Received: 15 July 2020 Revised: 18 October 2021 Accepted: 20 October 2021 DOI: 10.1111/jwas.12865 APPLIED STUDIES Effect of transportation time and stocking density on seawater quality and survival of Anisotremus scapularis (Perciformes: Haemulidae) Luis A. Espinoza-Ramos1 | Renzo Pepe-Victoriano2 | Manuel Nande3 Jordan I. Huanacuni1 1 Facultad de Ciencias Agropecuarias, Escuela | Profesional de Ingeniería Pesquera, Abstract Universidad Nacional Jorge Basadre The transport of live fish for aquaculture is a key issue in Grohmann, Tacna, Peru the domestication of new species. National level programs 2 Facultad de Recursos Naturales Renovables, Universidad Arturo Prat, Area de Biología were developed in Peru for controlled repopulation of Marina y Acuicultura, Arica, Chile Peruvian grunt (Anisotremus scapularis), reared in extensive 3 CIIMAR/CIMAR—Interdisciplinary Centre of Marine and Environmental Research, University of Porto, Matosinhos, Portugal systems or ongrown in floating cages, but these were limited by inadequate knowledge of the best transport parameters to ensure survival. This study aims to identify the Correspondence effect of low-density (21.18 ± 4.38) medium (31.77 ± 6.57) Luis A. Espinoza-Ramos, Universidad Nacional and high-density in (42.36 ± 8.76 kg m3), corresponding to Jorge Basadre Grohmann, Facultad de Ciencias Agropecuarias, Escuela Profesional 6 (48), 9 (72), and 12 (96 indbag1) indL1 during the de Ingeniería Pesquera, Avenida Cusco s/n, transport time (8, 10, and 12 hr), on survival. Also seawater Tacna C.P. 23000, Peru. Email: lespinozar@unjbg.edu.pe temperature, dissolved oxygen, pH, ammoniacal nitrogen (NH3 N), ammonia (NH3), and ammonium (NH4) were Funding information Canon funds for Scientific and Technological Research Projects at UNJBG—Rectoral Resolution No. 3780-2014-UN/JBG. recorded at the end of transport. Survival at 8 and 10 hr at low-density was similar, but decreased at 12 hr. In contrast, all densities showed a greater effect after 12 hr of transport with 61.11 ± 17.35; 67.13 ± 7.13, and 70.49 ± 4.70% survival, respectively. Finally, the influence of the variables analyzed to contribute to survival and the sum of these, plus other parameters that were not measured, such as stress, leads to the conclusion of between 8 and 10 hr of transport time and not exceeding stocking density of 72 ind/bag (31.77 ± 6.57 kg m3) should be used. This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. © 2021 The Authors. Journal of the World Aquaculture Society published by Wiley Periodicals LLC on behalf of World Aquaculture Society. 1042 wileyonlinelibrary.com/journal/jwas J World Aquac Soc. 2022;53:1042–1050. KEYWORDS juvenile, live fish, Peruvian grunt, seawater quality, transport 1 | I N T RO DU CT I O N Peruvian grunt Anisotremus scapularis (von Tschudi, 1846) is a marine fish native to the eastern South Pacific of importance in the artisanal fishery of Peru (Medicina, 2014) with potential for aquaculture (Espinoza-Ramos, ChilliLayme, Pepe-Victoriano, Pino-Choqueapaza, & Contreras-Mamani, 2019; Montes, Castro, Linares, Orihuela, & Carrera, 2019), and exhibits carnivorous bentophage habits forming large shoals (Angel & Ojeda, 2001; Berrios & Vargas, 2004; Ruiz & Wolff, 2011). Peruvian grunt is a coastal fish (Kluger, Scotti, Vivar, & Wolff, 2019; Kluger, Taylor, Mendo, Tam, & Wolff, 2016) found at moderate depths (Alaica, 2018) which inhabits in the intertidal and subtidal rocky area (Angel & Ojeda, 2001; Berrios & Vargas, 2004; Salazar et al., 2018). The fish distribution includes Ecuador, Peru, and Chile (Castro-Romero & Muñoz, 2011; Chirichigno & Cornejo, 2001; Froese & Pauly, 2019; Gárate & Pacheco, 2004). The experimental culture of A. scapularis in Peru is expanding because of the great potential, among other factors, to its high conditioning capacity, adaptability to handling, and reduced mortality in the larval stage (Espinoza-Ramos et al., 2019). However, the growth of juveniles to commercial size remains one of the main obstacles to their exploitation in the commercial sector (Dionicio-Acedo, Rosado-Salazar, Flores-Mego, FloresRamos, & Aguirre-Velarde, 2017). New studies of the juvenile growing in floating cages or semi-extensive estuaries are necessary to optimize this phase and reduce costs. Likewise, the incorporation of a new species involves the creation of broodstock from juveniles from different areas. To guarantee the success of these new strategies, it involves the transport of live fish from the hatchery to the place where they will be transferred, avoiding economic losses (Piper et al., 1982). Sometimes fish transport results in mortality at or after seeding because of poor physiological conditions or haul stress (Emmanuel, Fayinka, & Aladetohun, 2013; Gomes et al., 2003; Islam & Hossain, 2013; Ross & Ross, 2008; Weber, Peleteiro, Martín, & Aldegunde, 2009). Therefore, maintaining seawater quality parameters during transport, such as dissolved oxygen (OD), pH, temperature, salinity, carbon dioxide, alkalinity, ammoniacal nitrogen (NH3 N), ammonia (NH3), and ammonium (NH4), is essential in the successful transport of live fish (Belema et al., 2017; Metar et al., 2018). The pH in seawater is related to higher metabolic activity and carbon dioxide production by fish during transport (Watson, Kilgore, & Martinez, 2010). Also, one of the leading causes of death of fish transported in bags is the accumulation of concentrations of ammonia (Barbieri & Bondioli, 2015; Watson et al., 2010). Therefore, the increase in the concentration of waste metabolites could be proportional to the stocking density and transport time into the bags for this species (Lim, Dhert, & Sorgeloos, 2003). Although A. scapularis is doing an effective transition to aquaculture (Espinoza-Ramos et al., 2019), culture, and transport parameters have not yet been standardized. For this reason, Rosado, Dionicio, and AguirreVelarde (2016) performed transport simulations of A. scapularis juveniles with the sedative tricaine MS-222; however, further studies are still required, such as oxygen consumption, transport density, transport hours, fasting time, preparation temperature, transport and arrival, testing sedative types, and concentrations, and others, all, to determine the density and adequate time for transporting of A. scapularis juveniles. Therefore, we hypothesize that time and stocking density affect seawater quality during the transport of juvenile Peruvian grunts and their survival. In order to check our hypothesis, the objective of the present study was to evaluate the effect of stocking density and transport time of juvenile A. scapularis, analyzing key parameters (seawater temperature, dissolved oxygen, pH, ammoniacal nitrogen (NH3 N), ammonia (NH3), and ammonium (NH4) during transport and their effect on survival. 17497345, 2022, 5, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/jwas.12865 by UGTO - Universidad de Guanajuato, Wiley Online Library on [19/09/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License 1043 ESPINOZA-RAMOS ET AL. 2 2.1 ESPINOZA-RAMOS ET AL. MATERIALS AND METHODS | | Conditioning Peruvian grunt (A. scapularis) juvenile were cultivated at the Morro Sama Aquaculture Center, the specimens were conditioned in three Australian type tanks of 10 m3 volume for 10 days at 16.2 ± 0.87 C, 7.1 ± 0.25 mg L1 of dissolved oxygen and natural photoperiod with open seawater through-flow system (2 L s1). Previous biometric selection of juveniles reared in the Morro Sama aquaculture center facilities was carried out (individual range 6.48 ± 0.43 cm of total length and 3.53 ± 0.73 g of wet weight). They were fed five times a day with artisanal food composed of 52.3% protein, 14.5% lipids, 8.8% moisture, 12.7% ash, and 1.2% crude fiber. The juveniles of A. scapularis were fasting 24 hr, to ensure intestinal emptying. 2.2 | Transport and sampling The fish were randomly deposited in 24-L volume polyethylene bags (N = 27) with 8 L of sterilized seawater, filtering at 1 μm filter cartridge and UV treatment (AL-PVC-160 W, American Ultraviolet, IN), at low-density (LD, 21.18 ± 4.38), medium (MD, 31.77 ± 6.57), and high density in (HD, 42.36 ± 8.76 kg m3), corresponding to 6 (48), 9 (72), and 12 (96) indL1 (total individual per bag). Oxygen was injected into the bags until completing the 2/3 of 24 L of total capacity of each one of them and hermetically closed by using cable ties. Each bag was placed in 42 42 39.5 cm isothermal boxes, technopor code 554 (Consorcio Disarguesa, Lima, Perú). Each density was evaluated in triplicate at 8, 10, and 12 hr of transportation. 2.3 | Physico-chemical parameters The initial concentrations of physical–chemical parameters of seawater were measured for each bag without fish. After transport for each time (N = 3) and stocking density (N = 3) per triplicate (total bags, N = 27), the same parameters were measured. Once each bag was opened, dead fish were removed, then the live ones were conditioned in 10 m3 tanks. Parameters such as seawater temperature and dissolved oxygen were measured using YSI-550A oximeter and the pH with the Ecosense-pH100A pH meter (YSI, Yellow Springs, OH). In addition, the analysis of ammoniacal nitrogen (NH3 N), ammonia (NH3 ), and ammonium (NH4) using the HACH Company Portable Colorimeter System by Neesler Ammonia analysis adapted from Standard Methods for the Examination of Water and Wastewater (Method No. 8038, HATCH), the samples were evaluated at 425 nm with the DR-400 HACH spectrophotometer kit (0.000–2.500 mg L1 ; Hach., 2003) of initial seawater and after transport of fish. 2.4 | Survival Survival of A. scapularis juveniles was calculated at the end of the experiment using the following formula: Survival ð%Þ ¼ Nf 100 Ni where Nf is the number of final fish alive at the end of the transport experiment and Ni is the number initial fish (Wang, Zhang, Liu, Adányi, & Zhang, 2020). 17497345, 2022, 5, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/jwas.12865 by UGTO - Universidad de Guanajuato, Wiley Online Library on [19/09/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License 1044 2.5 1045 Statistical analysis | All data were tested for normality by Shapiro–Wilk's test and homogeneity of variance by Levene's test before analysis. Survival and physicochemical parameters data at the end of the experiments were compared by two-factor ANOVA and (post hoc) Tukey to identify significant differences between treatments (p < .05) (Zar, 2010). Statistical analyses were performed in STATISTICA 10.0 statistical package (StatSoft, Tulsa, OK). A principal component analysis (PCA) was performed to evaluate the relationship between density during each transporting time with variables as temperature (Tª), ammoniacal N (NH3 N), ammonia (NH3), and ammonium (NH4), pH, dissolved oxygen (O2), and survival. 3 RESULTS | 3.1 Physico-chemical parameters | Seawater temperature at the end of all experimental treatments increased 2 C of mean (range of 16.87–17.67 C) compared to the initial temperature (15.96 ± 0.25 C; Table 1). Seawater temperature was not affected, depending on the transport time with the analyzed densities (F = 0.20, p = .927), however, the temperature showed significant differences at times (F = 6.9, p < .005) and densities (F = 9.8, p < .001) independently evaluated. Dissolved oxygen in seawater at the end of the transport also increased significantly for all treatments compared to the initial value (5.95 ± 0.85 mg L1). The dissolved oxygen concentration was not different, depending on the transport time, with the densities analyzed (F = 2.16, p = .115), however, it is significantly different to LD, MD, and HD (F = 9.90, p < .001). The pH (F = 3.6, p = .024), concentrations of ammoniacal nitrogen (F = 35.77, p < .000) and ammonia (F = 93.09, p < .000) were affected by the density, the transport time, and the interaction of both variables. The ammonium concentration did not show significant difference in all the experimental treatments (F = 1.04, p = .416; Table 1). The first principal component (F1) describes the fish density and explains variable clustering in 65.48%, while variable two (F2) represent the transport time and explains 25.92%. The results obtained in the PCA showed a direct grouping between toxic metabolites such as ammoniacal N (NH3 N), ammonia (NH3), and ammonium (NH4). Also, pH and dissolved oxygen parameters were clustered, temperature and survival were represented separately (Figure 1). 3.2 | Survival Survival was not different, among the densities analyzed (F = 1.60, p = .218), however, it is significantly different at transport time evaluated (F = 50.41, p < .000). Consequently, the highest survival percentages were obtained (Figure 2) in treatments performed at 8 hr (95.83, 100.00, and 97.92%) and those less than 12 hr (61.11, 67.13, and 70.49%). 4 | DISCUSSION The results of this study show the first approach to changes in seawater quality during the transportation of three densities (LD, MD, and HD) of Peruvian grunt for a short period (8 hr) and two long periods (>8 hr) according to Sampaio and Freire (2016). Changes in seawater quality affect fish physiological response during transport time, causing stress and high mortality rates (Lim et al., 2003). However, some marine species could tolerate the higher ranges of 17497345, 2022, 5, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/jwas.12865 by UGTO - Universidad de Guanajuato, Wiley Online Library on [19/09/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License ESPINOZA-RAMOS ET AL. TABLE 1 scapularis ESPINOZA-RAMOS ET AL. Physicochemical parameters at the beginning and the end of transport of juveniles of Anisotremus Treatments Seawater SD Dissolved Time (hr) (ind/bag) temperature ( C) oxygen (mg L1) pH Ammoniacal Ammonia nitrogen (μg L1) (μg L1) Beginning 1.17 ± 0.38 8 10 12 15.96 ± 0.25 LD (48) 5.95 ± 0.85 17.17 ± 0.06abc 13.21 ± 1.09ab 7.65 ± 0.10 Ammonium (μg L1) 1.21 ± 0.02 1.29 ± 0.03 6.43 ± 0.07a 2.35 ± 0.13d 2.84 ± 0.14e 3.12 ± 0.10g MD (72) 17.37 ± 0.12abc 11.68 ± 0.74ab 6.36 ± 0.03a 5.00 ± 0.04bc 6.05 ± 0.05bc 6.45 ± 0.05d HD (96) 17.67 ± 0.12a 11.24 ± 0.08b 6.21 ± 0.08b 4.80 ± 0.10bc 5.69 ± 0.01c 6.07 ± 0.03d LD (48) 17.13 ± 0.06abc 16.40 ± 0.79a 6.37 ± 0.06a 4.25 ± 0.06bc 5.14 ± 0.00d 5.48 ± 0.00f MD (72) 17.33 ± 0.12 abc 11.48 ± 1.22ab 6.22 ± 0.04b 5.00 ± 0.23bc 6.05 ± 0.07bc HD (96) 17.47 ± 0.06ab 6.12 ± 0.03b 8.20 ± 0.20a 9.92 ± 0.02a LD (48) 16.87 ± 0.12c 6.45 ± 0.03d 10.58 ± 0.08a 14.04 ± 3.50ab 6.22 ± 0.04b 5.31 ± 0.07b 6.46 ± 0.31b 6.85 ± 0.20c 14.04 ± 1.30ab 6.21 ± 0.04 b 7.95 ± 0.70a 9.62 ± 0.50a 10.26 ± 0.10b 17.30 ± 0.53abc 11.41 ± 1.37ab 6.15 ± 0.01b 8.34 ± 0.16a 10.10 ± 0.15a 10.77 ± 0.07a MD (72) 17.00 ± 0.17bc HD (96) 9.80 ± 3.00b Note: Different letters through the same column indicate significant differences (two-way ANOVA; n = 3; p < .05; g < f < e < d < c < b < a). Abbreviations: HD, high density; LD, low density; MD, medium density; SD, stocking densities. F I G U R E 1 Principal component analysis (PCA) showed the relationship between low (21.18 ± 4.38), medium (31.77 ± 6.57), and high-density (42.36 ± 8.76 kg m3) of juvenile Peruvian grunt in each transporting time (8, 10, and 12 hr) exposed variables as temperature (Tª), ammoniacal N (NH3 N), ammonia (NH3), ammonium (NH4), pH (pH), dissolved oxygen (O2), and survival toxic compounds without affecting their survival, such as the flathead gray mullet Mugil cephalus (Vagner, Lefrançois, Ferrari, Satta, & Domenici, 2008) and the European sea bass Dicentrarchus labrax (Montgomery, Simpson, Engelhard, Birchenough, & Wilson, 2019). Furthermore, tropical freshwater fish such as the tambacu Colossoma 17497345, 2022, 5, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/jwas.12865 by UGTO - Universidad de Guanajuato, Wiley Online Library on [19/09/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License 1046 1047 F I G U R E 2 Survival of Anisotremus scapularis juveniles at the end of the experiment. Different letters within each transport time treatment indicate significant differences (mean, n = 3, p < .05, d < c < b < a) macropomum Piaractus mesopotamicus also show a high range of tolerance to changes in water quality (Quaresma, Santos, Ribeiro, Leite, & Sampaio, 2020). Our results showed the first screening of biotic and abiotic parameters that affect the modification of seawater quality with different biomass loads. Thus, the starting temperature to which the fish acclimatized (16 C) was the optimal temperature used in the culture of juveniles in this species (Espinoza-Ramos et al., 2019). During transport time, the temperature increased by 2 C, also increasing the metabolism of the fish. Thus, a higher temperature increase in aquatic species (5 C) causes high demand for dissolved oxygen, resulting in ammonia and carbon dioxide accumulation (Svobodová, Lloyd, Máchová, & Vykusová, 1993). A decrease of 5 C implies a reduced metabolism and reduction in the demand for dissolved oxygen; furthermore, low ammonia and accumulation of carbon dioxide in teleostean transport (Lim et al., 2003; Swann, 1993). In addition, dissolved oxygen is the single most important factor in the transport of live fish and must be supplied in adequate concentrations (Watson et al., 2010). Nevertheless, the values obtained during transport for all the treatments were significantly higher than the initial values. This fact was directly related to the supply of dissolved oxygen inside the bags before transport. Contrary, relevant pH decreases were shown during the periods of longest transport time to HD (2.42 ± 0.09) causing the increase in acidity of the seawater. This acidification is mainly because of an increase in the concentration of carbon dioxide in seawater caused by the fish respiratory activity (Lim et al., 2003; Watson et al., 2010). The increase in the seawater acidity could be cause gill dysfunction in seawater species (Martyshev, 2020; Munday, Donelson, Dixson, & Endo, 2009). Also, according to Timmons, Ebeling, Wheaton, Summerfelt, and Vinci (2002) marine fish have a low tolerance to NH3 N and should be kept below 50 μg L1 thus, during the transport time, the fish remained well below critical (2.35—8.34 μg NH3 NL1). Furthermore, the ammonia (NH3) concentrations increased in the treatments with the highest density (HD) and longest transport time (12 hr), indicating a directly proportional relationship between NH3 concentrations (8.34 ± 0.16 μg L1), stocking densities and transport time. Consequently, the highest NH4 concentrations were reported in treatments with HD at 10 and 12 hr, as well as at MD at 12 hr of transport, and the lowest concentration in treatment LD at 8 hr of transportation. Thus, a directly proportional relationship was obtained between NH4 concentrations and high densities, with the degradation of seawater quality because of the increase of fish excretion metabolites (Franklin & Edward, 2019). Similarly, the harmful effect of ammonia on seawater quality in freshwater fish transport was observed related to a longer transport time (Cupp et al., 2017; Smutná, Vorlová, & Svobodová, 2002). In addition, results similar to the maximum concentrations recorded in our study (10.77 μg NH4L1) were obtained by Rosado et al. (2016) with values of 10.92 μg NH4L1 in 17497345, 2022, 5, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/jwas.12865 by UGTO - Universidad de Guanajuato, Wiley Online Library on [19/09/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License ESPINOZA-RAMOS ET AL. ESPINOZA-RAMOS ET AL. a transport simulation for A. scapularis. Furthermore, the highest concentrations of NH3 N, NH3, and NH4 corresponding to the 12-hr transport treatments coincide with the reduction in pH, also recorded by Crosby et al. (2011), which indicates the acidification of seawater by increasing of nitrogenous compounds could increase the adverse effects on the viability of fish during transport. However, the results obtained in our study are below the average concentrations of nitrogen compounds for most marine fish (Ip & Chew, 2010). The results of the study indicated that the survival of A. scapularis juveniles was significantly higher at low densities (48 ind/bag) and duration (8 hr) of transport in polyethylene bags. The highest mortality was recorded at the end of the duration of transport and could be associated, among other unmeasured factors in this study, with the significant degradation of seawater quality, with an increase in nitrogen compounds and a slight increase in temperature followed by a decrease in pH. Almost similar observations have been reported in the transport of other fish species (Golombieski, Silva, Baldisserotto, & Da Silva, 2003; Gomes et al., 2003). 5 | C O N CL U S I O N In summary, transport time and stocking densities significantly affect the survival of Peruvian grunts because of changes in seawater quality. Thus, the influence of the variables analyzed to contribute to survival, and the sum of these, plus other parameters that were not measured such as stress, leads to the conclusion to use between 8 and 10 hr of transport time and not to exceed 72 ind/bag of stocking density. ACKNOWLEDGMENTS We express their gratitude to the authorities of the Jorge Basadre Grohmann National University for the financing of the Corvina and Sargo Project, and to the authorities of FONDEPES for facilities provided in Morro Sama Aquaculture Center. CONF LICT OF IN TE RE ST The author declares that they have no competing interests. AUTHOR CONTRIBUTIONS Luis A. Espinoza-Ramos: Conceptualization, methodology, formal analysis, data curation, research, writing—original draft, writing—review and editing, project management, fund raising. Renzo Pepe-Victoriano: Supervision, drafting— original draft, drafting—review and editing. Jordan I. Huanacuni: Data curation, formal analysis, data curation, drafting—original draft, drafting—review and editing, writing—review and editing. Manuel Nande: Formal analysis, drafting—original draft, drafting—review and editing, writing—review and editing. ORCID Luis A. Espinoza-Ramos Renzo Pepe-Victoriano Jordan I. 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