Fish Transport: Stocking Density & Survival of Anisotremus scapularis

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: [email protected]
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.
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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).
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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
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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
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1046
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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
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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. Huanacuni
Manuel Nande
https://orcid.org/0000-0001-7958-7331
https://orcid.org/0000-0002-7630-1411
https://orcid.org/0000-0001-7381-8004
https://orcid.org/0000-0002-7733-1903
RE FE R ENC E S
Alaica, A. K. (2018). Partial and complete deposits and depictions: Social zooarchaeology, iconography and the role of animals in
late Moche Peru. Journal of Archaeological Science: Reports, 20, 864–872. https://doi.org/10.1016/j.jasrep.2018.02.002
Angel, A., & Ojeda, F. P. (2001). Structure and trophic organization of subtidal fish assemblages on the northern Chilean
coast: The effect of habitat complexity. Marine Ecology Progress Series, 217, 81–91. https://doi.org/10.3354/
meps217081
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
1048
1049
Barbieri, E., & Bondioli, A. C. V. (2015). Acute toxicity of ammonia in Pacu fish (Piaractus mesopotamicus, Holmberg, 1887) at
different temperatures levels. Aquaculture Research, 46(3), 565–571. https://doi.org/10.1111/are.12203
Belema, M., Idowu, K. O., Aghogho, K.-D., Ndubuisi, A., Oluwakemi, A., & Stella, U. (2017). Handling and
packaging of ornamental fishes for successful transportation. International Journal of Fisheries and Aquatic Studies, 5(5), 263–265. Retrieved from. https://www.fisheriesjournal.com/archives/2017/vol5issue5/PartD/5-474-296.pdf
fica de la asociacio
n de peces intermareales de la costa rocosa del norte de
Berrios, V., & Vargas, M. (2004). Estructura tro
Chile. Revista de Biología Tropical, 52(1), 201. https://doi.org/10.15517/rbt.v52i1.14881
Castro-Romero, R., & Muñoz, G. (2011). Two new species of Colobomatus (Copepoda, Phylichthyidae) parasitic on coastal
fishes in chilean waters. Crustaceana, 84(4), 385–400. https://doi.org/10.1163/001121611X555417
Chirichigno, N., & Cornejo, R. M. (2001). Catálogo comentado de los peces marinos del Perú. Callao-Perú: IMARPE.
Crosby, T. C., Hill, J. E., Martinez, C. V, Watson, C. A., Pouder, D. B., & Yanong, R. P. E. (2011). On-farm transport of ornamental fish 1. Fisheries and Aquatic Sciences Department, Florida Cooperative Extension Service, Institute of Food and
Agricultural Sciences, University of Florida., 1–7.
Cupp, A. R., Fredricks, K. T., Porcher, S. T., Smerud, J. R., Hartleb, C. F., & Gaikowski, M. P. (2017). Survival and behavioural
responses of cool and warm water fish sedated with AQUI-S ® 20E (10% eugenol) at high loading densities. Aquaculture
Research, 48(4), 1576–1589. https://doi.org/10.1111/are.12992
n de dietas
Dionicio-Acedo, J., Rosado-Salazar, M., Flores-Mego, J., Flores-Ramos, L., & Aguirre-Velarde, A. (2017). Evaluacio
n bioquímica muscular de juveniles de chita, Anisotremus
comerciales en el crecimiento y su efecto en la composicio
scapularis (Tschudi, 1846) (Familia: Haemulidae). Latin American Journal of Aquatic Research, 45(2), 410–420. https://doi.
org/10.3856/vol45-issue2-fulltext-16
Emmanuel, B. E., Fayinka, D. O., & Aladetohun, N. F. (2013). Transportation and the effects of stocking density on the
survival and growth of Nile tilapia, Oreochromis niloticus (Linnaeus). World Journal of Agricultural Sciences, 1(1), 1–7.
Espinoza-Ramos, L. A., Chilli-Layme, V. F., Pepe-Victoriano, R. G., Pino-Choqueapaza, J., & Contreras-Mamani, Z. (2019).
n Tacna. Ciencia & Desarrollo,
Captura, acondicionamiento y primer desove de sargo Anisotremus scapularis en la Regio
18(25(2)), 68–74. https://doi.org/10.33326/26176033.2019.25.867
Franklin, D. A., & Edward, L. L. (2019). Ammonia toxicity and adaptive response in marine fishes—A review. Indian Journal of
Geo-Marine Sciences, 48(3), 273–279.
Froese, R., & Pauly, D. (2019). Species list: World wide web electronic publication. Retrieved from FishBase Website www.
fishbase.org
n y abundancia de la ictiofauna de aguas someras en San Bartolo
Gárate, A., & Pacheco, A. (2004). Cambios en la distribucio
(Lima, Perú) después del ENSO 1997-98. Ecología Aplicada, 3(1,2), 148–153. Retrieved from. http://eprints.uanl.mx/
5481/1/1020149995.PDF
Golombieski, J. I., Silva, L. V. F., Baldisserotto, B., & Da Silva, J. H. S. (2003). Transport of silver catfish (Rhamdia quelen) fingerlings at different times, load densities, and temperatures. Aquaculture, 216(1–4), 95–102. https://doi.org/10.1016/
S0044-8486(02)00256-9
Gomes, L. C., Araujo-Lima, C. A. R. M., Roubach, R., Chippari-Gomes, A. R., Lopes, N. P., & Urbinati, E. C. (2003). Effect of
fish density during transportation on stress and mortality of juvenile Tambaqui Colossoma macropomum. Journal of the
World Aquaculture Society, 34(1), 76–84. https://doi.org/10.1111/j.1749-7345.2003.tb00041.x
Hach. (2003). HACH DR/2400 spectrophotometer procedures manual. Colorado. Retrieved from: Loveland. http://www.
ecommerce.hach.com/stores/hach/pdfs/dr2400cd/eng_pdf/NitrogenAmm_None_Other_NES_Eng_Ody.pdf
Ip, Y., & Chew, S. (2010). Ammonia production, excretion, toxicity, and defense in fish: A review. Frontiers in Physiology,
1(134), 1–20. https://doi.org/10.3389/fphys.2010.00134
Islam, M. N., & Hossain, M. A. (2013). Mortality rate of fish seeds (Labeo rohita) during traditional transportation system in
the Northwest Bangladesh. Journal of Scientific Research, 5(2), 383–392. https://doi.org/10.3329/jsr.v5i2.10572
Kluger, L. C., Scotti, M., Vivar, I., & Wolff, M. (2019). Specialization of fishers leads to greater impact of external disturbance:
Evidence from a social-ecological network modelling exercise for Sechura Bay, northern Peru. Ocean and Coastal Management, 179(104861), 1–15. https://doi.org/10.1016/j.ocecoaman.2019.104861
Kluger, L. C., Taylor, M. H., Mendo, J., Tam, J., & Wolff, M. (2016). Carrying capacity simulations as a tool for ecosystembased management of a scallop aquaculture system. Ecological Modelling, 331, 44–55. https://doi.org/10.1016/j.
ecolmodel.2015.09.002
Lim, L. C., Dhert, P., & Sorgeloos, P. (2003). Recent developments and improvements in ornamental fish packaging systems
for air transport. Aquaculture Research, 34(11), 923–935. https://doi.org/10.1046/j.1365-2109.2003.00946.x
Martyshev, F. G. (2020). Transport of live fish. In Pond fisheries (pp. 419–430). London, UK: CRC Press. https://doi.org/10.
1201/9781003072546-21
Medicina, J. A. (2014). Pesca artesanal en el Perú artisanal fishing in Peru. Ingeniería Industrial, 32, 27–58.
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.
Metar, S., Chogale, N., Shinde, K., Satam, S. B., Sadawarte, V., Sawant, A., … Singh, H. (2018). Transportation of live marine
ornamental fish. Advanced Agricultural Research & Technology Journal, 2(2), 206–208. Retrieved from. http://isasat.org/
vol-ii-issue-ii-july-2018/14_AARJ_II_2_Metar_et_al_206-208.pdf
Montes, M., Castro, A. M., Linares, J. F., Orihuela, L. I., & Carrera, L. J. (2019). Embryonic development of peruvian grunt
Anisotremus scapularis (Perciformes: Haemulidae). Revista de Biologia Marina y Oceanografia, 54(2), 166–173. https://doi.
org/10.22370/rbmo.2019.54.2.1881
Montgomery, D. W., Simpson, S. D., Engelhard, G. H., Birchenough, S. N. R., & Wilson, R. W. (2019). Rising CO2 enhances
hypoxia tolerance in a marine fish. Scientific Reports, 9(1), 1–10. https://doi.org/10.1038/s41598-019-51572-4
Munday, P. L., Donelson, J. M., Dixson, D. L., & Endo, G. G. K. (2009). Effects of ocean acidification on the early life history
of a tropical marine fish. Proceedings of the Royal Society B: Biological Sciences, 276(1671), 3275–3283. https://doi.org/
10.1098/rspb.2009.0784
Piper, R. G., McElwain, I. B., Orme, L. E., McCraren, J. P., Fowler, L. C., & Leonard, J. R. (1982). Fish hatchery management.
Washington, D.C.: U.S. Dept. of the Interior, Fish and Wildlife Service.
Quaresma, F. d. S., dos Santos, F. L. B., Ribeiro, P. F., Leite, L. A., & Sampaio, A. H. (2020). Acute toxicity of non-ionized
ammonia on tambacu (Colossoma macropomum x Piaractus mesopotamicus). Revista Ciência Agronômica, 51(3), 1–6.
https://doi.org/10.5935/1806-6690.20200046
n de Diferentes Concentraciones de Tricaína (MS-222) en el
Rosado, M., Dionicio, J., & Aguirre-Velarde, A. (2016). Evaluacio
Transporte de Chitas (Anisotremus scapularis) Juveniles. Revista de Investigaciones Veterinarias Del Perú, 27(4), 687.
https://doi.org/10.15381/rivep.v27i4.12576
Ross, L. G., & Ross, B. (2008). Anaesthetic and sedative techniques for aquatic animals (3rd ed.). Oxford, UK: Wiley-Blackwell.
https://doi.org/10.1002/9781444302264
Ruiz, D. J., & Wolff, M. (2011). The Bolivar channel ecosystem of the Galapagos marine reserve: Energy flow structure and
role of keystone groups. Journal of Sea Research, 66(2), 123–134. https://doi.org/10.1016/j.seares.2011.05.006
Salazar, D., Arenas, C., Andrade, P., Olguín, L., Torres, J., Flores, C., … Robles, C. (2018). From the use of space to
territorialisation during the Early Holocene in Taltal, coastal Atacama Desert, Chile. Quaternary International, 473,
225–241. https://doi.org/10.1016/j.quaint.2017.09.035
Sampaio, F. D. F., & Freire, C. A. (2016). An overview of stress physiology of fish transport: Changes in water quality as a
function of transport duration. Fish and Fisheries, 17(4), 1055–1072. https://doi.org/10.1111/faf.12158
Smutná, M., Vorlová, L., & Svobodová, Z. (2002). Pathobiochemistry of ammonia in the internal environment of fish (review).
Acta Veterinaria Brno, 71(2), 169–181. https://doi.org/10.2754/avb200271020169
Svobodová, Z., Lloyd, R., Máchová, J., & Vykusová, B. (1993). Water quality and fish health. In EIFAC Technical Paper (Vol. 54).
Swann, L. (1993). Transportation of fish in bags. In NCRAC extension fact sheets (Vol. 10, pp. 1–4). West Lafayette, IN: Introduction: North Cantral Regional Aquaculture Center. Retrieved from. https://lib.dr.iastate.edu/ncrac_factsheets/10/
Timmons, M. B., Ebeling, J. M., Wheaton, F. W., Summerfelt, S. T., & Vinci, B. J. (2002). Recirculating aquaculture systems
(2nd ed.). Ithaca, NY 14850: Cayuga Aqua Ventures.
Vagner, M., Lefrançois, C., Ferrari, R. S., Satta, A., & Domenici, P. (2008). The effect of acute hypoxia on swimming stamina
at optimal swimming speed in flathead grey mullet Mugil cephalus. Marine Biology, 155(2), 183–190. https://doi.org/10.
1007/s00227-008-1016-x
von Tschudi, J. J. (1846). Untersuchungen über die Fauna Peruana. In Ichthyologie. St. Gallen, Switzerland: [s.n.]. https://doi.
org/10.5962/bhl.title.60791
Wang, W., Zhang, Y., Liu, Y., Adányi, N., & Zhang, X. (2020). Effects of waterless live transportation on survivability, physiological responses and flesh quality in Chinese farmed sturgeon (Acipenser schrenckii). Aquaculture, 518, 1–9. https://doi.
org/10.1016/j.aquaculture.2019.734834
Watson, C., Kilgore, K. H., & Martinez, C. (2010). Shipping fish in boxes. South Regional Aquaculture Center, 3903, 1–9.
Weber, R. A., Peleteiro, J. B., Martín, L. O. G., & Aldegunde, M. (2009). The efficacy of 2-phenoxyethanol, metomidate, clove
oil and MS-222 as anaesthetic agents in the Senegalese sole (Solea senegalensis Kaup 1858). Aquaculture, 288(1–2),
147–150. https://doi.org/10.1016/j.aquaculture.2008.11.024
Zar, J. H. (2010). Biostatistical analysis (5th ed.). Upper Saddle River, NJ 07458: Pearson Prentice Hall.
How to cite this article: Espinoza-Ramos, L. A., Pepe-Victoriano, R., Huanacuni, J. I., & Nande, M. (2022).
Effect of transportation time and stocking density on seawater quality and survival of Anisotremus scapularis
(Perciformes: Haemulidae). Journal of the World Aquaculture Society, 53(5), 1042–1050. https://doi.org/10.
1111/jwas.12865
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