North American Journal of Aquaculture Spawning ...

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Spawning, Larviculture, and Salinity Tolerance of Alewives and Blueback Herring in Captivity a

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Matthew A. DiMaggio , Harvey J. Pine , Linas W. Kenter & David L. Berlinsky

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Department of Biological Sciences, University of New Hampshire, 38 College Road, Durham, 03824, New Hampshire, USA b

Department of Environmental Studies, Colby-Sawyer College, 541 Main Street, New London, 03257, New Hampshire, USA Published online: 08 Jun 2015.

Click for updates To cite this article: Matthew A. DiMaggio, Harvey J. Pine, Linas W. Kenter & David L. Berlinsky (2015) Spawning, Larviculture, and Salinity Tolerance of Alewives and Blueback Herring in Captivity, North American Journal of Aquaculture, 77:3, 302-311, DOI: 10.1080/15222055.2015.1009590 To link to this article: http://dx.doi.org/10.1080/15222055.2015.1009590

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North American Journal of Aquaculture 77:302–311, 2015 C American Fisheries Society 2015 ISSN: 1522-2055 print / 1548-8454 online DOI: 10.1080/15222055.2015.1009590

ARTICLE

Spawning, Larviculture, and Salinity Tolerance of Alewives and Blueback Herring in Captivity Matthew A. DiMaggio1 Department of Biological Sciences, University of New Hampshire, 38 College Road, Durham, New Hampshire 03824, USA

Harvey J. Pine

Downloaded by [Maxillo Facciali] at 05:22 04 August 2015

Department of Environmental Studies, Colby-Sawyer College, 541 Main Street, New London, New Hampshire 03257, USA

Linas W. Kenter and David L. Berlinsky* Department of Biological Sciences, University of New Hampshire, 38 College Road, Durham, New Hampshire 03824, USA

Abstract Precipitous declines in wild populations of river herring species (Alewives Alosa pseudoharengus and Blueback Herring A. aestivalis) have led to increased interest in stock enhancement efforts. Additionally, their popularity as a baitfish among recreational anglers has generated interest in commercial production of these species for marine baitfish markets. The objective of this investigation was to elucidate practical culture protocols for captive propagation of these species for commercial and restoration purposes. Wild Blueback Herring, captured during their annual spawning migration, spawned in tanks volitionally, while Alewives required exogenous hormone administration. Larvae of both species were successfully raised through metamorphosis using a feeding regime comprised of enriched rotifers followed by Artemia nauplii and a commercially available diet. Survival of early larvae acclimated to salinities ranging from 5‰ to 15‰ was high for both species (>94.0%) while that for older larvae acclimated to 15, 20, and 30‰ ranged from 64.7% to 95.3%. Juveniles raised at varying salinities (0–30‰) exhibited high survival (95.6–100.0%) and excellent feed conversion ratios (≤1.31) in all treatments. In acute salinity transfer experiments, high survival was observed when fish of both species (233–275 d posthatch) were transferred from low to high salinities, but low survival (10.0% and 3.3%) was observed in Alewives transferred from 15‰ or 30‰ to freshwater (0‰). A nodular fibrotic growth was found on 3.7% and 10.1% of the cultured Alewives and Blueback Herring (≥231 d posthatch), respectively, that likely followed tissue trauma and ulceration. The results of these studies provide a framework for river herring culture in recirculating systems.

Alewives Alosa pseudoharengus and Blueback Herring A. aestivalis are anadromous, clupeid fishes found along the Atlantic coast of North America that are collectively referred to as river herring in the United States and gaspereau in Canada (Munroe 2002). River herring supported important fisheries throughout their range for centuries where they were used for

food, bait, and fertilizer (Messieh 1977; Loesch 1987). They also serve as important prey for many riverine, estuarine, and oceanic fishes, birds, and mammals (Walters et al. 2009; Jones et al. 2010). The ranges of Alewives and Blueback Herring extend from Labrador to South Carolina and from Nova Scotia to Florida, respectively, and in areas of sympatry, both species

*Corresponding author: [email protected] 1 Present address: Tropical Aquaculture Laboratory, Program in Fisheries and Aquatic Sciences, School of Forest Resources and Conservation, Institute of Food and Agricultural Sciences, University of Florida, 1408 24th Street Southeast, Ruskin, Florida 33570, USA. Received October 30, 2014; accepted January 12, 2015

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are often found in the same spawning rivers. Although very similar in appearance, river herring species can be distinguished by morphological characteristics including eye diameter, body depth, and peritoneum color (Mullen et al. 1986). The timing of their spawning migrations and preferred spawning habitats may also be species-specific but hybridization is not uncommon (Loesch 1987; O’Connell and Angermeier 1997; McBride et al. 2014). River herring populations have exhibited drastic declines throughout much of their range, were listed as a U.S. National Marine Fisheries Service “species of concern” in 2006, and were considered as candidates for the U.S. Endangered Species List (NOAA NMFS 2009, 2013). While the exact causes of these population declines are unknown, the most likely threats include spawning habitat loss due to construction of dams and other impediments to migration, habitat degradation, overexploitation, and increased predation from recovering Striped Bass Morone saxatilis populations (DFO 2001; Heimbuch 2008; NOAA NMFS 2009; Davis et al. 2012). In response to these declines, a number of state-specific fishing restrictions have been implemented, including harvest moratoria in several states. Restoration efforts have been initiated through adult relocation and release of hatchery-produced larvae and fry (K. Sullivan, New Hampshire Fish and Game, personal communication). In addition to stock enhancement, river herring have also been considered as a candidate marine baitfish species to support the lucrative marine recreational fishing industry in the Northeast (M. A. DiMaggio, M. Watson, and D. L. Berlinsky, abstract presented at World Aquaculture Society meeting, 2013). As detailed hatchery procedures have not been established (Heinrich 1981), the current studies were undertaken to provide practical methods for captive spawning and larviculture of river herring species. Studies were also conducted to determine larval and juvenile tolerance to salinity changes, such as those that might be experienced by baitfish during acclimation, transport, and use. METHODS Broodstock Acquisition Sexually mature Alewives and Blueback Herring (or bluebacks) were collected during their annual spawning migration from fish ladders located in the Lamprey and Oyster rivers, Strafford County, New Hampshire, from May through June during 2012 and 2013. The species were identified by morphological differences that were verified with 100% accuracy by postmortem examination of their peritoneal cavities (Leim and Scott 1966; Scott and Crossman 1973). Alewives in both seasons appeared in the spawning rivers approximately 3 weeks earlier than bluebacks and in much greater numbers. Broodstock (TL, ∼25 cm; weight, ∼200 g) were transported to the Aquaculture Research Center at the University of New Hampshire (ARCUNH), Durham, New Hampshire, and transferred to six 1,750-L

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tanks that were incorporated within a 11,000-L recirculating system. The broodstock system was equipped with biological and mechanical filtration, foam fractionation, ultraviolet sterilization, and supplemental aeration. Salinity and water temperature were controlled to simulate the natural spawning environment and were maintained at 2–4‰ and 15–19◦ C, respectively. Water temperature was increased throughout the spawning season to match that of the rivers from which the broodstock were captured. During all handling procedures, broodstock were anesthetized with tricaine methanesulfonate (100 mg/L; MS222, Western Chemical, Ferndale, Washington). Males were distinguished from females by the presence of milt upon application of gentle pressure anterior to the urogenital opening. Broodstock Spawning Alewives.— During the 2012 spawning season, female Alewives were evaluated by intraovarian cannulation (Shehadeh et al. 1973) and found to have fully vitellogenic oocytes, but eggs could not be palpated (stripped) for manual spawning. Furthermore, Alewives observed for up to 21 d failed to volitionally tank spawn when maintained in equal sex ratios of six males : six females or 12 males : 12 females. Consequently, during the 2013 spawning season, females (F; 27.5 ± 0.3 cm TL [mean ± SE], 176.0 ± 9.4 g) were implanted in the dorsal musculature with 95% cholesterol : 5% cellulose pellets (Sherwood et al. 1988) containing 25 µg [D-Ala6 Des-Gly10]-luteinizing hormone releasing hormone (LHRH) ethylamide (LHRHa; Bachem, Belmont, California) and housed with males (M) in two experimental sex ratios (2F:6M and 4F:4M), with three replicate tanks per treatment. The culture tanks were observed for 96 h following hormone administration and spawned eggs were siphoned daily from the bottoms of the culture tanks, concentrated using a 500-µm-mesh sieve, and quantified volumetrically. A subsample of eggs (n = 200) from each spawn was evaluated under a dissecting microscope to determine developmental stage and fertilization success; six 500-µL egg aliquots were enumerated. The collected eggs were incubated in aerated, static, Macdonald jars (21–24◦ C, 3‰ salinity) containing 400 mg/L formalin (Parasite-S, Western Chemical, Ferndale, Washington) until hatching. The water in the hatching containers was completely replaced twice daily to prevent the accumulation of nitrogenous wastes from decomposing eggs and hatched larvae. Blueback Herring.— In 2012 it was determined that eggs could be stripped from some Blueback Herring females, particularly late in the spawning season, and that volitional spawning was feasible without hormone administration. “Dry” manual spawning was performed with seven females by blotting the urogenital opening, stripping eggs into 2-L, polyethylene beakers and adding ∼100 µL fresh milt/100 mL eggs. Approximately 500 mL of water was added to the egg–sperm mixtures; they were then gently swirled for 2 min and finally rinsed twice with freshwater to remove sperm. The fertilized eggs were incubated

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in Macdonald jars as described above. In 2013, 6–18 females were paired 1:1 with spermiating males per tank in six spawning trials and tanks were examined daily for the presence of spawned eggs. Fertilization success was determined as described above. Larviculture Alewife and blueback larvae (0 d posthatch [DPH]) were stocked separately into 12 round, black, 150-L plastic tanks at densities of approximately 50–125 fish/L. Water in the tanks was gently aerated and held static from 0 to 45 DPH. Debris was siphoned from the tank bottoms daily, and 50% of the tank water volume was exchanged on alternate days to prevent the accumulation of nitrogenous wastes. Water temperature ranged from 17◦ C to 24◦ C over the course of the trial and photoperiod was adjusted to simulate seasonal fluctuations (∼13 h light : 11 h dark; ∼400 lx). Salinity was held at 5‰ using a mixture of fresh well water and synthetic sea salts (Instant Ocean, Spectrum Brands, Atlanta, Georgia). Larvae were fed rotifers Brachionus plicatilis enriched with an algal concentrate (Rotigrow Plus, Reed Mariculture, Campbell, California), 3–6 times daily at a feeding density of 20 rotifers/mL from 2 to 25 DPH. Rotifers were reintroduced when few or none remained in the water column. The algal concentrate was also maintained in the larviculture tanks during rotifer feeding (“green water”; >500,000 cells/mL) to increase larval feeding efficiency and preserve the nutrient profiles of introduced live feeds. From 19 to 25 DPH, the larvae were fed with both decapsulated Artemia nauplii and rotifers, and when the majority of larvae were visibly consuming Artemia, rotifer feeding and microalgae supplementation were suspended. Artemia were fed two to three times daily at densities of 2 Artemia individuals/mL from 19 to 40 DPH. Beginning at 35 DPH the larvae were offered a commercially prepared 250–360-µm granule diet (Otohime B1, Reed Mariculture, Campbell, California; 51% crude protein, 11% crude fat) by coating the water surface layer (∼600 µL portions). When the majority of larvae were visibly consuming the diet, Artemia supplementation was suspended and the diet was fed four times daily. The larvae were gradually transitioned to larger particle sizes (Otohime B2, 360–650 µm, 51% crude protein, 11% crude fat; and Gemma Wean Diamond, (Skretting, Stavanger, Norway), 800 mm, 57% crude protein, 15% crude fat) as larval growth progressed. For growth measurements, larvae (n = 9.7 ± 0.2) were periodically collected from the culture tank (see Figure 1), euthanized with an overdose (100 mg/L) of MS-222, and photographed under a dissecting microscope (Nikon, Chiyoda-ku, Tokyo). Larval lengths were digitally analyzed using SigmaScan Pro 5.0 software and pictures were evaluated for the presence of inflated swim bladders. Length was defined as a straight line measurement from the anteriormost point of the head to the posterior tip of the notochord for preflexion larvae or to the posterior edge of the hypural plates for flexion and postflexion larvae.

Juvenile Salinity Growth Experiment Alewives.— The juvenile Alewives used in this study were cultured as described above to 144 DPH and initially held in the broodstock system at a salinity of 5‰. The experiment was carried out in three, identical, 970-L recirculating systems, each with four 235-L circular tanks, a bead filter, foam fractionator, ultraviolet sterilizer, and supplemental aeration. Experimental systems were assigned to one of three treatments (0, 15, and 30‰) with four replicate tanks per salinity, at a density of 45 fish/tank. A subsample of 8% of the total stocked population (n = 540) was anesthetized at the start of the experiment to determine mean TL and weight. System salinities were adjusted over a 5-d period to attain the desired final salinities by adding well water (0‰ treatment), sterilized seawater and well water (Great Bay Estuary, New Hampshire; 15‰ treatment), and sterilized seawater and artificial sea salts (30‰ treatment). Temperature was held constant at 21◦ C with titanium heating elements and the photoperiod was held static at 12 h light : 12 h dark with artificial lighting. Alewives were initially fed a 1.2-mm sinking pellet (BioVita Fry, Bio-Oregon, Longview, Washington; 50% crude protein, 22% crude fat) at 1.5% of the biomass in each tank twice daily for days 0–65 of the experiment. The diet was transitioned to a 2mm sinking pellet (Europa 15NP, Skretting; 55% crude protein, 15% crude fat) from day 66 to day 87, and feed quantity was reduced to 1% of the tank biomass fed twice daily. Growth (TL and weight) was periodically evaluated on days 24, 45, and 66 from an 11% subsample (n = 5) from all replicates across all treatments. Feed volumes were adjusted to compensate for observed mortalities and increases in biomass throughout the experimental period. The experiment was concluded after 87 d in culture and all fish were enumerated, weighed, and measured to assess final survival and growth. Specific growth rate (SGRwt ) was calculated using the following formula: % SGRwt = 100 × [ln(final weight of fish) − ln(initial weight of fish)] / trial duration (d). Feed conversion ratio (FCR) was calculated using the following formula: FCR = feed intake / body weight gain. All weights used in formulas are in grams. Blueback Herring.—The methods for the blueback juvenile salinity growth experiment were similar to those described above except the fish were 226 DPH at the start of the experiment, were stocked at a density of 40 fish/tank, and were cultured at 3, 15, and 30‰ salinity. Salinity was increased to discourage parasitic fungi that were occasionally detected on the fish’s fins. Bluebacks were fed at 1.5% of the biomass in each tank twice daily for days 0–47 of the experiment and growth (TL and weight) was evaluated on day 26 from a 13% subsample (n = 5) across all treatments. The experiment was concluded after 47 d in culture. Acute Salinity Transfer Study Forty-eight hours after the conclusion of the salinity growth experiments, juveniles were transferred to three, identical, 740-L recirculating systems, each with three 115-L circular tanks, moving bed biofilter, and supplemental aeration.

ALEWIVES AND BLUEBACK HERRING IN CAPTIVITY TABLE 1. Mean ± SE 48-h survival of Alewives and Blueback Herring following acute salinity transfers. Different letters within columns and transfer regime denotes significant differences (P < 0.05). Transfer regimes constitute transfer from three salinities to a final common salinity (transfer into the same salinity treatments served as controls).

Alewife


Salinity transfer regime (‰) 0→0 15→0 30→0 0→15 15→15 30→15 0→30 15→30 30→30

Blueback Herring

Survival (%)

Salinity transfer regime (‰)

± ± ± ± ± ± ± ± ±

3→3 15→3 30→3 3→15 15→15 30→15 3→30 15→30 30→30

96.7 10.0 3.3 100.0 100.0 100.0 100.0 100.0 100.0

3.3 z 5.8 y 3.3 y 0.0 z 0.0 z 0.0 z 0.0 z 0.0 z 0.0 z

Survival (%) 100.0 96.7 93.3 100.0 100.0 100.0 100.0 100.0 100.0

± ± ± ± ± ± ± ± ±

0.0 z 3.3 z 6.7 z 0.0 z 0.0 z 0.0 z 0.0 z 0.0 z 0.0 z

The experimental systems were assigned to one of three salinity treatments identical to that of the previous study (0, 15, and 30‰ for Alewives and 3, 15, and 30‰ for bluebacks). Ten fish from the three salinity treatment systems were each transferred to a single separate tank in each of the three experimental systems according to the transfer regimes outlined in Table 1. Transfer into the same salinity treatments (i.e., 0 → 0, 3 → 3) served as controls. All tanks were monitored for mortalities over a 48-h interval. This experiment was conducted an additional two times, resulting in three replicates for all acute salinity transfers. Gradual Salinity Acclimation Low-range salinity acclimation.—Alewife and blueback larvae used in the low-range acclimation study were cultured for 28 and 25 d, respectively, using methods previously described. A total of 450 larvae of a single species (Alewives: TL = 12.78 ± 0.46 mm; bluebacks: TL 12.33 ± 0.26 mm) were transferred from the larval rearing system and equally distributed among nine 37.9-L static glass aquaria filled with 19 L of water and gently aerated. Water in both the larval rearing and aquarium systems were initially maintained at 5‰ using a mixture of synthetic sea salt and well water, and water temperature ranged from 21◦ C to 22◦ C throughout the course of the experiment. Aquaria were randomly assigned to one of three treatments (5, 10, and 15‰) and salinities were increased in the 10‰ and 15‰ treatments 2.5‰ per day by the addition of synthetic sea salt, until terminal salinities were attained. River herring larvae maintained at 5‰ served as controls for mortalities associated with experimental stress. Water exchanges (9.5 L) were carried out daily to control for the accumulation of nitrogenous wastes and larvae were fed Artemia nauplii and dry diet as described above. Aquaria were maintained at final treatment salinities for a minimum of 72 h and survival was assessed daily and recorded.

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High-range salinity acclimation.—Methods for the highrange acclimation were similar to those described for the lowrange acclimation experiment except that Alewife and blueback larvae were 40 and 48 DPH and had a TL (mean ± SE) of 17.48 ± 0.54 mm and 12.82 ± 0.32 mm, respectively. Aquaria were randomly assigned to one of three treatments (15, 20, and 30‰) and salinities were increased 2.5‰ per day by the addition of synthetic sea salt until terminal salinities were attained. Juvenile Health Assessment Captive spawned Alewives and Blueback Herring were observed over the course of 1 year’s development for gross indications of disease and parasitism. The presence of nodular growths emanating from the soft tissue and bones of the upper and lower jaws of both species were noted. A subsample of 539 Alewives (231 DPH) and 469 Blueback Herring (273 DPH) were captured, anesthetized (100 mg/L MS-222), and visually assessed to determine prevalence of growths among the captive populations. Three fish of each species that exhibited the growths were euthanized (100 mg/L MS-222), and the nodules were excised and fixed in 10% neutral buffered formalin for 24 h and processed for routine histology with hematoxylin and eosin staining. Prepared slides were evaluated by the University of New Hampshire Veterinary Diagnostic Laboratory (UNHVDL). Statistical Analysis All data were analyzed using an ANOVA in the PROC GLM function of SAS version 9.3 (SAS Institute, Cary, North Carolina) followed by a Tukey’s honestly significantly different means separation test except as noted below. All percentage data were arcsine-square-root transformed prior to analyses. Log transformations were performed on all other data that violated the assumptions of ANOVA. Data that could not be transformed were subjected to a Kruskal–Wallis one-way ANOVA and pairwise comparisons were made using a Wilcoxon rank sum test using a Bonferroni correction. Mean egg production per female (72- and 96-h spawns), total egg production per female, and total egg production per gram female body weight were analyzed with a two-tailed Student’s t-test for the Alewife spawning sex ratio experiment. All numerical data are represented as the mean ± SE. A P-value < 0.05 was considered statistically significant for all analyses. RESULTS Spawning and Larviculture Alewives spawned within 72 h following hormone implantation and bluebacks required no hormones and spawned volitionally. Eggs of both species incubated in Macdonald jars hatched in approximately 48–72 h at 21–24◦ C. Preliminary larval feeding regimes (Figure 1) were established and larvae were

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FIGURE 1. Mean length of (A) Alewives and (B) Blueback Herring cultured for 45 and 55 DPH, respectively. Length was defined as a straight line measurement from the anteriormost point of the head to the posterior tip of the notochord for preflexion larvae or to the posterior edge of the hypurals for flexion and postflexion larvae. Error bars represent ± 1 SE. Shaded regions indicate a general feeding regime used during the larval culture period. Rotifers refer to Brachionus plicatilis, Artemia refers to Artemia sp., and dry diet refers to Otohime B1. Rotifers and Artemia were co-fed for 19–25 DPH and Artemia and dry diets were co-fed for 35–40 DPH. Initiation of swim bladder inflation and metamorphosis is depicted by black arrows.

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FIGURE 2. (A) Larval development of Alewives. The black arrow indicates a visibly inflated swim bladder at 25 DPH. (B) Larval development of Blueback Herring. The black arrow indicates a visibly inflated swim bladder at 21 DPH. Black scale bars = 5 mm for photographs in lower right of panels A and B. A 1-mm Sedgewick Rafter grid was placed in the background of all other photographs to show scale.

weaned; postmetamorphic Alewives and bluebacks were produced for use in subsequent experimentation. Larvae of both species began exogenous feeding by 2 DPH once yolk and oil reserves were exhausted. Growth of larval Alewives was rapid and at 45 DPH were 18.57 ± 0.73 mm in length (mean ± SE). Swim bladder inflation and metamorphosis was first observed in larvae at 25 and 45 DPH, respectively (Figures 1A, 2A). Bluebacks also exhibited rapid growth and were 25.56 ± 1.18 mm in length at 55 DPH. Swim bladder inflation and metamorpho-

sis was first observed in larvae at 14 and 55 DPH, respectively (Figures 1B, 2B). Alewife Spawning Sex Ratio Alewives produced 1,056 ± 47 eggs/mL, on average, and a total of six spawns were collected from the 1:1 treatment over the 96-h experimental period. Eggs were collected from all of the tanks on two consecutive days. Eggs were collected from two of the three replicate tanks on two consecutive days in the

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TABLE 2. Mean ± SE egg production (number of eggs) per female (72- and 96-h spawns), total egg production per female, total egg production per gram female body weight (eggs/g BW), and fertilization success for Alewives stocked in 1:1 and 1:3 (female : male) sex ratios. Different letters within columns denote significant differences (P < 0.05). Fertilization was not statistically analyzed due reduced spawning frequency in the 1:3 treatment.

Sex ratio (F:M)

Eggs/female (72 h)

Eggs/female (96 h)

Eggs/female (total)

Eggs/g BW (total)

Fertilization rate (%)

1:1 1:3

25,608 ± 8,129 z 20,944 ± 18,293 z

4,488 ± 3,113 z 8,624 ± 8,997 z

30,096 ± 6,260 z 29,568 ± 15,388 z

171 ± 60 z 174 ± 155 z

83.2 ± 2.0 80.3 ± 9.2

1:3 treatment over the 96-h time period. Differences in total egg production per female (P = 0.9762), total egg production per gram female body weight (P = 0.9791), egg production per female (72 h) (P = 0.7072), and egg production per female (96 h) (P = 0.4936) were not significantly different between the two treatments investigated (Table 2). Mean fertilization could not be evaluated statistically as eggs were only spawned in two replicates in the 1:3 ratio treatment. Mean fertilization values are reported in Table 2 for descriptive purposes only. Juvenile Salinity Growth Experiment Alewives.— No significant differences in growth parameters were detected among any of the treatment salinities throughout the course of the experiment. Final mean ± SE TL and weight ranged from 164 ± 1 to 166 ± 1 mm and from 43.8 ± 0.5 to 45.2 ± 0.6 g, respectively. A narrow range of SGRwt values (2.01 ± 0.01% to 2.05 ± 0.02%) with no significant differences (P = 0.4962) were observed among treatment groups (Table 3). Alewives exhibited high efficiency (FCR < 1) in conversion of feed into biomass independent of environmental salinity, but the FCR in 15‰ was significantly lower than that in the 0‰ (P = 0.0081) and 30‰ (P = 0.0430) treatments (Table 3). Survival of Alewives raised in 15‰ salinity (100%) was significantly (P = 0.0164) higher than for Alewives raised at 0‰ (95.6 ± 0%; Table 3). No differences were detected in most water quality conditions among treatments and thus data were pooled (temperature, 19.8 TABLE 3. Mean ± SE survival, feed conversion ratio (FCR), and specific growth rate (SGRwt ) for Alewives and Blueback Herring cultured at three different salinities over 87- and 47-d experimental periods, respectively. Different letters within columns and unique to species denotes significant differences (P < 0.05).

Salinity (‰) 0 15 30 3 15 30

Survival (%)

FCR

Alewife 95.6 ± 0.0 y 0.98 ± 0.00 y 100.0 ± 0.0 z 0.94 ± 0.01 z 98.9 ± 0.6 zy 0.97 ± 0.01 y

SGRwt (%) 2.03 ± 0.03 z 2.05 ± 0.02 z 2.01 ± 0.01 z

Blueback Herring 95.6 ± 0.6 z 1.31 ± 0.08 z 1.97 ± 0.06 y 98.1 ± 1.2 z 1.07 ± 0.05 zy 2.23 ± 0.03 z 99.4 ± 0.6 z 1.11 ± 0.03 y 2.25 ± 0.06 z

± 0.1◦ C; DO, 6.7 ± 0.1 mg/L; TAN, 0.12 ± 0.01 mg/L; and nitrite, 0.315 ± 0.058 mg/L). Significant differences (P < 0.0001) in pH (7.70 ± 0.01–7.97 ± 0.02) among treatments were not considered to be biologically relevant. Blueback Herring.— No significant differences in growth metrics were detected among any of the treatment salinities at day 26 of the experiment. At the conclusion of the experiment (47 d), final mean ± SE TL (144 ± 1 mm) and weight (27.9 ± 0.6 g) of fish in the 3‰ treatment were significantly lower than those in the 15‰ and 30‰ treatments (P < 0.0001). Fish in the 3‰ treatment also had a lower SGRwt (1.97 ± 0.06%; P = 0.0094) than fish in the 15‰ (2.23 ± 0.03%) and 30‰ (2.25 ± 0.06%) treatments (Table 3). No differences in survival were detected among any of the treatments (P = 0.0570; Table 3). The highest FCR (1.31 ± 0.08) found in the 3‰ treatment was significantly higher than that in the 15‰ treatment (1.07 ± 0.05; P = 0.0410; Table 3). No differences were detected among treatment salinities for temperature and TAN and thus water quality data were pooled (mean experimental values: temperature, 20.0 ± 0.1◦ C; TAN, 0.09 ± 0.01 mg/L). Significant differences (P < 0.0003) in DO, pH, and nitrite were identified among treatments; however, these results were not considered biologically relevant with ranges of 6.43 ± 0.12 to 7.08 ± 0.08 mg/L (mean ± SE) for DO (>75% saturation), 7.74 ± 0.03 to 8.05 ± 0.02 for pH, and 0.119 ± 0.020 to 0.342 ± 0.058 mg/L for nitrite. Acute Salinity Transfer Complete (100%) 48-h survival was observed for both species when fish were acutely transferred from all salinity treatments into water at 15‰ and 30‰ salinity (Table 1). Bluebacks transferred from 3, 15, and 30‰ into 3‰ salinity also exhibited high survival (>93%). Alewives transferred from 0‰ to 0‰ (control) exhibited significantly (P = 0.0004) higher survival than those transferred from salinities of 15‰ into 0‰ (10.0 ± 5.8%) or 30‰ into 0‰ (3.3 ± 3.3%) Gradual Salinity Acclimation No differences in survival were detected for Alewives (P = 0.7571) or bluebacks (P = 0.6372) following low-range gradual acclimation. Survival of Alewives and Blueback Herring for all salinities was greater than 98% and 94%, respectively. No significant differences in survival were also found among



FIGURE 3. (A) Blueback Herring presenting with nodular fibrosis (arrow) resulting from chronic trauma and ulceration. (B) Hematoxylin and eosin stained section of nodular fibrosis (nf), normal tissue (nt), and epidermal ulceration (u). Scale bar = 500 µm.

high-range salinity treatments (Alewives: P = 0.3977; bluebacks: P = 0.5411). Mean ± SE survival rates were 76.0 ± 3.1%, 69.3 ± 7.5%, and 64.7 ± 4.8% for Alewives and 90.0 ± 4.2%, 92.7 ± 1.8%, and 95.3 ± 0.7% for bluebacks at 15, 20, and 30‰ salinities, respectively.

River Herring Health Assessment A nodular growth was found on 3.7% and 10.1% of the cultured Alewives and Blueback Herring, respectively. Histopathology revealed irregular, nodular proliferation of granulation tissue and areas of epidermal ulceration. Growths were diagnosed as nodular fibrosis with bony proliferation resulting from fibroplasia following trauma and ulceration (Figure 3). No evidence of atypia or infectious agents was noted.

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DISCUSSION In this study both Alewives and Blueback Herring were successfully spawned and cultured in standard recirculating aquaculture systems using techniques developed for other marine and anadromous species. Based on the survival, feed conversion, and specific growth rates observed during this investigation, these techniques appear suitable for mass rearing of river herring species for stock enhancement and baitfish production. Both Alewives and Blueback Herring acquired during their spawning migration batch-spawned when held in relatively small (1,800 L) tanks. Blueback Herring, however, spawned in the tanks volitionally and were sometimes able to be manually spawned, while Alewives required hormonal induction for spawning in tanks. Spawning success was also reported with other clupeids such as the American Shad Alosa sapidissima (Mylonas et al. 1995) and Pacific Herring Clupea pallasii (Kreiberg et al. 1987) following exogenous gonadotropinreleasing hormone analog (GnRHa) administration. Differences in the natural life histories of river herring species may explain the differences in captive spawning requirements. The temporal and spatial preferences for each vary throughout the spawning range (Chittenden 1972; Loesch 1987; O’Connell and Angermeier 1997; Walsh et al. 2005). While both species have been found to spawn in lentic and lotic environments, in the Northeast where they are more sympatric they exhibit greater spatial segregation. Alewives prefer lentic spawning environments and migrate farther upstream to freshwater pools and ponds, while Blueback Herring often remain in lotic environments. In New Hampshire, bluebacks arrive in the spawning rivers later than Alewives, are less likely to ascend fish ladders, and have been observed to spawn below the head of tide (Chittenden 1972; Loesch 1987; Sullivan, personal communication). The closer proximity to spawning likely precluded the need for hormonal spawning induction in bluebacks while Alewives which were farther from spawning, spatially and temporally, probably lacked the environmental cues to trigger the cascading hormonal events necessary for gamete maturation and spawning behavior. In these studies, no differences in Alewife spawning success were observed between sex ratios of 1:1 (4F:4M) and 1:3 (2F:6M) due to high variability within treatments. Published estimates of Alewife fecundity in the wild range from 11,000–273,900 eggs/female and the high variability was due to different sampling methods and geographic regions (Norden 1967; Jessop 1993). In our spawning trials, approximately 30,000 eggs/female were obtained, but the number of contributing females was not determined. As similar spawning success was also observed with significantly higher broodstock numbers (24F:24M, data not shown), additional research is necessary to optimize broodstock density and sex ratios and to establish methods for predicting an individual female’s reproductive success.


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DIMAGGIO ET AL.

Alewives and Blueback Herring larvae performed well in an artificial culture environment, employing culture conditions and feeding protocols developed for other anadromous species such as Rainbow Smelt Osmerus mordax (Colburn et al. 2012). Larvae of both species began exogenous feeding by 2 DPH, once yolk and oil reserves were exhausted, and required rotifers as a first prey item because of their relatively small gapes. River herring larvae readily consumed rotifers, Artemia, and commercially prepared diets throughout the course of the larval-rearing period, and feeding regimes developed during this investigation provide a framework for commercial production as well as further nutritional studies with river herring larvae. In a preliminary investigation we also demonstrated the feasibility of early weaning by eliminating Artemia feeding and transitioning Alewife larvae directly from rotifers onto prepared commercial diets by 11 DPH (authors’ unpublished data). Although the effects of using this feeding regime on larval survival is still unclear, eliminating Artemia feeding can have a significant cost-saving advantage during the labor-intensive larviculture phase (Ruyet 1989; Yufera et al. 2000). Further studies should focus on optimizing feeding protocols by minimizing the duration and use of live feeds. Alewives and Blueback Herring were capable of adapting to full strength seawater by 50 and 58 DPH, respectively, following gradual acclimation. These results are consistent with those observed in American Shad that tolerate transfers to full seawater (35‰) by 45 DPH (Zydlewski and McCormick 1997). Considering the gradual acclimation (2.5‰) and relatively late developmental stage of the fish (postmetamorphosis), the experimental approach taken in the current studies was very conservative and these species may be saltwater tolerant at a younger age than tested. Although previous studies examined salinity tolerance of juvenile river herring (Stanley and Colby 1971; Chittenden 1972; Christensen et al. 2012), the ontogeny of saltwater tolerance in larvae has not been investigated. Other anadromous species such as the Rainbow Smelt can adapt to saline conditions during their early larval stages, and this may be due to the close proximity of their spawning areas to the estuaries and the short time span for out-migration to occur (Fuda et al. 2007). While Alewives undertake more extensive spawning migrations, bluebacks appear to spawn below the dams in tidal areas in New Hampshire and may thus develop saltwater tolerance earlier in their development. Experiments are currently underway to test this hypothesis. Growth rates (SGRwt ) and feed conversion (FCR) were similar for Alewives and Blueback Herring juveniles raised in both salt water and freshwater, which afford culturists flexibility in production systems and markets. Feed conversion ratios reported in this investigation (FCRs: 0.94–1.31) were considerably lower than values for other marine baitfish species such as Pigfish Orthopristis chrysoptera (FCRs: 2.00–5.90: DiMaggio et al. 2014), Pinfish Lagodon rhomboides (FCRs: 1.70– 3.10: Ohs et al. 2010), and Gulf Killifish Fundulus grandis (FCRs: 1.77–3.10: Phelps et al. 2010). Moreover, the observed

conversion efficiency and growth rates for both river herring species is encouraging as growth trials were terminated when fish had attained market size (∼150 mm). Both species also exhibited 100% survival when transferred from low (0‰ and 3‰) to high (15‰ and 30‰) salinity water. This osmoregulatory plasticity is beneficial as river herring cultured in freshwater could forgo an acclimation period prior to sale as a marine bait. Collectively, these studies demonstrate the potential of reducing costs by culturing these fish in freshwater recirculating systems and then using them as high-value baitfish in marine systems. While Blueback Herring survived well when directly transferred from high to low salinity conditions, Alewives experienced significant mortality. The inability of Alewives to survive transfers to 0‰ salinity indicates an impairment of hyperosmoregulation and is similar to results observed with juvenile American Shad that experienced 50% mortality when transferred from 12‰ to 0‰ salinity (Zydlewski and McCormick 1997). Detailed analysis of the osmoregulatory physiology of freshwater- and saltwater-adapted Alewives has been reported previously (Christensen et al. 2012), but similar studies with bluebacks have not been published. The disparate results that we observed may reflect differences in osmoregulatory mechanisms between these species or highlight the benefits of supplying low salt levels (3‰) during acute transfer. The nodular fibroses observed on the mouths of both Alewives and Blueback Herring were not pathogenic but inhibited feeding in severe cases. The nodules likely resulted from nonspecific reactions to superficial wounds caused by collisions with the tank walls. Similar growths have been observed in other species of schooling fish raised in captivity (Inga Sidor, UNHVDL, personal communication). Alterations in the hydrodynamics and stocking densities of culture tanks may help to reduce the incidence of this condition but further research is necessary to confirm these hypotheses. In conclusion, these experiments demonstrated that both Alewives and Blueback Herring can be reared in recirculating systems until a desired size is attained for stock enhancement or for use as baitfish. River herring larvae accept diets typical for other marine and anadromous species and juveniles are able to tolerate a wide range of salinities. Further research is necessary to optimize conditions for longterm culture of these ecologically and economically valuable species.

ACKNOWLEDGMENTS The authors acknowledge Aurora Burgess, Catherin Caruso, Calvin Diessner, Kristin Duclos, Amber Litterer, and Tim Breton for assistance with all facets of this investigation. This work was funded by New Hampshire Sea Grant and the New Hampshire Agricultural Experiment Station. This is Scientific Contribution 2602 from the New Hampshire Agricultural Experiment Station.



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