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- Oxford University Press
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- © The Author(s) 2023. Published by Oxford University Press and the Society for Experimental Biology.
- eISSN
- 2051-1434
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- 10.1093/conphys/coac085
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Abstract
Volume 11 • 2023 10.1093/conphys/coac085 Research article Partial-year continuous light treatment reduces precocious maturation in age 1+ hatchery–reared male spring Chinook Salmon (Oncorhynchus tshawytscha) 1, 1 2 2 1,2 Nick F Hoffman , Lea R Medeiros , Neil D Graham , Hayley M Nuetzel , Andrew L Pierce and James J Nagler Department of Biological Sciences, University of Idaho, 875 Perimeter Dr., Moscow, ID 83844, USA Columbia River Inter-Tribal Fish Commission, Fishery Science Department, 700 NE Multnomah St., Suite 1200, Portland, OR 97232, USA *Corresponding author: Department of Biological Sciences, University of Idaho, 875 Perimeter Dr. MS 3051, Moscow, ID 83844-3051, USA. Telephone: (208) 749-7522. Email: nhoffman@uidaho.edu .......................................................................................................................................................... Hatchery programs designed to conserve and increase the abundance of natural populations of spring Chinook Salmon Oncorhynchus tshawytscha have reported high proportions of males precociously maturing at age 2, called minijacks. High proportions of minijacks detract from hatchery supplementation, conservation and production goals. This study tested the effects of rearing juvenile Chinook Salmon under continuous light (LL) on minijack maturation in two trials. The controls were maintained on a simulated natural photoperiod for both trials. For trial 1, LL treatment began on the summer solstice 2019 or the autumn equinox 2019 and ended in late March 2020 (LL-Jun-Apr and LL-Sep-Apr, respectively). A significant reduction in the mean percent of minijacks (%MJ) was observed versus control (28.8%MJ) in both LL-Jun-Apr (5.4%MJ) and LL-Sep-Apr (9.3%MJ). Trial 2 was designed to evaluate whether stopping LL treatment sooner was still effective at reducing maturation proportions relative to controls. LL treatments began on the summer solstice 2020 and continued until the winter solstice (LL- Jun-Dec) or the final sampling in April 2021 (LL-June-Apr). LL-Jun-Dec tanks were returned to a simulated natural photoperiod after the winter solstice. Both photoperiod treatments showed a significant reduction in mean %MJ from the control (66%MJ): LL-Jun-Dec (11.6%MJ), LL-Jun-Apr (10.3%MJ). In both trials, minijacks had higher body weights, were longer and had increased condition factor when compared to females and immature males in all treatment groups at the final sampling. In both trials, there was little or no effect of LL treatment on fork length or body weight in immature males and females versus controls, but an increase in condition factor versus controls was observed. This study shows that continuous light treatment reduces minijack maturation in juvenile male spring Chinook Salmon and could provide an effective method for Spring Chinook Salmon hatcheries interested in reducing minijack production. Key words: sex, photoperiod, hatchery Editor: Dr. Steven Cooke Received 1 September 2022; Revised 7 December 2022; Editorial Decision 9 December 2022; Accepted 16 December 2022 Cite as: Hoffman NF, Medeiros LR, Draham ND, Nuetzel HM, Pierce AL, Nagler JJ (2023) Partial-year continuous light treatment reduces precocious maturation in age 1+ hatchery–reared male spring Chinook Salmon (Oncorhynchus tshawytscha) . Conserv Physiol 11(1): coac085; doi:10.1093/conphys/coac085. .......................................................................................................................................................... .......................................................................................................................................................... © The Author(s) 2023. Published by Oxford University Press and the Society for Experimental Biology. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/ by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited. Research article Conservation Physiology • Volume 11 2023 .......................................................................................................................................................... Previous studies have often focused on feed manipulation Introduction or ration reduction as a mechanism to reduce precocious Chinook Salmon Oncorhynchus tshawytscha express a diver- maturation rates (Larsen et al., 2006; Galbreath et al., 2020; sity of life history pathways, which not only facilitates species Pierce et al., 2021). While reduced feed ration during summer resiliency but also results in fitness trade-offs (Bourret et al., and fall months was effective in reducing minijack matura- 2016). For example, in Chinook Salmon (and many other tion, it also resulted in an undesirable reduction in the size of species), age at first maturity is phenotypically plastic and immature fish produced (Larsen et al., 2006), necessitating influenced by a range of abiotic and biotic factors (Healey, the investigation of treatments that would not negatively 1991; Taranger et al., 2010). While variation in age at first impact growth. Photoperiod is a key environmental regu- maturity increases population resilience against disastrous lator of maturation in salmonids and modifying circannual environmental events in a particular year (Greene et al., 2010; rhythms through photoperiod manipulation is highly effective Satterthwaite et al., 2017), earlier maturing individuals often at controlling the timing of puberty in salmonids (Bromage experience reduced reproductive success (Berejikian et al., et al., 1984; Duston and Bromage, 1988). Continuous light 2010; Ford et al., 2012). In anadromous Chinook Salmon, treatment has been used in a variety of salmonid species to adults typically mature at age 4; however, a notable portion of control unwanted early sexual maturation (Taranger et al., the males mature at age 3 (jack; Healey, 1991). In addition to 2010). Furthermore, several studies in different species of the jack life history form, precocious maturation in freshwater salmonids have demonstrated that, in the hatchery setting, can occur in Chinook Salmon males at age 1 (microjacks) continuous light treatments can effectively reduce the rate and age 2 (minijacks, Larsen et al., 2013). It was previously of male precocious maturation in fall spawning species. In believed that smoltification and precocious maturation were Arctic charr (Salvelinus alpinus), continuous light beginning mutually exclusive in Chinook salmon (Foote et al., 1991). and ending at different times of the year resulted in a range However, there is evidence that precociously maturing males of male precocious maturation proportions, with the best can show signs of smolt-like behaviour but are physiologically outcome resulting from an autumn start date and a return to different from non-mature smolts (Larsen et al., 2010). In a natural photoperiod in the spring (Liu and Duston, 2016, contrast to males, precocious maturation at age 1 or 2 is 2018). Overwinter continuous light treatments in Atlantic extremely rare in Chinook Salmon females within their native salmon (Salmo salar) also resulted in a decrease in the number range (Healey, 1991). In naturally spawning Chinook Salmon of fish precociously maturing (Taranger et al., 1999; Schulz et populations, microjacks and minijacks use a “sneaker” tactic al., 2006; Leclercq et al., 2010). Previous work in Chinook to gain access to much larger anadromous females and suc- Salmon showed that continuous light treatments beginning cessfully fertilize a portion of spawned ova (Ford et al., 2015). in the fall and continuing for nearly a full year can decrease This life history strategy reduces the mortality associated with the proportions of both female and male fish precociously leaving freshwater and living multiple years in the ocean and maturing as 2-year-olds (Unwin et al., 2005). is maintained, albeit at a low level, within many populations by frequency dependent selection (Berejikian et al., 2010; The aim of this study was to test whether partial-year Schroder et al., 2012). continuous light treatments can reduce the proportion of male spring Chinook Salmon precociously maturing as mini- In salmonid hatchery programs, however, elevated levels jacks assuming the constraints associated with a conservation of precocious male maturation compared to wild populations hatchery setting. Two trials, in successive years, tested contin- are often observed (Larsen et al., 2004). This is thought to be uous light treatments of 6 to 10 months with different start due to the accelerated growth rate and high energy reserves times (summer solstice and fall equinox) and end times (win- resulting from increased food availability in the hatchery ter solstice and near the spring equinox). The proportion of environment (Larsen et al., 2006; Taranger et al., 2010). In resulting minijacks was based on the measurement of elevated the Columbia River Basin, hatchery programmes motivated plasma levels of the male sex hormone 11-ketotestosterone at by conservation goals have been established to increase the the termination of the trials (Medeiros et al., 2018). abundance of spring Chinook Salmon stocks listed under the US Endangered Species Act. These conservation hatcheries use a broodstock management strategy designed to minimize Materials and Methods genetic divergence from the naturally spawning population they are meant to enhance (Mobrand et al., 2005; Paquet et Study fish al., 2011; Fast et al., 2015; Waters et al., 2015). However, The protocol for sampling design and fish care for this study these hatcheries often produce more minijacks (up to 70% of was in accordance with and approved by the University of the male juveniles produced annually; Harstad et al., 2014) Idaho Animal Care and Use Committee. Adult spring Chi- than what is observed in the wild (Larsen et al., 2010). The nook Salmon were collected at the Roza Adult Monitoring high proportion of minijacks from hatcheries reduces the Facility, WA (river kilometre 206 on Yakima River) from total number of anadromous males available for the fishery April to September (2018 and 2019) and transported to the that could be produced. Therefore, methods to reduce the Cle Elem Supplementation Research Facility (CESRF, river high proportion of minijacks in these hatchery programs are kilometre 297 on Yakima River; Cle Elum, WA.). These fish needed. .......................................................................................................................................................... 2 Conservation Physiology • Volume 11 2023 Research article .......................................................................................................................................................... were progeny from crosses of first-generation hatchery origin one of three photoperiod regimes (eight replicate tanks for anadromous parents (i.e. SH line; Fast et al., 2015, Waters each treatment): a simulated natural photoperiod (control, et al., 2015). Gametes were obtained from these adults in 46.7324 N, 117.0002 W), continuous light maintained from September and used to produce progeny for this study in 21 June 2020 to 2 April 2021 (LL-June-Apr), and continuous 2018 (trial 1, n = 2880) and 2019 (trial 2, n = 2400). Juve- light from 21 June 2020 to 21 December 2020 then returned niles, 6 months post spawned (averaging 255.5 mg in body to simulated natural photoperiod until 2 April 2021 (LL-Jun- weight and 32.6 mm in fork length) were transported to Dec; Figure 1, right panel). the University of Idaho Aquaculture Research Institute (ARI; Moscow, ID) in March of each year. Upon arrival at the ARI, Sampling procedures fish were randomly split between two 340-L troughs (dimen- In trial 1, prior to sampling, fish were euthanized with an sions = 3.5-m long × 0.6-m wide × 0.3-m depth) and fed to overdose of buffered tricaine methane sulfonate (MS-222; satiation every 1–2 hours during working hours every day. ◦ 0.1 g/L; Western Chemical, Ferndale, WA). Collection of The troughs were maintained at 14–15 C by an inline chiller FL (mm) and BW (g) for a subset of fish occurred on 23 on a recirculating water system. The fish were maintained on a September 2019 (n = 16 per tank) and 17 December 2019 simulated natural photoperiod with an abrupt light and dark (n = 20 per tank). Size parameters for the remaining fish were switch prior to the distribution into experimental tanks. collected at the final sampling on 23–26 March 2020. Fulton’s condition factor (K) was calculated as: K = 100×weight g ÷ ( ) Experimental design fork length cm . At the final sampling, blood was taken by ( ) Trial 1 was conducted from 20 June 2019 to 26 March 2020, severing the caudal peduncle and collecting it from the dorsal and trial 2 was conducted from 21 June 2020 to 2 April vessel with a heparinized Natelson tube (Kimble Chase; Rock- 2021. The end dates for the trials were selected because by wood, TN). Blood was centrifuged at 7300 × g for 5 min- this time maturation status can accurately be assessed for utes and plasma was aspirated and stored at −80 C. Male fish spawning in the fall (Medeiros et al., 2018). For both fish were identified through dissection and visual inspec- trials, 24 light-proof tanks (60 litres each) on a dedicated tion of gonads (control = 320, LL-June-Apr = 352, LL-Sept- recirculating water system were maintained at 14.5–15 Cby Apr = 321, see Supplementary Table 1). To assess matura- an inline chiller on a recirculating system. Through both trials, tion status of male fish, 11-ketotestosterone (11-KT) was alkalinity ranged from 250 to 110 ppm, mean pH was 7.95 extracted from thawed plasma samples using ether extraction and hardness ranged from 228 to 165 mg CaCO /L. Each as previously described (Caldwell et al., 2014). Reconstituted tank was covered with a light proof lid. Artificial lighting 11-KT samples were assayed in triplicate using an 11-KT was supplied by A160WE Tuna Sun aquarium lights (Kessil Enzyme Linked Immunosorbent Assay (ELISA) Kit (Cayman Aquarium; Richmond, CA) mounted on the underside of each Chemical; Ann Arbor, MI). Samples were diluted and re- lid. Photoperiod duration and intensity (1000 lux at water assayed based on initial concentrations until values fell on surface and 300 lux at tank bottom) were controlled by A- the standard curve (20–80% binding). Intra/inter-assay coef- Series Spectral controllers (Kessil Aquarium, Richmond, CA) ficients of variation (%) for trial 1 and trial 2 were 6.27/6.67 set up in series. Fish were fed Bio-Oregon pellets (www.bio- and 3.67/9.78, respectively. oregon.com) to satiation twice daily from Monday to Friday The fish in trial 2 were sampled as described above for and once daily on Saturday and Sunday. Pellet size was trial 1. BW and FL were collected from a subset of indi- adjusted appropriately for fish size throughout the trials. vidual fish on 21 December 2020 (n = 384, 16 per tank). For trial 1, in June 2019, parr with a mean fork length Blood from males (n, control = 338, LL-June-Apr = 329, LL- [FL] = 72.0 ± 0.7 mm standard error (SE) and mean body Dec-Apr = 343) was sampled from the remaining fish during weight [BW] = 3.89 ± 0.1 g SE) were randomly distributed the final sampling period from 29 March to 2 April (see into the experimental tanks (n = 120 per tank) and assigned Supplementary Table 1). to one of three photoperiod regimes (8 replicate tanks for each treatment): a simulated natural photoperiod (control, Data analyses ◦ ◦ 46.7324 N, 117.0002 W), continuous (24-hour) light main- A modification of the method previously described by tained from 21 June 2019 to 23 March 2020 (LL-Jun-Apr), Medeiros et al. (2018) was used for assigning individual and a simulated natural photoperiod from 21 June 2019 males into maturation categories based on plasma 11-KT through 23 September 2019 then switched to continuous light values from samples collected at the final samplings for both until 23 March 2020 (LL-Sep-Apr; Figure 1, left panel). The trials. Analyses were performed in RStudio version 1.4.1106 final sampling was planned for early April but was shifted (www.R-project.org). Modality of the 11-KT distributions was earlier due to the COVID-19 pandemic. assessed using the excess mass test (Multimode package; For trial 2, in June 2020, parr (FL = 75. ± 0.8 mm SE, https://arxiv.org/abs/1803.00472/). For distributions that were BW = 5.1 ± 0.2 g SE) were randomly distributed into the same significantly bimodal, NormalMixEM (mixtools package; experimental tanks (n = 100 per tank) and subjected to the www.jstatsoft.org/v32/i06/), was used to determine a cutoff same rearing conditions as trial 1. The tanks were assigned value between the modes. Those fish below the cutoff value .......................................................................................................................................................... 3 Research article Conservation Physiology • Volume 11 2023 .......................................................................................................................................................... Figure 1: Photoperiod regimes for trial 1 (left panel) and trial 2 (right panel). Control is a simulated natural photoperiod and treatment lines indicate the period of time during which spring Chinook Salmon (Oncorhynchus tshawytscha) were exposed to continuous 24-hour light for each photoperiod treatment. The photoperiod treatment lines are depicted as osff et by ±0.5 hours for visual clarity only; actual day length was as described in the Materials and Methods. were assigned as immature males (IMs) and those above Results as minijacks (MJs). All females were assigned as immature In both trials there were distinct bimodal distributions of females (IFs). The significant bimodal distributions and cutoff plasma 11-KT in the control groups with little or no overlap values from the control groups were used to assign all of the between modes, which allowed 11-KT cutoff concentrations males’ maturation status for both trials. to be determined for each trial (trial 1 = 1.79 ng/mL, trial The proportion of males maturing as MJs for each 2 = 2.56 ng/mL; see Supplementary figures 1-2 respectively). treatment was calculated as Proportion MJ = #MJ males The distribution of plasma 11-KT concentrations for the ÷total#males per tank . Proportion data were arcsine- continuous light treatments was not significantly bimodal square root transformed prior to analysis and are presented (see Supplementary figures 3-6). Continuous light photope- as percentages. For other variables measured at the final riod treatments had a strong effect on reducing the %MJ sampling, after verifying that assumptions of normality were at the end of both trials (One-way ANOVA, P < 0.0001; met prior to pooling individuals and calculating the means Figure 2). For both trials, the mean %MJ in the control group from each tank, individual values within a photoperiod was significantly higher than the respective continuous light treatment groups. No significant differences in mean %MJ treatment and maturation status category were averaged for each tank and used as inputs to the statistical analysis. BW were detected between the continuous light treatments in and FL values were log transformed prior to analysis to either trial. Between years, the trial 2 control group had a higher mean %MJ (66%) compared to the trial 1 control meet the assumptions of normality. Thus, individual tanks from each treatment (n = 8 in each treatment) were used as group (mean = 28.8%). Of the 24-hour photoperiod regimes, the experimental units for these analyses. trial 1 LL-Jun-Apr had the lowest mean %MJ (5.4%) and trial 2 LL-Jun-Dec the highest (mean = 11.7%). In trial 1, mean Comparisons from the intermediate samplings for fish %MJs for LL-Sep-Apr was 9.3% and 10.3% for LL-Jun-Apr size and %MJ at final sampling between treatments were in trial 2. done with ordinary one-way analysis of variance (ANOVA) Two-way ANOVA revealed that the following factors had followed by Tukey’s multiple comparison test. Two-way a strong effect on BW in trial 1 and trial 2: treatment, mat- ANOVA was used to test for effects of maturation category uration category and the interaction between them (Table 1). and treatment on BW, FL and K at the final samplings. Where significant interactions were found, ordinary one- The MJs, regardless of treatment, were significantly heavier way ANOVA was used to identify the effects of maturation than IFs and IMs at the end of both trials (Figure 3). MJs category and treatment followed by Tukey’s multiple in the control groups weighed less (trial 1 = 42.7 g, trial 2 = 55.0 g) than MJs in both trials’ continuous light treat- comparison test. A significance level of α = 0.05 was used for all ANOVA and multiple comparison analyses. All ments, except in the trial 2 LL-Jun-Dec treatment (55.5 g). morphometric measurements are presented as mean ± SE. No significant differences in BW were detected between IMs ANOVA analyses were completed in PRISM software version and IFs within any of the photoperiod treatments. No signif- 9.1.1 (GraphPad Inc., La Jolla, CA). icant differences in BW were detected between photoperiod .......................................................................................................................................................... 4 Conservation Physiology • Volume 11 2023 Research article .......................................................................................................................................................... The data were analysed and presented as for BW and FL for consistency. In trial 1, K for MJs in LL-Jun-Apr (1.28) and LL-Sep-Apr (1.31) was significantly increased compared to the control (1.20; one-way ANOVA followed by Tukey’s mul- tiple comparison test, P = 0.0036 and 0.0001, respectively; Figure 5). There was no significant difference in K for MJs in trial 2 between light treatment and control (One-way ANOVA followed by Tukey’s multiple comparison test, LL-Jun-Apr: P = 0.9512, LL-Jun-Dec: P = 0.4256). In trial 1, IFs and IMs in the continuous light treatments had increased K compared to IFs and IMs in the control treatment (one-way ANOVA followed by Tukey’s multiple comparison test, IFs: LL-Jun- Apr, P = 0.0271, LL-Sep-Apr, P = 0.0039; IMs: LL-Jun-Apr, P = 0.0002, LL-Sep-Apr, P < 0.0001). Likewise in trial 2, IFs and IMs in the continuous light treatments had increased K compared to IFs and IMs in the control treatment (one- way ANOVA followed by Tukey’s multiple comparison test, Figure 2: Comparison of %MJ spring Chinook Salmon IFs: LL-Jun-Apr P = 0.0053, LL-Jun-Dec P = 0.0299; IMs: LL- (Oncorhynchus tshawytscha, proportion minijacks presented as Jun-Apr P = 0.0001, LL-Jun-Dec P = 0.0015). K for MJs was percentages) across treatments for each trial. Tanks from each significantly higher than IMs and IFs within all treatments treatment (n = 8 in each treatment) used as experimental units. Mean and SE %MJ values. Different lowercase letters between treatments, except in trial 2 LL-Jun-Apr. within each trial, indicate significant differences (one-way ANOVA followed by Tukey’s multiple comparison test, P < 0.0001). There were no differences in BW, FL and K between treatment groups at the intermediate sampling for trial 1 in September (combined BW = 10.2 g, FL = 93.9 mm, K = 1.2). treatments in IMs or IFs in trial 1. However, a significant However, by the December sampling, the control group had reduction in BW was observed in IFs in trial 2’s LL-Jun-Dec a higher BW and FL (BW = 15.7 g, FL = 110.7 mm) rela- (27.8 g) treatment versus the control treatment (35.5 g; one- tive to the light treatment groups (LL-Jun-Apr BW = 13.0 g, way ANOVA followed by Tukey’s multiple comparison test, FL = 104.7 mm; LL-Sept BW = 13.3 g, FL = 107.0 mm, one- P = 0.0484). way ANOVA followed by Tukey’s multiple comparison test P < 0.0001). No differences in size parameters were observed Results from two-way ANOVA showed that maturation at the intermediate sampling in December for trial 2 (com- category and the interaction between category and treatment bined BW = 18.9 g, FL = 115.0 mm, K = 1.2). had a strong effect on FL (Table 1). There was not a significant effect of treatment on FL (P = 0.1647). Like BW, the FL of MJs was significantly greater than IFs and IMs in all treatments at Discussion the end of each trial (Figure 4). In trial 1, FL of MJs in LL- Continuous light treatments reduce Jun-Apr and LL-Sep-Apr (174.9 and 170.5 mm respectively; one-way ANOVA followed by Tukey’s multiple comparison minijack proportions test, P < 0.001) were significantly longer than in the control This study shows that partial-year continuous light treatment (149.6 mm). Also, in trial 1 no significant difference in FL strongly reduces the proportion of age 1+ male spring Chi- was observed between IFs and IMs regardless of treatment nook Salmon with elevated 11-KT in the spring, which indi- (one-way ANOVA followed by Tukey’s multiple comparison cates a corresponding reduction in fish precociously maturing test, P > 0.05). Like trial 1, MJs in trial 2 light treatments as 2-year-old MJs the following fall (Medeiros et al., 2018). (LL-Jun-Apr = 174.0 mm and LL-Jun-Dec = 168.4 mm) were All continuous light regimes resulted in significant decreases longer than MJs in the control treatment (160.8 mm, one- in the proportion of MJs compared to fish on a simulated way ANOVA followed by Tukey’s multiple comparison test, natural photoperiod. To our knowledge, only two previous P = 0.0003 and 0.0481, respectively). IFs in the trial 2 control studies have been conducted that found photoperiodic effects group (143.1 mm) were significantly longer than IFs in LL- on precocious maturation in Chinook Salmon. However, these Jun-Apr and LL-Jun-Dec treatments (135.3, and 130.8 mm, were conducted under different circumstances and with differ- one-way ANOVA followed by Tukey’s multiple comparison ent goals from the present study. In California winter Chinook test, P = 0.0401 and 0.0007, respectively). Lastly, in trial 2, Salmon, an unusual population in which juveniles emerge no significant differences between IFs and IMs were detected from late summer to fall, earlier shifted photoperiods begun when comparing within treatment groups (P > 0.05). in the fall at ∼3 months post-fertilization increased microjack For both trial 1 and 2, two-way ANOVA revealed no signif- maturation 9 months later (Beckman et al., 2007). In a stock icant interaction effect for K. However, maturation category of Chinook Salmon introduced into New Zealand and raised and treatment had a significant effect on final K (Table 2). under production aquaculture conditions, a continuous light .......................................................................................................................................................... 5 Research article Conservation Physiology • Volume 11 2023 .......................................................................................................................................................... Table 1: Results from two-way ANOVAs on the eeff cts of photoperiod treatment, maturation category and the interaction of photoperiod treatment and maturation category on body weight (BW; g), fork length (FL; mm) and Fulton’s condition factor (K) in age 1+ male spring Chinook Salmon (Oncorhynchus tshawytscha) at the end of each trial. Response Effect SS DF F P value Trial 1 BW Photoperiod treatment 1745 2 4.18 0.0197 Maturation category 25 036 2 59.97 <0.0001 Interaction 4076 4 4.881 0.0017 Trial 2 BW Photoperiod treatment 357.5 2 4.389 0.0164 Maturation category 13 211 2 162.2 <0.0001 Interaction 579.4 4 3.557 0.0112 Trial 1 FL Photoperiod treatment 429.5 2 1.856 0.1647 Maturation category 22 675 2 98.02 <0.0001 Interaction 2761 4 5.966 0.0004 Trial 2 FL Photoperiod treatment 198.1 2 2.504 0.0899 Maturation category 17 809 2 225.1 <0.0001 Interaction 1225 4 7.739 <0.0001 Trial 1 K Photoperiod treatment 0.139 2 29.82 <0.0001 Maturation category 0.159 2 34.15 <0.0001 Interaction 0.004 4 0.4435 0.7767 Trial 2 K Photoperiod treatment 0.033 2 13.39 <0.0001 Maturation category 0.071 2 29.15 <0.0001 Interaction 0.011 4 2.303 0.0682 Significant ( α = 0.05) P values are in bold Figure 3: Comparisons of spring Chinook Salmon (Oncorhynchus tshawytscha) BW (mean ± SE) between treatment and maturation category for trial 1 (left panel) and trial 2 (right panel) in juvenile spring Chinook Salmon measured at final samplings. Lowercase letters indicate comparisons between maturation categories within a photoperiod treatment group (bars not sharing a letter differ significantly; one-way ANOVA followed by Tukey’s multiple comparison tests, P < 0.05). Uppercase letters indicate comparisons between photoperiod treatment groups within each maturation category (significance indicat ion and statistical analysis same as for lowercase letters). photoperiod beginning in the fall at age 1 and continuing the continuous light photoperiod used in the New Zealand for nearly a full year reduced precocious maturation at age study would be impossible in a conservation hatchery setting 2 in both males and females (Unwin et al., 2005). However, such as CESRF, where fish are released at age 1+ in the .......................................................................................................................................................... 6 Conservation Physiology • Volume 11 2023 Research article .......................................................................................................................................................... Figure 4: Comparisons of spring Chinook Salmon (Oncorhynchus tshawytscha) FL (mean ± SE) between treatment and maturation category for trial 1 (left panel) and trial 2 (right panel) in juvenile spring Chinook Salmon measured at final samplings. Lowercase letters indicate comparisons between maturation categories within a photoperiod treatment group (bars not sharing a letter differ significantly; one-way ANOVA followed by Tukey’s multiple comparison tests, P < 0.05). Uppercase letters indicate comparisons between photoperiod treatment groups within each maturation category (significance indicat ion and statistical analysis same as for lowercase letters). Figure 5: Comparisons of spring Chinook Salmon (Oncorhynchus tshawytscha) K (mean ± SE) between treatment and maturation categories for trial 1 (left panel) and trial 2 (right panel) measured at final samplings. Lowercase letters indicate comparisons between maturation categories within a photoperiod treatment group (bars not sharing a letter differ significantly; one-way ANOVA followed by Tukey’s multiple comparison tests, P < 0.05). Uppercase letters indicate comparisons between photoperiod treatment groups within each maturation category (significance indication and statistical analysis same as for lowercase letters). spring. Thus, while these previous studies demonstrate that prepare juvenile salmonids for downstream migration and seawater entry (McCormick, 2013). Smoltification includes photoperiod manipulation can influence precocious matura- the development of hypoosmoregulatory ability, which is tion in Chinook Salmon, they provide little guidance on how + + associated with increases in gill Na /K -ATPase enzyme to apply photoperiod manipulation with the goal of reducing activity (NKA) and a decrease in condition factor (K), along MJ maturation in conservation hatcheries for spring Chinook with other changes (McCormick, 2013). Peak levels of NKA Salmon. occur during May in Yakima River spring Chinook Salmon, whereas the smoltification-related decrease in K begins in early April (Beckman et al., 2000; Larsen et al., 2010). Potential ee ff cts of continuous light Juveniles released from CESRF need to smolt properly to treatments on smoltification return as anadromous adults. Studies in Atlantic Salmon Like its role in reproduction, photoperiod is the key suggest that juveniles reared under continuous light can smolt environmental cue regulating smoltification, the suite of properly, as long as the continuous light is followed by a behavioural, morphological, and physiological changes that “winter” of at least 6 weeks of short photoperiod followed .......................................................................................................................................................... 7 Research article Conservation Physiology • Volume 11 2023 .......................................................................................................................................................... by a switch to long photoperiod (Duston and Saunders, 1990; for which returning adults are not allowed to spawn in the Duncan and Bromage, 1998; Strand et al., 2018). Thus, river (Fast et al., 2015; Waters et al., 2015). To assess any the LL-Jun-Apr and LL-Sep-Apr photoperiods used in the effects of a single generation of hatchery rearing, some of present study might be expected to disrupt smoltification. the returning adults from the integrated line (designated as However, the LL-Jun-Dec photoperiod allowed 13 weeks supplementation hatchery or SH line fish) may be used to of naturally increasing short photoperiod (<12 hours light propagate juveniles to study potential effects of a single gen- per day) followed by 8 weeks of naturally increasing long eration of hatchery rearing on reproductive parameters and photoperiod (>12 hours light per day) before the expected juvenile growth, after which the juveniles are culled (Knudsen NKA peak in Yakima River spring Chinook Salmon. Thus, et al., 2006, 2008). As these juveniles are never released, they there is reason to think that smoltification may be properly are available for research and are the fish used in the current entrained in this group. Juvenile Chinook Salmon raised study. under a naturally increasing photoperiod showed stronger At a broader scale, a study that investigated the proportion and more coordinated changes in indices associated with of MJs produced among integrated and segregated spring smoltification versus fish raised under a continuous light Chinook Salmon hatcheries across the Columbia River basin or a constant photoperiod (Hoffnagle and Fivizzani, 1998). showed that integrated hatchery lines produced higher per- Although condition factor was increased versus controls in centages of MJs (Harstad et al., 2014). In agreement with all of the continuous light treatments, including the LL-Jun- this study, the MJ maturation proportion is higher in the Dec group, photoperiod manipulation may cause different CESRF integrated and supplementation hatchery lines than aspects of smoltification to become desynchronized, without in the segregated line (Larsen et al., 2019). Therefore, we impeding the ability of fish to osmoregulate and grow in believe that the supplementation hatchery line used in our saltwater (Duston and Saunders, 1990; Duncan et al., 1998). study is representative of the integrated production line, at In addition, the late March to early April final sampling least insofar as response to photoperiod is concerned. The point in the present study was before K decreases in smolting difference in MJ proportion between integrated and segre- Yakima River spring Chinook salmon and thus would not gated lines may be due to differences in hatchery broodstock capture any decrease associated with smolting (Beckman et management, especially given that age at maturity is under al., 2000; Larsen et al., 2010). The present study was designed relatively strong genetic control in Chinook Salmon (Hankin to determine whether photoperiod treatment can reduce et al., 1993). Segregated hatcheries select against precocious precocious male maturation at CESRF, not as an assessment males across multiple generations, which is proposed to lead of the effects on smoltification. Investigations evaluating to reduced expression of this phenotype (Harstad et al., 2014; the effects of continuous light regimes on smoltification are Larsen et al., 2019). In contrast, the natural origin fish used as necessary before any conclusions can be drawn regarding the broodstock in integrated programs are part of the naturally usefulness of photoperiod manipulation as a management spawning population, which includes some precocious male tool. ancestry. This is proposed to result in higher proportions of MJs when progeny from these parents are raised in the Method to reduce minijack proportions hatchery environment (Harstad et al., 2014; Larsen et al., while limiting genetic divergence 2019). Thus, the results from this study present a potentially effective method for reducing the proportion of MJs produced Integrated conservation hatcheries are managed to recover by integrated hatchery programmes, without compromising and enhance populations of salmonids while limiting genetic broodstock management designed to minimize genetic diver- divergence from natural origin fish. To meet production goals, gence between the hatchery reared and natural population. the hatchery programme at CESRF, which provided the juve- nile Chinook Salmon for this study, uses gametes harvested from natural origin adults returning to the Yakima River, WA Effect of light treatment on size each year. The juveniles produced at CESRF are then released into the Yakima River and returning adults of both hatchery Some past investigations on smolt to adult returns in Chi- and natural origin are allowed to spawn in the river. This nook Salmon have shown that larger smolts return at higher type of program contrasts with segregated hatchery brood- rates than their smaller counterparts (Martin and Wertheimer, stock management programs, which utilize hatchery origin 1989; Beckman et al., 1999; Beckman et al., 2017), whereas adults as broodstock across multiple generations. In order to others have not (Feldhaus et al., 2016). For this and other compare the effects of integrated and segregated broodstock reasons, hatcheries often aim to release large smolts, making it management, as well as any effects of a single generation desirable that the methods used to reduce precocious matura- of hatchery rearing, CESRF produces two lines of juvenile tion do not reduce the size of released immature fish. Previous Chinook Salmon: (i) an integrated production line in which studies aimed at reducing MJ proportions in Yakima River the broodstock are comprised of natural-origin returning spring Chinook Salmon used reduced ration during summer adults descended from parents that spawned in the wild, and and fall months, which resulted in reduced size of immature (ii) a segregated hatchery control line for which broodstock fish relative to fully fed controls (Larsen et al., 2006, 2013). are hatchery-origin fish (of increasing hatchery lineage) and The continuous light treatments in this study had little consis- .......................................................................................................................................................... 8 Conservation Physiology • Volume 11 2023 Research article .......................................................................................................................................................... tent effect on weight or lengths of immature males or females Data availability in either trial at the end of the study in April. Therefore, it Data generated during the course of this study are available seems unlikely that the photoperiod treatment would affect through the corresponding author upon request. the ability of hatchery managers to use previously established protocols to obtain their target release size. Acknowledgements Differences in %MJ between trials We are grateful to retired CRITFC scientist Dr Peter Galbreath A large difference in the percentage of precociously maturing for providing support for beginning this study. We would fish in the control treatments occurred between the two like to thank the Yakama Nation and WDFW staff, partic- trials in this study. This result is best explained by a strong ularly Chad Stockton, at the Cle Elum Supplementation and effect from the different family genetic backgrounds of the Research Facility for providing us with the fish to conduct individual broodstock used to produce the fish used in these these trials. We would also like to thank the staff at the Uni- experiments. Galbreath et al. (2022) similarly report a wide versity of Idaho’s Coldwater Aquaculture Research Institute range in MJ proportions between family crosses across three for providing fish care throughout both trials. brood years of the SH line. Estimated MJ rates from gen- eralized linear models ranged from 20% to 80%, and this high inter-family variation was found to be largely driven Supplementary material by random effects of the individual dams and sires (Gal- breath et al., 2022). This suggests heritable factors likely Supplementary material is available at Conservation Physiol- influence precocious maturation rates, and as such, year to ogy online. year variation in the proportion of MJs is expected given that a different subset of returning adults are captured for spawning at CESRF each year. Furthermore, the variation References in the proportion of precociously maturing Chinook Salmon males at integrated hatcheries (including CESRF) has been Beckman BR, Dickhoff WW, Zaugg WS, Sharpe C, Hirtzel S, Schrock previously reported to range from 8% to 71% (Larsen et R, Larsen DA, Ewing RD, Palmisano A, Schreck CB et al. (1999) al., 2004; Larsen et al., 2013; Harstad et al., 2014). As Growth, smoltification, and smolt-to-adult return of spring Chinook the proportions of precociously maturing fish in the con- salmon from hatcheries on the Deschutes River, Oregon. TAm trol treatments of this study were within this range, it is Fish Soc 128: 1125–1150. https://doi.org/10.1577/1548-8659(1999 assumed to be in line with the natural variation between )128<1125:GSASTA>2.0.CO;2. years rather than an effect of the treatment or environmental Beckman BR, Gadberry B, Parkins P, Cooper KA, Arkush KD (2007) State- conditions. dependent life history plasticity in Sacramento River winter-run Chi- nook salmon (Oncorhynchus tshawytscha): interactions among pho- toperiod and growth modulate smolting and early male maturation. Conclusion Can J Fish Aquat Sci 64: 256–271. https://doi.org/10.1139/f07-001. Beckman BR, Harstad DL, Spangenberg DK, Gerstenberger RS, Brun CV, This study shows that partial-year continuous light treat- Larsen DA (2017) The impact of different hatchery rearing environ- ments significantly reduce precocious male maturation as ments on smolt-to-adult survival of spring Chinook salmon. T Am Fish MJs in spring Chinook Salmon while maintaining the genetic Soc 146: 539–555. https://doi.org/10.1080/00028487.2017.1281168. diversity present in the natural origin fish. Additionally, these continuous light treatments generally did not affect immature Beckman BR, Larsen DA, Sharpe C, Lee-Pawlak B, Schreck CB, Dickhoff fish weight or length relative to control treatments, which WW (2000) Physiological status of naturally reared juvenile spring allows the target size at release to still be under the con- Chinook salmon in the Yakima River: seasonal dynamics and changes trol of the protocols in place at conservation hatcheries. associated with smolting. T Am Fish Soc 129: 727–753. https://doi. However, further investigations into the effect of these light org/10.1577/1548-8659(2000)129<0727:PSONRJ treatments on smoltification, sex ratios and returning age E;2.3.CO;2. class structure must be conducted to fully evaluate the effec- Berejikian BA, Bradford M, Van Doornik DM, Endicott RC, Hoffnagle TL, tiveness of this tool within the salmon hatchery management Tezak EP, Moore ME, Atkins J (2010) Mating success of alternative sphere. male phenotypes and evidence for frequency-dependent selection in Chinook salmon, Oncorhynchus tshawytscha. Can J Fish Aquat Sci 67: 1933–1941. https://doi.org/10.1139/F10-112. Funding Bourret SL, Caudill CC, Keefer ML (2016) Diversity of juvenile Chi- This study was supported by funding from the Bonneville nook salmon life history pathways. Rev Fish Biol Fish 26: 375–403. 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Appl 8: 956–971. https://doi.org/10.1111/eva.12331. ..........................................................................................................................................................
Journal
Conservation Physiology – Oxford University Press
Published: Jan 20, 2023
Keywords: sex; photoperiod; hatchery