol JCM To determine differences in membrane thickness, thickness quotient, porosity and permeability to oxygen among populations, one-way ANOVA tests were performed. Differences in all structural features were compared among the control, dead and live treatments at each mortality threshold using one-way ANOVA tests.
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When differences among populations or treatments were found, Tukey's post hoc tests were performed to see where these differences occurred. In all instances, membrane thickness quotient and porosity data were logit transformed prior to ANOVA analysis. Statistical analysis was conducted using SPSS River Tilt eggs had a smaller diameter 5.
Figure 3. Recorded features of eggs examined under electron microscope relevant to objectives 1 and 2. Data on the left of the solid line refer to objective 1 and enable comparison of egg architecture among populations tested. Data on the right of the solid line refer to objective 2 and enable comparison of egg architecture among control eggs and those that died or survived when exposed to hypoxia. Dashed lines separate data for each mortality threshold.
Error bars indicate standard deviation. The relative requirements of the River Dochart and River Tilt eggs varied depending on whether oxygen or intragravel velocity was limiting. At high intragravel velocity and low oxygen content, River Dochart eggs had higher requirements than the River Tilt eggs. However, the reverse is true at low intragravel velocity but high oxygen concentrations. Figure 4. Data calculated using the mass transfer model equation 2.
Note that lines do not represent mortality thresholds, but the concentration at which sublethal reductions of post-hatch fitness could be expected. Headshot and Commercial Photographer based in Calgary, Alberta. We work on-location or in-studio and we provide photography services to our clients when, where, and how they need it.
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For the past three years, First Nations communities and their supporters across British Columbia have worked to educate residents of the area on the challenges of restoring wild salmon in the Fraser Basin and Salish Sea corridor. The group has traveled caravan-style along the length of the river, performing ancient song, dance and salmon ceremonies.
Audrey Siegl looks out across the water in on the shores of Crab Park, Vancouver, commercial docks at her back.
On the Fraser River, faltering salmon populations have impacted tribes and urban economies.
Siegl joined the caravan as a member of the Musqueam First Nation. But now, its salmon are in decline. While salmon once comprised 60 percent of fishery profits, they now account for only 20 percent of the fish caught and sold from the river. Photographer Michael O. Snyder and journalist Courtney Sexton traveled north in to capture the stories of interwoven stakeholders in the health of the Fraser River and its fish.