Introduction

Tilapia is the generic term for several genera and species of the family Cichlidae, of which Oreochromis is important for aquaculture. Tilapias are assumed to have evolved from a marine ancestor and several varieties are euryhaline and thus able to tolerate and adapt to different salinity conditions (^{El-Sayed 2006}). The temperature increases, altered rainfall regimes, and competition for freshwater between agricultural and urban sectors associated with global climate change have instigated studies on tilapia culture in estuarine and coastal environments (^{Prunet and Bornancin 1989}, ^{Romana-Eguia and Eguia 1999}, ^{Mena-Herrera et al. 2002}, ^{El-Sayed 2006}, ^{Fraga et al. 2012}). Because of zootechnical characteristics such as hardiness, acceptance of a wide variety of food, high feed conversion, and ability to reproduce year-round (^{Lupchinski et al. 2011}), tilapia is the second most important group of farmed fish in the world and considered to have the best potential for commercial culture in the 21st century (^{Fitzsimmons 2010}). Interest in tilapia culture in seawater in arid areas and near the coast arose in order to find another source of protein for human consumption (^{Cabrera et al. 2001}). These fish are herbivorous and omnivorous, which favors the use of ingredients of plant origin in their culture because of their high digestibility of proteins, carbohydrates, and energy (^{Shiau and Huang 1989}, ^{Davies et al. 2011}). Their high lipogenic activity is associated with their catabolic ability to metabolize carbohydrates (^{Qiang et al. 2014}). In regions where the availability of freshwater for aquacul-ture is limited, tilapia farming in marine environments is of interest from a scientific and commercial point of view (^{Pang 2005/06}, ^{El-Sayed 2006}), since there is growing demand for this fish.

The growth rates and feed conversion ratios of tilapia species such as Oreochromis aureus, Oreochromis spilurus, and hybrids reared in seawater are comparable to those of tilapia reared in freshwater (^{Cruz et al. 1990}, ^{Martínez-Contreras 2003}). The results of an intensive culture of hybrid tilapia (Oreochromis niloticus × O. aureus) in floating cages in the Barra de Navidad lagoon system (Jalisco, Mexico) indicate that the culture of this hybrid in seawater for commercial purposes is feasible (^{Martínez-Contreras 2003}). Though there are several comparative studies on the culture of tilapia species and hybrids in seawater and freshwater (^{Iwama et al. 1997}, ^{Mena-Herrera et al. 2002}, ^{Kamal and Mair 2005}, ^{Cnaani and Hulata 2011}), the performance efficiency of the red tilapia hybrid Oreochromis mossambicus × O. aureus has not been well studied. Therefore, the objective of the present study was to determine the growth perfomance, survival, and oxygen:nitrogen (O:N) ratio as an indicator of the metabolic substrate of the tilapia hybrid O. mossambicus × O. aureus cultured in seawater and freshwater.

Materials and methods

A batch of 3000 juvenile hybrid red tilapia (O. mossambicus × O. aureus) was obtained from the Centro Acuícola de Zacatepec, Morelos, Mexico (Comisión Nacional de Pesca). The already masculinized fish were transported by plane to our laboratory. Half of the organisms were acclimated from freshwater to seawater by daily increments of 5 in salinity until a final concentration of 34.5. Acclimated and non-acclimated individuals of a similar weight (24.9 ± 0.2 g on average) were selected and distributed in groups of 50 in two culture systems, each one with four 500-L fiberglass tanks. Each tank constituted the experimental unit. Each culture system was connected to a biofilter coupled to a reservoir recirculation system in order to renew 5% of the water volume every day. Water temperature was maintained at 28.0 ± 1 °C using a heater (6500 W) in each reservoir. Water quality variables (ammonium, nitrite, nitrate, carbonate, and pH levels) were evaluated twice a week in each culture system using a commercial test kit (Aquarium Pharmaceutical, Inc., Canada). Fish were fed to apparent satiation four times a day for 90 days. The diet was formulated based on their requirements to contain 40.2% crude protein and 8.5% crude fat (Table 1). Growth performance (i.e., weight gain) was evaluated in each experimental unit every 30 days.

Table 1: Ingredients (g/100 g diet) and proximate composition (g/100 g) of the diet. 

^a Tuna meal: 60% crude protein, 6.9% crude fat.

^b Pet food grade: 65% crude protein, 12% crude fat.

^c 42% crude protein, 1.0% crude fat.

^d 8% crude protein, 3.9% crude fat.

^e Donated by DSM, Guadalajara, Mexico.

^f Calculated by difference as nitrogen free extract + fiber.

The following biological indices were calculated: thermal growth coefficient (according to ^{Jobling 2003}) = 1000 × ((final weight^1/3 - initial weight^1/3)/Σ (days × temperature)); protein efficiency ratio = body weight gain/consumed protein; feed intake = food consumed × 100/[final weight + initial weight]/2)/days; feed conversion efficiency = body weight gain/food consumed; and feed conversion ratio = food consumed/body weight gain.

The apparent digestibility coefficients of the dietary nutrients were evaluated by determining the acid-insoluble ash content in the diet and in the feces according to the method proposed by ^{Tejada (1992)} and modified by ^{Montaño-Vargas et al. (2002)}. Proximate analyses of the experimental diet and feces were performed following standard methods (^{AOAC 1995}). The nitrogen-free extract was determined by difference (^{Jobling 2001}).

At the end of the study, respiration chambers were used to analyze oxygen consumption and ammonium excretion of one randomly-chosen fish from each treatment and experimental unit in the postpandrial state as reported by ^{Barreto-Curiel (2012)}. The O:N atomic ratio was calculated according to ^{Handa et al. (2013)} as follows: O:N = ([oxygen consumed]/16)/( [ammonium excreted]/14).

Student's t test for independent samples was used to estimate possible significant differences between the biological indices and the respirometric parameters of the experimental treatments. The differences were considered statistically significant if P < 0.05. All statistical analyses were performed using SigmaStat 3.5 (Systat Software, Inc., Chicago, IL, USA).

Results

After 90 days of the experiment, survival in both culture treatments was 99.5% (Table 2). There were no significant differences (P > 0.05) in weight gain and thermal growth coefficient between the fish cultured in seawater and freshwater (Table 2). Likewise, the protein efficiency ratio, feed intake, feed conversion efficiency, and feed conversion ratio did not differ significantly between the treatment groups. The individuals cultured in seawater had the highest digestibility values for dietary dry matter, protein, lipids, and carbohydrates. No significant differences (P > 0.05) in oxygen consumption, ammonium excretion, and O:N ratio were observed between the treatment groups (Table 3).

Table 2: Biological indices of juvenile hybrid tilapia (Oreochromis mossambicus x Oreochromis aureus) after being fed an experimental diet for 90 days in seawater and freshwater (mean ± standard deviation). 

^a TGC = thermal growth coefficient.

^b PER = protein efficiency ratio.

^c FI = feed intake.

^d FCE = feed conversion efficiency.

^e FCR = feed conversion ratio.

* Means in the same row are significantly different (P < 0.05).

Oxygen consumption, ammonium excretion, and oxygen:nitrogen (O:N) ratio of juvenile hybrid tilapia (Oreochromis mossambicus x Oreochromis aureus) grown in seawater and freshwater (mean ± standard deviation). 

Discussion

All tilapia are freshwater fish but their euryhaline ability allows several species and hybrids to adapt and develop in brackish and marine waters (^{Kamal and Mair 2005}). In this study, the culture of hybrid red tilapia (O. mossambicus × O. aureus) in seawater and freshwater did not reveal significant differences in either growth performance or the biological indices evaluated after 90 days. The growth performance was similar to that reported for hybrid tilapia (O. mossambicus × O. niloticus) fingerlings reared in seawater and freshwater and fed a commercial pelleted diet ad libitum for eight weeks (^{Martínez-Contreras 2003}). The hybrid O. mossambicus × O. aureus shows high tolerance to salinity and can grow normally in seawater (^{El-Sayed 2006}). A significant positive correlation between relative weight gain and increased salinity was reported for the hybrid O. mossambicus × O. niloticus (^{Kamal and Mair 2005}), a tendency that we did not observe in this study. In Florida red tilapia (O. mossambicus × O. urolepis hornorum), an increase in salinity promotes greater feed intake (^{Watanabe et al. 1988}). This behavior was not observed in the present study because feed intake did not differ significantly between treatment groups.

In the case of euryhaline fish such as tilapia, their culture in seawater, because of osmoregulation, is assumed to affect the activity of digestive enzymes and influence the feed conversion ratio and efficiency (^{Rubio et al. 2005}, ^{Ridha 2015}); however, this was not observed in the present study. It has been suggested that fish growth in saline environments is associated with osmoregulation and the expression of proteins such as transferrin (^{Rengmark and Lingaas 2007}), the ability to adapt their feed intake to the environmental salinity conditions, the metabolic rate, and endocrine factors (Prunet and Bornancin 1988, ^{Boeuf and Payan 2001}). Our digestibility values for dry matter, proteins, and lipids differed relative to the culture medium. In relation to the effect of salinity on changes in digestive enzymatic activity and nutrient digestibility in fish (^{Moutou et al. 2004}, ^{Rubio et al. 2005}), in the hybrid O. mossambicus × O. niloticus the activity of trypsine and a-amylase increases with salinity (^{Sandoval-Muy et al. 2012}). This is related to a possible activation of zymogens in the intestinal lumen (^{Moutou et al. 2004}). A recent study (in preparation) on the characterization of lipases in our laboratory revealed that in the anadromous striped bass (Morone saxatilis), the activity of lipase increased in the presence of NaCl; this does not occur in the Pacific bluefin tuna (Thunnus orientalis) and totoaba (Totoaba macdonaldi), species that are completely catadromous. Additional studies on the effect of salinity on the digestibility of dietary macronutrients and energy in the hybrid red tilapia are needed to be able to optimize its nutrition and culture in saline environments.

The O:N ratio is an indicator of the main substrate used by organisms to produce energy aerobically. Values of 3-16 indicate the catabolism of proteins, values of 16-60 indicate the combined used of proteins and lipids as substrates, and values >60 indicate that lipids are the predominant source of energy (^{Langenbuch and Pörtner 2002}, ^{Tseng and Hwang 2008}). In this study, the O:N values obtained for hybrid red tilapia reared in seawater and freshwater suggest a combined use of proteins and lipids as energy substrates in both treatments, which indicates that the difference in salinity did not significantly affect the type of metabolic substrate used as the predominant source of energy. This behavior is similar to that reported for Sphoeroides annulatus. This species was exposed to a variation in salinity of 31 and no significant differences were observed in the O:N atomic ratio and its main source of metabolic energy (^{Pérez-Robles et al. 2012}).

The red tilapia hybrid O. mossambicus × O. aureus is considered to have high potential for cultivation in a marine environment because of its high salinity tolerance, adaptation to confinement with high survival, rapid growth, and attractive sensory characteristics such as agreeably-tasting meat and a similar color to that of snappers (^{Fraga et al. 2012}). Our results show that it is feasible to cultivate this hybrid species in seawater and obtain a growth performance similar to that achieved in freshwater. We conclude that this strain of tilapia has the ability to adapt and thrive in a marine environmment and that its farming practices could be expanded.