Effects of different feed management treatments on water quality for Pacific white shrimp Litopenaeus vannamei

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1 DOI: /are ORIGINAL ARTICLE Effects of different feed management treatments on water quality for Pacific white shrimp Litopenaeus vannamei Lauren N Jescovitch Carter Ullman Melanie Rhodes Donald Allen Davis School of Fisheries, Aquaculture and Aquatic Sciences, Auburn University, Auburn, AL, USA Correspondence Lauren N Jescovitch, School of Fisheries, Aquaculture and Aquatic Sciences, Auburn University, Auburn, AL, USA. lzj0016@auburn.edu Funding information United Soybean Board, Grant/Award Number: Abstract Increasing feeding rates may provide an increase in production, thus nutrients such as nitrogen, phosphorus and organic matter will also increase. These nutrients promote a greater oxygen demand and concentrations of toxic metabolites which can lead to frequent problems with low dissolved oxygen and an abundance of bluegreen algae. Four feed management practices were evaluated among sixteen 0.1 ha ponds culturing Pacific white shrimp (Litopenaeus vannamei). Feeding treatments included hand feeding using the Standard Feeding Protocol (SFP), SFP plus 15% from 8 to 16 weeks, an automatic-solar timer which fed SFP+15%, and an AQ1 acoustic demand feeder allowing up to 12 kg/daypond based on shrimps feeding response. Samples were analysed at weeks 0, 4 and 8 16 for the following parameters: chlorophyll a, total ammonia nitrogen, nitrite nitrogen, nitrate nitrogen, total nitrogen, total phosphorus, soluble reactive phosphorus, total suspended solids, total suspended volatile solids, turbidity, conductivity, salinity and biological oxygen demand. Samples were collected and shipped overnight to Auburn, Alabama for offsite analysis. On-site water quality was also obtained at the farm. The AQ1 acoustic demand feeder produced the most shrimp with a yield of 4,568 kg/ha; however, the AQ1 also had the highest total ammonia nitrogen and nitrite nitrogen levels late in the growing season. The AQ1 feeder may be a viable, reduced labour and cost alternative for the shrimp commercial industry; however, such technologies must also be matched to the ability of the production system to process nutrients. KEYWORDS automatic feeding, feeding techniques, Pacific white shrimp, timed feeding, water quality 1 INTRODUCTION Litopenaeus vannamei accounted for 80% of the 4,580,770 tonnes of global shrimp production and had a value of $18M (FAO Stat, 2014). Feed is typically one of the largest variable costs in aquaculture and proper application of feed has been shown to have significant reductions in the production costs (De Silva, 1989). In order for farmers to produce shrimp competitively, feeding should be closely monitored and optimized in order to improve returns on the production. Not only is the cost of the feed expensive, but the labour associated with feeding as well. Manual labour efforts exert time and money to feed shrimp periodically through the day which could be spent elsewhere on the farm. Automatic, timer feeders have been successful in reducing the time and energy devoted to feeding while increasing the number of daily feedings. Automatic feeders include possibilities such as monitoring/collecting data, solar triggered, timed, acoustic feedback and much more. Feeders with automated feedback loops, have the potential to feed shrimp at a more optimal rate by only applying feed during periods of active feeding. Efficient feed management practices are critical to improve production and minimize environmental impacts, such as deteriorated water quality. Farmers need to monitor water quality, so that they can John Wiley & Sons Ltd wileyonlinelibrary.com/journal/are Aquaculture Research. 2018;49:

2 JESCOVITCH ET AL. 527 observe trends in changes of concentrations and adapt their management practices accordingly. Many water quality parameters are interrelated and interact with each other (Xu & Boyd, 2016), and changes in one variable give insight about changes in a related variable. Water quality can have severe effects on living organisms if not managed properly. Increasing feeding rates may provide an increase in production; however, nutrient loading of nitrogen, phosphorus and organic matter will also increase. These nutrients promote a greater oxygen demand and concentrations of toxic metabolites which can lead to frequent problems with low dissolved oxygen and an abundance of blue-green algae (Boyd, 2015). Rapid changes in concentration or high levels of some variables are thought to compromise immunocompetence of animals and make them more susceptible to pathogenic organisms (Hargraves & Tucker, 2003). Consequently, there is considerable interest in connecting the effects of feed management to water quality. This study evaluates the use of intensified feeding strategies that could be adopted by farmers in respect to water quality. 16-week culture period. SFP and SFP+15 treatments were fed, by hand, twice daily (08:00 and 16:00 hours). The solar-timed feeder fed six feedings per day (08:00, 10:00, 12:00, 14:00, 16:00, 18:00 hours) and was intended to feed according to the SFP. Mechanical problems caused the solar-time feeders to feed an amount similar to the SFP+15%. AQ1 acoustic demand feeder was set to a limit 12 kg/daypond based on shrimp feeding response and allowed feeding between 07:00 and 19:00 hours. AQ1 treatments were constrained to a power supply, so these treatments were not randomly assigned to ponds; however, the SFP and SFP+15 treatments were randomly assigned to the remaining ponds. Shrimp were fed using a high-soy sinking feed (35% CP and 7% Lipid) manufactured by Zeigler, Inc. (Gardners, PA, USA); this is an open formula (D. Allen Davis, personal communication). Each feeding protocol outlined above was evaluated by a series of water quality analyses over a 16-week grow-out season; with feeding treatments starting at week 4. Shrimp were harvested during week 16 in September MATERIALS AND METHODS Four feed management techniques were evaluated among 16 ponds culturing Pacific white shrimp (L. vannamei) at the Alabama Department of Conservation and Natural Resource Division Claude Peteet Mariculture Center, Gulf Shores, Alabama. 2.1 Experimental design Litopenaeus vannamei postlarvae were obtained from Shrimp Improvement Systems, Islamorada, FL, USA on May 11, After a 2-week nursery period, the juvenile were quantified, harvested and distributed into culture ponds at 17.2 shrimp/m 2. Grow-out ponds were approximately 0.1 ha in surface area, lined (1.52 mm high-density polyethylene lining), with a 25-cm layer of sandy-loam soil on the bottom. All ponds were supplied with mechanical aeration (Air-O-Lator, Kansas City, MO, USA) and supplemental 1 or 2 hp Aire-O 2 (Air-O 2, Aeration Industries International, Inc. Minneapolis, MN, USA) if DO dropped below 3 mg/l. Supply water was brackish (11 13 g/l) from the Intracoastal Canal between Mobile Bay and Perdido Bay, Alabama and was filtered through a 250 lm sock. 2.2 Feed management treatments Four treatments methods were evaluated: a manual-standard Feeding Protocol (SFP), manual-sfp that included a 15% increase (SFP+15%) in daily ration for the final 8 weeks of growth, automatic-solar-timed feeder (FIAP, Ursensollen, Germany) using the same ration as the SFP+15 and automatic- AQ1 SF200 acoustic feeder (AQ1 Systems, Tasmania, Australia) fed ad libitum using a hydrophone and computer software to monitor feeding activity. The SFP was calculated with a predicted growth of 1.3 g/week, and a feed conversion ratio (FCR) of 1.2, assuming a survival rate of 75% over 2.3 On-site analyses Water samples were collected before morning feeding and analysed weekly for total ammonia nitrogen (TAN) using an Orion ammonia electrode probe (Thermo Fisher Scientific Inc., Waltham, MA, USA) and Secchi disk visibility. Measurements of temperature, dissolved oxygen, ph and salinity were recorded three times a day (05:00, 14:00, 19:00 hours) using a YSI ProPlus meter (Yellow Spring Instrument Co., Yellow Springs, OH, USA). To draw comparison between all water quality analyses, data were only used from the same weeks as when water was shipped for off-site analysis (described in Section 2.2). Shrimp sampling was conducted weekly using two, fivefoot casting nets (monofilament net, 1.22 m radius and 0.95 cm opening) to catch approximately 60 shrimp in each pond to determine weight and diagnose health. Weekly feed inputs as well as final production were also recorded. 2.4 Off-site analyses Water samples were collected in the afternoon during YSI check (weeks 0, 4 and 8 16) and shipped overnight, on ice, to the E.W. Shell Fisheries Center at Auburn University for off-site analysis. Samples were analysed using standard analytical protocols for chlorophyll a by membrane filtration, acetone methanol extraction of phytoplankton and spectroscopy (Eaton, Clesceri, Rice, & Greenberg, 2005); TAN by the salicylate method (Bower & Holm-Hansen, 1980; Le & Boyd, 2012), nitrite nitrogen by the diazotization method (Boyd & Tucker, 1992), nitrate nitrogen by the szechrome NAS reagent method (Van Rijn, 1993), total nitrogen and total phosphorus by ultraviolet spectrophotometric screening method and ascorbic acid methods, respectively, following digestion in potassium persulphate solution (Eaton et al., 2005; Gross, Boyd, & Seo, 1999); soluble reactive phosphorus by ascorbic acid method (Eaton et al., 2005); total suspended solids and total suspended volatile solids (Boyd & Tucker,

3 528 JESCOVITCH ET AL. TABLE 1 Mean averages of water quality parameters over 16 weeks for SFP, SFP+15, timed and AQ1 feed management treatments for onsite field analysis Parameter SFP SFP+15 Timed AQ1 Secchi Disk (1.26, 17.00) (1.21, 11.33) (1.417, 11.33) (1.21, 11.33) TAN (mg/l) (0, 3.000) (0, 0.500) (0, 4.000) (0, 1.000) Temperature ( C) Morning 29.9 ( ) 30.0 ( ) 29.9 ( ) 30.1 ( ) Afternoon 32.2 ( ) 32.0 ( ) 32.1 ( ) 32.1 ( ) Night 32.1 ( ) 32.1 ( ) 32.1 ( ) 32.3 ( ) Dissolved oxygen (mg/l) Morning 4.50 ( ) 4.59 ( ) 4.60 ( ) 4.39 ( ) Afternoon 9.86 ( ) 9.07 ( ) 9.25 ( ) 9.14 ( ) Night 8.81 ( ) 8.38 ( ) 8.02 ( ) 8.00 ( ) ph Morning 8.02 ( ) 8.04 ( ) 7.95 ( ) 7.98 ( ) Afternoon 9.10 ( ) 8.97 ( ) 8.99 ( ) 8.89 ( ) Night 9.00 ( ) 8.90 ( ) 8.84 ( ) 8.79 ( ) Salinity (g/l) Morning ( ) ( ) ( ) ( ) Afternoon ( ) ( ) ( ) ( ) Night ( ) ( ) ( ) ( ) Values represent the mean SD and values in parenthesis represent minimum and maximum readings. 1992), turbidity by nephelometry (Eaton et al., 2005); conductivity and salinity (Orion 3 Star Probe; Thermo Scientific, Waltham, MA, USA); and biological oxygen demand (Boyd & Tucker, 1992). 2.5 Statistical analysis Data were analysed using SIGMAPLOT version 11.0 statistical software (Aspire Software International, Ashburn, VA, USA). Water quality variables were analysed using the repeated measures, two-way analysis of variance (ANOVA) procedure followed by the Holm Sidak method to determine where differences occurred (p <.05). Pearson Correlation was used for water quality variables that showed differences between treatments versus feed input. The TAN data sets from off-site and on-site analysis were evaluated using a 2-sample t test (p <.001). Production was analysed based on analysis of variance followed by Student Newman Keuls multiple range test. Unfortunately, one each of the time and AQ1 treatment ponds were removed from data analyses due to a low DO-related mortality and feeder malfunction, respectively. 3 RESULTS AND DISCUSSION On-site analyses are shown in Table 1. There were no effects from feeding rate treatment for the water quality (on-site and off-site) parameters measured for the 16-week grow-out period. Off-site analyses are shown in Table 2. All values measured off-site were within acceptable ranges during the 16 week grow-out season (Boyd & Tucker, 1992). There were no treatment effects for the following off-site parameters: chlorophyll a, nitrate nitrogen, total nitrogen, total phosphorus, soluble reactive phosphorus, total suspended solids, total suspended volatile solids, turbidity, conductivity, salinity and biological oxygen demand. However, it should be noted that season variation is a factor contributing to the concentration present in each treatment which should be expected due to the fluctuations in temperature and weather (Boyd, 2015). Both salinity and ph measured were not significantly different at on-site and off-site locations and, besides TAN, were the only parameters that could be accurately measured at both locations. Differences attributed to time of sample collection (not a side-by-side analysis) and parameter analysis may also contribute to no differences between on-site and off-site data for the parameters mentioned above. Juvenile L. vannamei has best survival at salinities between 15 and 25 g/l (Bray, Lawrence, & Leung-Trujillo, 1994); however, Ponce-Palafox, Martinez-Palacios and Ross (1997) reported best survival between 33 and 40 g/l. The current study ranges from 11 to 12 g/l salinity, so it is most comparable to 15 g/l in Lin and Chen (2001) which estimated a 96 h LC50 of mg/l for ammonia-n and 1.20 mg/l NH 3 -N. Safety level for L. vannamei (96-h LC ) was calculated to be 2.44 mg/l ammonia-n and 0.12 mg/l NH3-N. There were differences between the feeding treatments within TAN (off-site) and nitrite nitrogen (Table 3). The TAN was greatest with the AQ1 treatment with concentrations of 1.79 mg/l and 2.35 mg/l for weeks 9 and 14 respectively. During week 10, SFP had 1.40 mg/l TAN which was greater than SFP+15 with 0.03 mg/l. The greatest recording for off-site TAN was during week 14 for AQ1 with 2.35 mg/l TAN; thus, all TAN was within safe concentrations during the present study.

4 JESCOVITCH ET AL. 529 TABLE 2 Mean averages of water quality parameters over 16 weeks for SFP, SFP+15, timed and AQ1 feed management treatments for off-site laboratory analysis Parameter SFP SFP+15 Timed AQ1 Turbidity (NTU) (2.40, 29.20) (1.80, 13.80) (2.80, 47.10) (2.20, 46.70) Total suspended solids (mg/l) (0.0200, ) (0.0240, ) (0.0270, ) (0.0150, ) Total suspended volatile solids (mg/l) (0, ) (0, ) (0, ) (0, ) Conductivity (ms/cm) (13.79, 23.38) (14.14, 23.41) (14.39, 23.49) (14.36, 24.75) Salinity (g/l) (7.90, 13.50) (8.20, 12.20) (8.30, 12.60) (8.30, 12.50) Chlorophyll a (lg/l) (9.7, 916.4) (15.6, 942.5) (15.0, 994.7) (4.4, 498.8) TAN (mg/l) off-site (0, 3.872) (0, 0.890) (0, 3.660) (0, 3.970) Nitrite nitrogen (mg/l) (0, 0.802) (0, 0.082) (0, 0.164) (0, 0.753) Nitrate nitrogen (mg/l) (0, 0.130) (0, 0.190) (0, 0.195) (0, 0.215) Total Nitrogen (mg/l) (0, 7.351) (0, 5.461) (0, 6.353) (0.336, 8.671) Soluble reactive phosphorus (mg/l) (0, 1.178) (0, 1.342) (0, 0.980) (0, 1.431) Total phosphorus (mg/l) (0.192, 1.258) (0.112, 1.477) (0.120, 1.012) (0.105, 1.859) Biological oxygen demand (mg/l) (2.40, 26.84) (1.44, 20.92) (2.64, 22.28) (1.84, 21.12) Values represent the mean SD and values in parenthesis represent minimum and maximum readings. TABLE 3 Significant differences between treatments at specific time periods for total ammonia nitrogen off-site and nitrite nitrogen Parameter SFP SFP+15 Timed AQ1 Total ammonia nitrogen (mg/l) Week a 0.16a 1.33ab 1.79b Week a 0.03b 0.93ab 0.19ab Week a 0.38a 1.11ab 2.35b Nitrite nitrogen (mg/l) Week a 0.00b 0.06ab 0.01b Week ab 0.02a 0.05ab 0.27b Week a 0.01a 0.04a 0.44b Differences shown with letter indicators for values of least square means for treatment versus time (p <.05). Nitrite nitrogen increases were seen during weeks 11, 14 and 15. During week 11, nitrite nitrogen in the SFP treatment measured 0.23 mg/l which was greater than the SFP+15 and AQ1 treatments, but not the timer treatment that was 0.06 mg/l. In week 14, nitrite nitrogen was greater in AQ1 with 0.27 mg/l than the SFP+15 with 0.02 mg/l. AQ1 also had the highest nitrite nitrogen concentration in week 15 with 0.44 mg/l which was different than the other three treatments. Safe levels for L. vannamei juveniles were determined at 10 g/l and 15 g/l salinities with 154 mg/l NO 2 -N (Schuler, Boardman, Kuhn, & Flick, 2010) and 143 mg/l NO 2 -N (Lin & Chen, 2003) respectively. It is possible if we did not limit the AQ1 daily feed input to 12 kg/day the nitrite would have been higher. The TAN and nitrite nitrogen differences follow the time delay of the nitrogen cycle; however, there were no differences found between treatments for nitrate nitrogen as stated above. These differences can be associated with feed input, algae diversity or the waste assimilation capacity of the pond. To determine if these differences were associated to the feed and nutrient input, TAN and nitrite nitrogen values were correlated with weekly feed inputs from weeks 8 16, or when all treatments were currently on-going (total feed inputs are listed in Table 4). SFP+15 and AQ1 TAN concentrations were negatively correlated to feed input with p-value =.014 and r 2 =.187, and p-value =.002 and r 2 =.393 respectively. AQ1 nitrite nitrogen was negatively correlated to feed input with p-value =.002 and r 2 =.406. Because nutrient input should express increased nitrogen (Boyd, 2015), these findings of negative correlations show that there may be an undetermined, hidden factor that caused this relationship. This is an area of study that merits further investigation because of the complexity of interactions between water quality parameters. The TAN was a water quality parameter that was measured using different methods for on-site and off-site analysis. As an unexpected result, TAN on-site and TAN off-site measurements were significantly different over the 16-week grow-out period (Figure 1). The highest concentrations for on-site measurements were during week 10 with SFP and timer treatments; although, the greatest concentrations for off-site were also observed during week 9 and 14. The week 14 observation for the AQ1 treatment would lead to the differences

5 530 JESCOVITCH ET AL. TABLE 4 Growth performance data of Pacific white shrimp cultured in lined earthen ponds for 16 weeks fed using varying feeding strategies, stocked at 17 shrimp/m 2 with a mean initial weight 0.07 g Treatment Yield Final wt. (g) % Survival FCR Weight gain (g) Weight gain (g/week) Biomass (kg) Feed input (kg) %Body wt. Fed Final population Shrimp/ m 2 SFP 3,068.5 a a a 1.47 a a a , SFP+15% 3,032.5 a a a 1.54 a a a , Timed 3,294.3 a b b 1.79 b a a , AQ1 4,568.8 b c c 2.24 c b b , p-value.0016 < <.0001 < < PSE SFP, standard feeding protocol; PSE, pooled standard error. Values represent means (n = 4). Values in the same column with different superscripts are significantly different (p <.05) based on analysis of variance followed by Student Newman Keuls multiple range test. FIGURE 1 Total ammonia nitrogen on-site and off-site comparison using averages for standard feeding protocol (SFP), SFP+15, timed and AQ1 feed management treatment found for nitrite nitrogen per the nitrogen cycle as discussed above. The multiple data points for the treatments in the off-site show that these elevated concentrations were more accurate than the on-site values measured with a probe. Zhou and Boyd (2016) stated that the use of the ammonia ion selective electrode is strongly affected by sodium and potassium, thus the electrodes are not recommended for waters with high salinity. However, researchers still use and rely on TAN measurements using an ion selective probe in seawater (Morris, Samocha, Davis, & Fox, 2011; Ray & Lotz, 2017). Differences in the present study could be due to probe failure or improper calibration, analytical error, human error, contamination, etc. It should be noted that TAN may fluctuate over time during collection/shipping of samples; however, this should not vary as much as it did between on-site and of-site data. Algae die-offs had also occurred periodically; however, the exact dates of these episodes were not recorded. Unexpected results in TAN on-site and off-site merit further investigation for a side-by-side analysis of both methods for further information. Despite the differences found between methods, both on-site and off-site samples showed increased TAN concentrations in the AQ1 treatment compared to the other feeding treatments. Nevertheless, production and growth performance was significantly greater with the AQ1 treatment reaching a yield of 4,568.8 kg/ha (Table 4). According to Tacon, Nates and McNeil (2005), standard production is around 1,000 3,000 kg/hayear for L. vannamei in semi-intensive outdoor farms. Due to the higher final biomass and the increased feed inputs, this system should require continuous system monitoring and feedback to provide appropriate and timely actions associated when water quality starts to deteriorate (Tacon, Jory, & Nunes, 2013). Future research would include pushing the waste assimilation capacity of the ponds with greater densities and feed inputs because the current study was done below carrying capacity for the ponds. For instance, Sookying, Silva, Davis and Hanson (2011) found that higher stocking density (17, 26, 35 and 45 shrimp/m 2 ) resulted in greater yield with final production between 2,660 and 6,149 kg/ha at the same location as the current study, which had the greatest yield of 4,569 kg/ha with the AQ1 treatment. 4 CONCLUSION Feeding treatment practices determine production and water quality for shrimp ponds. With a reduced-labour management practice, the AQ1 has a high initial investment, but has clear increased growth

6 JESCOVITCH ET AL. 531 performance for Pacific white shrimp. The AQ1 treatment can have high TAN and nitrite production later in the season, but the SFP and timer treatments will have these high productions of TAN and nitrite 2 3 weeks after strict feeding management is introduced. The AQ1 is likely to have higher feed inputs, thus higher loading rates which should be considered during water quality analyses. Even though TAN and nitrite were elevated for the AQ1 system, these concentrations were still within safe concentrations for Pacific white shrimp at 17 shrimp/m 2 with a feed input limited to 12 kg/daypond. AQ1 acoustic feeding is recommended as a viable reduced-labour feeding management, but water quality needs to be supplemented with appropriate aeration and maintaining buffer capacity to reduce potential ammonia and nitrite toxicity-effects as discussed above. The initial investment of the AQ1 acoustic feeders may be off-set with the potential in production. Based on the observations from the present study, the use of TAN probes resulted in different results and may be less reliable than traditional wet chemistry methods. In the current study, there were no blind controls to confirm the accuracy and precision of either method. However, evaluation of the salicylate method in the laboratory has been promoted and deemed as a standard water quality analysis. Farmers should be wary of using a TAN probe when ammonia concentrations are high. Further research with a side-byside comparison of TAN methods used in this study with greater stocking densities would prove valuable. ACKNOWLEDGMENTS The authors would like to show appreciation to those who have critically review this manuscript as well as those that helped, especially Romi Novriadi, Thomas Derbes II, Sirirat Chatvijitkul, and Mike Loop, in supporting this study at the Claude Peteet Mariculture Center, Alabama Marine Resources Division (Gulf Shores, Alabama, USA). 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Comparison of Nessler, phenate, salicylate and ion selective electrode procedures for determination of total ammonia nitrogen in aquaculture. Aquaculture, 450(1), How to cite this article: Jescovitch LN, Ullman C, Rhodes M, Davis DA. Effects of different feed management treatments on water quality for Pacific white shrimp Litopenaeus vannamei. Aquac Res. 2018;49: