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Latin american journal of aquatic research

On-line version ISSN 0718-560X

Lat. Am. J. Aquat. Res. vol.46 no.5 Valparaíso Dec. 2018

http://dx.doi.org/10.3856/vol46-issue5-fulltext-7 

Research Article

Thermal tolerance and aerobic scope of tetra-hybrid tilapia Pargo-UNAM

Evnika Zarina Medina-Romo1 

Fernando Díaz1 

Ana Denise Re-Araujo1 

Leonardo Ibarra-Castro2 

Mario Garduño-Lugo3 

Erendira Rocío Latorre-Pozos1 

Ernesto Larios-Soriano1 

Carlos Rosas4 

1Laboratorio de Ecofisiología de Organismos Acuáticos, Departamento de Biotecnología Marina Centro de Investigación Científica y de Educación Superior de Ensenada (CICESE) Ensenada, Baja California, México

2Laboratorio de Reproducción de Peces Marinos, Centro de Investigación en Alimentación y Desarrollo (CIAD), Sinaloa, México

3Centro de Enseñanza, Investigación y Extensión en Ganadería Tropical Facultad de Medicina Veterinaria y Zootecnia, Universidad Nacional Autónoma de México Martínez de la Torre, Estado de Veracruz, México

4Unidad Multidisciplinaria de Docencia e Investigación, Facultad de Ciencias Universidad Nacional Autónoma de México, Sisal, Yucatán, México

ABSTRACT:

Fish actively select an adequate environment that fits their optimum culture/preferred temperature, this mechanism is called thermoregulatory behavior. However, what exactly is this mechanism, how does it work and what can we learn from it? Helped by their thermal limits, fish avoid temperature variations not favorable for their maximum growth. They find a thermal window where optimal temperature culture is located and use it in the best way possible for all activities. The present study is based on thermal biology studies, and its purpose is to learn the aerobic scope functions on Pargo-UNAM juveniles. The importance of this study is related to the fact that Pargo-UNAM fish, being a hybrid, has five different genetic backgrounds. We found that acclimation temperature influenced the preferred temperature of Pargo-UNAM, having a metabolic adjustment in the 20-32ºC range; the Final preferendum obtained was 29.5ºC. The maximum and minimum range of critical thermal limits was between 39.2-43.5ºC and 8-14.9ºC, respectively. The thermal window had an area of 355.2ºC2. The acclimation response ratio had a 0.40-0.35 interval for CTMax, and 0.52-0.69 for CTmin. Chase method used in Pargo-UNAM caused a maximum aerobic scope at 29ºC. Blood lactate concentration was the highest in fish acclimated at 20ºC; these values decreased while acclimation temperature increased. Results from Pargo-UNAM juveniles showed that these can be grown successfully in a 26-32ºC temperature range, with their greater performance at 29ºC, where the aerobic scope was at its maximum capacity.

Keywords: critical thermal; preferred temperature; thermal window; metabolism; lactate; aquaculture

INTRODUCTION

Tilapia is the most cultivated fish group around the world, ranking second in production after carp (FAO, 2014). I it would be important to have a thorough knowledge of the basics about its biological cycle, specifically concerning the thermotolerance aspects to produce tilapia commercially. Optimum temperature from tilapia ranges from 20ºC to 30ºC, and the reproduction occurs successfully at 26-29ºC (El-Sayed, 2006; Saavedra-Martínez, 2006). Pargo-UNAM (PU) is a red tilapia obtained via hybridization through inter-specific crosses (Ramírez-Paredes et al., 2012). It was developed in the Centro de Enseñanza, Investigación y Extensión en Ganadería Tropical (CEIEGT) by Muñoz-Cordova & Garduño-Lugo (2003), in an attempt to improve the production of red tilapia strains in Mexico. Learning about the potential of hybrid tilapia through thermal biology would give us an advantage on aquaculture research.

The temperature is the main abiotic factor that influences numerous aspects of fish biology, distri-bution, and behavior (Fry, 1947). Thermal preference is an aspect of each species genetically inherent in its behavior. Aquatic organisms have developed a thermoregulatory behavior that enables them to actively select a thermal habitat that matches with their optimum temperature. In this habitat, it avoids temperature variations and reaches its best performance (Kelsch & Neill, 1990; Golovanov, 2013). The influence of endogenous factors such as age, weight, food availability, density, and pathogens, as well as abiotic factors such as season, water quality, and light intensity have a profound impact in the thermal behavior (Wedemeyer et al., 1976; Reynolds & Casterlin, 1978; Díaz et al., 2004).

Thermal tolerance of many aquatic ectotherms has been calculated through the critical thermal limits, consisting of exposing the fish to a constant increase or decrease rate of water temperature until a non-lethal endpoint is reached. At this point, fish may show a loss in the righting response or onset muscle spasms (Bennet & Beitinger, 1997). Thermal windows, minimum and maximum temperatures an organism can successfully tolerate, provide general insights into the niches of taxa (Fry, 1971; Rezende et al., 2014). Thermal thresholds represent a combination of physiological and biochemical features (Somero, 2004).

The oxygen consumption rate increases as the temperature rises, until the critical temperature threshold, is reached. At this point, there is a cellular transition from aerobic to anaerobic metabolism; therefore, the critical thermal limit becomes a match when the aerobic scope is close to zero. Above this point, the aerobic metabolism is suppressed due to a failure in the functions of ventilation and/or blood circulation, even if there is enough oxygen concen-tration available in the environment (Jost et al., 2012). Survival beyond the critical thermal maximum (CTMax) point is limited by time, due to the insufficient ATP yield from anaerobiosis. Temperature intervals between the critical thermal limits and optimal temperature are called Pejus, a transitory temperature where protection mechanisms against radical oxygen molecules are activated (Cumillaf et al., 2016; Rodríguez-Fuentes et al., 2017).

The fish aerobic scope is determined by the difference between the oxygen consumption maximum or maximum metabolic rate (MMR) and the standard metabolic rate (SMR) (Clark et al., 2013; Farrell, 2013, 2016; Roche et al., 2013; Chabot et al., 2016). Pörtner (2010) and Sokolova et al. (2012) propose that the maximum aerobic scope (AS) can be obtained in the optimal temperature because in this condition the organism reaches its maximum performance. None-theless, when the relationship between the MMR and SMR curves and acclimation temperature is extreme, the aerobic scope is almost zero; therefore, the metabolic condition has a minimum performance (Fry, 1947; Ferreira et al., 2014).

The response of blood lactate to exercise has been used to evaluate the aerobic capacity of sedentary, active or slow swimmers. After 5 min of a fish being chased, lactate builds up in its blood. For this reason, blood levels have been included as an indicator of the onset of anaerobic metabolism (Peak et al., 1997; Brooks et al., 1999).

The present study was designed to evaluate thermal tolerance responses after different acclimation tempe-ratures in Pargo-UNAM juveniles and determine the aerobic scope with the chase method. The main goal is to comprehend the thermal physiology of this hybrid, to improve and extend its aquacultural practices. Another goal is to understand how hybrid tilapia could deal with climate changes, which may affect its distribution.

MATERIALS AND METHODS

Obtaining experimental organisms

Pargo-UNAM fingerlings were obtained from the aquaculture facility at Centro de Enseñanza, Inves-tigación y Extensión de Ganadería Tropical (CIEGT-UNAM) at Tlapacoyan, Veracruz, and then transferred to Departamento de Biotecnología Marina del Centro de Investigación Científica y de Educación Superior de Ensenada (CICESE). A group of 250 fish ranging from 0.5 to 1.5 g wet weight was maintained in two 2000 L reservoirs with a continuous freshwater flow and constant aeration (water temperature was maintained at 28ºC). Fish were fed with the commercial diet NutripecMR PurinaMR pellets (2.4 mm, 44% protein, 15% lipids, Agribrands Purina México S. de R.L, México) three times per day to satiation, and feces were removed daily. Water quality parameters were as follows: pH 8.0 ± 0.1, 6.6 ± 0.8 mg O2 L-1 and alkalinity was 115.5 ± 9.5 mg CaCO3 L-1.

Thermal acclimation

Two hundred and fifty Pargo-UNAM juveniles were acclimated to determine the preferred temperature (PT), critical thermal maximum (CTMax), critical thermal minimum (CTMin), and aerobic scope (AS), in five 500 L tanks with 50 individuals for each acclimation temperature (AT), regulated with a 1000 W immersion heater or cold finger cooler. The temperature was increased or reduced from 28ºC (1ºC per day) until reaching temperatures of 20, 23, 26, 29, and 32ºC with a daily variation of ±1.0°C; acclimation time lasted for 30 days in controlled conditions (Saavedra-Martínez, 2006). The system allows an open water flow. Water quality was maintained at pH 7.8 ± 0.1, dissolved oxygen at 6.6 ± 0.3 mg O2 L-1 , and alkalinity by 115.5 mg CaCO3 L-1. Organisms were fed at satiation every day three times a day. Feces were removed daily. During acclimation, no signs of mortality were detected.

Preferred temperature

An acute method was used to determine the preferred temperature with a horizontal temperature gradient, as described by Díaz et al. (2007). The temperature gradient ranged from 8 to 40ºC (y = 3.542 + 1.426 x; R2 = 0.95, where y = segment temperature, and x = gradient segment). The intersection graphically calculated the final preferendum (FP) between preferred temperatures and the equality line (González et al., 2010).

To learn the preferred temperature (PT) of the organisms, we followed the acute method described by Reynolds & Casterlin (1979). 12 h before introducing the Pargo-UNAM in the horizontal thermal gradient, we labeled two groups of five organisms each with a plastic mark sewn to the caudal fin. Each group was placed in the virtual chamber of the corresponding experimental acclimation temperature. All temperatures are measured with an infrared digital thermometer (Steren model Her-425, Mexico). To avoid interference from feeding, and as recommended by Beamish & Trippel (1990), fish were not fed in a 24 h period before the trials. The experiment lasted for 2 h, and during its course, every 10 min we were recording the chamber (among the 20 chambers making up the gradient) at which organisms were located and the temperature.

CTMax, CTmin, ARR, and thermal window

CTMax data were obtained using 10 individuals, from each experimental condition, 40 L aquarium provided with 1000 W immersion heater and permanent aeration, to maintain a uniform temperature (González et al., 2010). Fish were introduced to the aquarium 30 min before the temperature started to increase, to reduce the direct effects of handling stress during measurements (Pérez et al., 2003). The temperature was increased at a rate of 1ºC min-1 from each acclimation temperature. This rate should be slow enough to allow deep body temperature and to follow the test temperature without a significant time delay until they showed a loss of righting response (LRR) symptoms (Lutterschmidt & Hutchinson, 1997). After reaching this point, organisms were returned to their acclimation temperature.

CTmin data were obtained from 10 Pargo-UNAM juveniles from each experimental condition. Then, they were introduced into the thermal horizontal gradient; a minimum temperature of 6.8ºC was set in the first segment. A fish was transferred 30 min before the experiment into the plastic cage, reducing the stress caused by handling (Pérez et al., 2003). Each cage was placed in sequential order in the gradient segment with AT and gradually was moved into the colder side at the rate of 1ºC min-1. LRR symptoms were recorded when the organism showed them, and they were returned immediately to acclimation temperature.

A thermal window was built with CTMax and CTmin values at each AT using a modified version of the method of Bennet & Beitinger (1997). Preferred temperature, Pejusmax, and Pejusmin were included in the thermal window (Cumillaf et al., 2016).

The acclimation response ratio (ARR) was calculated as an index to learn the magnitude of thermal acclimation using equation 1, proposed by Claussen (1977).

(1)

where: CTMax2-CTMax1 or CTmin2-CTmin1 (1) represent the difference between the values of critical temperatures (max or min) within the whole acclimation temperature range examined (TA2-TA1).

Chase method

Twelve juveniles were randomly selected from each AT tank to calculate the maximum metabolic rate (MMR). First, fish were placed into a circular exercise tank with fresh water; one by one (47 cm diameter, 15 cm water depth); temperature and aeration in the tank were controlled. After 15 min of recovery time by handling, fish were continuously chased with nets and lightly pushed when they stopped swimming or if they slowed down. The chasing time given was 5 min, according to Roche et al. (2013) and Norin et al. (2014); after that time, they were immediately introduced in a hermetic respirometric chamber and submerged in a freshwater bath, having the temperature controlled at the same AT as in the last environment they were at. We used six respirometric chambers (1 L) for each repetition provided with an optic fiber oxygen sensor (precision ± 0.005% O2, detection limit 0.03% O2) and connected them to an OXY-10 mini-amplifier (PreSens GmbH, PreSens©, Germany). A respirometric chamber without fish was used as a control to measure the oxygen consumed by microorganisms, by subtracting it in the final data. The initial oxygen concentration was recorded with an opened water flow; the water flow was immediately interrupted for 5 min, and the final oxygen concentration was recorded. The following equation was used to calculate the respiration rate:

(2)

where MO2 is the respiration rate (mg O2 h-1 kg-1ww), O2(i) is the initial oxygen concentration in the chamber (mg O2 L-1), O2(f) is the final oxygen concentration in the chamber (mg O2 L-1), V is the water volume in the chamber, minus the water volume displaced by the animal (L), t is the time (h), and M is the body mass of the experimental animal (kg-1 wet weight). Fish were weighed, and blood samples were taken from the caudal vein and finally returned to their respective AT tank.

Twelve fish were maintained for 24 h in the respirometric chamber and submerged in a bath of controlled temperature with open flow water to calculate SMR, at the same AT as in the last environment they were at. During this evaluation, fish were not fed. After that, flowing water was interrupted for 5 min, and the oxygen concentration was measured. The lower oxygen consumption was used to calculate the SMR. Both respiration rates were calculated from the oxygen consumption as mg O2 h-1 kg-1 ww. Induced AS can be obtained as MMR-SMR, where AS reflects the muscle activity of the chased fish. The factorial aerobic scope was obtained by MMR/SMR and Q10 = (MMR/SMR) (10/(T2-T1) where T2 and T1 represent AT.

Blood lactate

Blood samples were obtained with disposable 2 mL (pediatric) syringes from the caudal vein from each experimental fish, exposed to the chase method; then, a drop was immediately placed on a disposable lactate test strip of the Accutrend® Plus (Roche Diagnostics GmbH). For all the trials of metabolic rates, the measure of lactate was expressed as mmol L-1.

Data and statistical analysis

First, data were pooled for each acclimation temperature, to find differences among medians obtained from Acute method results. An exploratory data analysis (Tukey, 1977) and a one-way ANOVA Kruskal-Wallis analysis were performed. Linear regression was calculated from median values of Preferred Temperatures to determine the kind of response shown by organisms, in accordance with Johnson & Kelsch (1998). A descriptive statistical analysis (Tukey, 1977) and the one-way ANOVA test (Shapiro-Wilk) by Holm-Sidak were applied to detect the differences, with an All Pairwise comparison between mean values from each CTMax and CTmin data. MMR and SMR metabolic rates and lactate mea surements were plotted, and the differences were statistically compared from chase results. All statistical tests and graphics were performed using Sigma Plot v.12.

Table 1 ARR of tilapia Pargo-UNAM juveniles at different ARR acclimation temperatures, acclimation response ratio, obtained from mean values of CTMax and CTmin and temperature intervals. 

RESULTS

The temperature selection of Pargo-UNAM increased with the rise of AT. The slope obtained from the linear regression equation was 0.29 (PT = 21.420 + 0.290 × AT), R2 = 0.831. The final preferendum was 29.50ºC. The critical thermal limits for Pargo-UNAM juveniles increased as the acclimation temperature rose (P < 0.05). CTMax and CTmin ranges were 39.2 to 43.5ºC and 8 to 14.9ºC, respectively. The acclimation response ratio (ARR) range was 0.35-0.40 for CTMax and 0.52-0.69 for CTmin (Table 1).

The thermal window obtained for Pargo-UNAM showed a total area of 359.1°C2. The optimal zone outlined by the preferred temperatures showed an area of 63.93°C2 (Fig. 1). The zone representing Pejusmax and Pejusmin showed areas of 122.5ºC2 and 169.3ºC2, respectively.

The maximum metabolic rate increased with acclimation temperature from 20 to 29ºC, showing its peak in organisms acclimated to 29ºC and 261.0 ± 11.6 mg O2 h-1 kg-1 wet weight, and oxygen consumption is significantly reduced to 32°C. SMR values maintained a similar trend in organisms acclimated from 20 through 32ºC (Fig. 2a). The highest AS was in the fish acclimated to 29ºC, with 187 mg O2 h-1 kg-1 wet weight value, AS decreased in organisms acclimated to 20 and 32ºC (Fig. 2b). Blood lactate concentrations showed that the value decreased significantly from 1.8 to 1.15 mmol L-1 in 20°C and 32°C, respectively (P < 0.05) from fish exposed to chase. Controls ranged from 0.5 to 0.7 mmol L-1 (Fig. 2c).

DISCUSSION

According to Kelsch & Neill (1990) and Johnson & Kelsch (1998), the relationship between preferred temperature (PT) and the acclimation temperature can be divided into three classes: positive, independent, and negative. In the case of Pargo-UNAM juveniles, the 0.29 slope was positive, which represents a partial physiological adjustment to improve the metabolic efficiency at the new temperature. Later, this will reflect on a preferred temperature increase (Johnson & Kelsch, 1996). A positive response has been found in other fish such as Mozambique tilapia (Oreochromis mossambicus), common carp (Cyprinus carpio), bluegill (Lepomis macrochirus), and largemouth bass (Micropterus salmoides) (Badenhuizen 1967; Cherry et al., 1975; Cincotta & Stauffer, 1984). Species experiencing annual cycles of relatively high amplitude were expected to show temperature-preference relationships that are positive functions. Therefore, Pargo-UNAM juveniles can be classified in the eurytherms group.

Figure 1 A thermal window for Pargo-UNAM juveniles acclimated to different temperatures. The black dots with lines represent mean values from preferred temperatures ± SD. The 45° line represents the point where preferred and acclimation temperature are equal. The triangles represent the CTMax and CTmin, and the area outlined by these points includes Pejusmax and Pejusmin. 

Pargo-UNAM (PU) juveniles final preferendum (FP) was very close to other species of tilapia: Badenhuizen (1967) and Stauffer (1986) obtained a preferred temperature for Mozambique tilapia between 28 and 32.2ºC, respectively; for Nile tilapia (Oreochromis niloticus), Beamish & Trippel (1990) reported a 28-29.5°C interval. Some studies in O. niloticus (Azaza et al., 2008; Abdel-Tawwab & Wafeek, 2014) have shown preferred temperature in the 28-32ºC interval. Watanabe et al. (1993) reported that

Figure 2 a) Maximum metabolic rate (MMR) and standard metabolic rate (SMR) of fish exposed to chase, b) aerobic scope (AS) calculated as MMR-SMR, black dots represent the mean ± standard error, c) blood lactate of fish exposed to chase, the continuous line is experi-mental, and the dashed line represents control values. 

Florida red tilapia reached a maximum growth at 27ºC, which is very close to its FP. The results obtained in this study are important to improve Pargo-UNAM culture, so it can be developed successfully in regions where the water temperature is near 29.5°C.

Given the above, it can be assumed that in the FP organisms will optimize their physiological process in such manner that energy expenditure is reduced, which may translate in energy savings aimed directly to potential growth.

Figure 3 a) Factorial AS obtained from MMR/SMR from the chase, b) metabolic cost as Q10 obtained from the MMR. Black dots represent the mean values. 

Therefore, the FP can be used as a temperature measurement, selected by PU and as an index of the magnitude of temperatures to which the species is adapted (Johnson & Kelsch, 1998). This result demonstrates that PU was able to choose within the horizontal thermal gradient the most advantageous temperatures available on the virtual chambers, like those conditions in its environment. We conclude that PU was able to regulate its body temperature by using behavioral thermoregulation.

According to Pörtner (2010) and Sokolova et al. (2012), CTMax and CTmin represent the upper and lower limits corresponding to the critical thermal threshold. PU juveniles reached the CTMax at 43.5ºC. Thermal thresholds obtained from the thermal window are found in the geographical zones where tilapia is grown in Mexico. These areas are affected by temperatures that have increased or decreased, origi-nated by climate changes that have occurred in recent years (Noyola et al., 2015). That is why is crucial to learn the thermotolerance of aquatic species on a planet that is changing due to global warming. In the present study, we propose that values reported of CTMax in PU correspond to the critical threshold temperature at which the scope of metabolic activity is zero. The above explains why organisms in this threshold temperature can stay alive for a short period, where animals enter into physiological repair (Pörtner, 2010), and demonstrates that intervals between 26 to 29°C correspond to an acclimation temperature where the maximum performance is observed (Pörtner, 2010).

The CTmin reached by PU juveniles had an 8-14°C interval, as compared to the 2.5-11-3°C range of Cyprinidon variegatus (Bennet & Beitinger, 1997) and to the interval obtained by Currie et al. (1998) for Ictalurus punctatus (2.7-9.8ºC) and M. salmoides salmoides (3.2-10.7ºC); these ranges indicate that when comparing PU to these species, PU is more susceptible to cold water; except for Argyrosomus regius (11.7-13.24°C) (Kir et al., 2017) which is intolerant to cold. Concerning other fish, tilapia is more susceptible to low temperatures; therefore, its growth is reduced.

Acclimation response ratio is usually considered a reliable measurement to indicate the physiological response of fish to a given temperature change (Claussen, 1977; Chatterjee et al., 2004), although it depends on previously experienced temperatures (Díaz et al., 1998). ARR can be interpreted as the heat-tolerance degrees gained for each centigrade grade increased in acclimation temperature (He et al., 2014; Kir et al., 2017). Aquatic organisms inhabiting in cold or temperate regions show lower ARR values because they experience longer and more gradual temperature fluctuations; as a result, they have a reduced tolerance to abrupt temperature changes (Díaz et al., 1998, 2004). Cold-water species such as Schizothorax kozlovi (He et al., 2014), Oncorhynchus mykiss (Brett, 1952), and Salvelinus fontinalis (Currie et al., 1998) have shown ARR values of 0.21, 0.18, 0.14 and 0.1-0.30, respectively. In contrast, high ARR values such as PU values are characteristic of organisms experiencing wide temperature fluctuations in a short period, since they have no time to use adjustment mechanisms. For this reason, PU can be characterized as a subtropical fish because its ARR values are in the 0.34-0.67 range. Many commercially important fish are geographically located in subtropical and tropical zones, such as Tilapia spp., Ctenopharyngodon, Cyprinus, and Ictalurus and share similar ARR values, but the most important characteristic is that they are eurythermic; allowing them to tolerate changes and deal with global warming (Gunderson & Stillman, 2017).

The thermal window provides important insights regarding fish ecology, distribution, and survival tactics (Bennet & Beitinger, 1997) and determines optimal culture conditions (Noyola et al., 2013), providing a comparative index of eurythermicity among species (Eme & Bennet, 2009). The usefulness of thermal windows (reported as °C2) relies on its ability to offer a visual comparison among species, instead of only a thermal preference point. Also, thermal windows define intrinsic thermal tolerance zones, i.e., tolerance-independent from previous thermal acclimation history. A complete thermal window for PU juveniles with different zones such as the optimal, transition (Pejus) and critical limits threshold was included. According to this, the best performance of PU juveniles occurred in the optimal zone with a 63.4°C2 area. The total thermal window area of PU juveniles (355.2°C2) is higher than Labeo rohita, (273.5ºC2), Anabas testudineus (278.3°C2), Cyprinus carpio (311.6ºC2), Lutjanus guttatus (344.25°C2), Ocyurus chrysurus (282.0°C2) (Chatterjee et al., 2004; Larios, 2014; Noyola et al., 2015) and lower than Horabagrus brachisoma (526°C2), and Argyrosomus regius (460°C2) (Dalvi et al., 2009).

Due to the last characteristic, PU could be cultivated in many areas of Mexico where the minimum and maximum temperatures are between the 20-32°C range (INEGI, 2015). The relationship between the preferred temperature and metabolic optimal of fish is linked with the concept of aerobic scope (Fry, 1947). The maximum aerobic scope for activity generally occurs at the preferred temperature. The highest aerobic scope obtained for PU was 29°C, where this temperature corresponds to the preferred temperature. Thus, the highest amount of available energy could be channeled to adaptive functions in PU juveniles, such as activity, growth, reproduction, and survival, in a similar manner as other species (Beamish, 1981; Jobling, 1981; Kelsch & Neill, 1990; Kelsch, 1996; Alsop et al., 1999; Lee et al., 2003).

In PU, AS values are like the aerobic scope of Ocyurus chrysurus, a tropical fish with similar thermal tolerance. Chase increased swimming activity, which led the organism to increase its muscular energy demand and, as a result, a rise in oxygen consumption. Factorial aerobic scope shows that PU and O. chrysurus could be cataloged as semi-sedentary fish (Noyola et al., 2015)

Lactate and amino acids are the preferred substrates for gluconeogenesis when there is an oxygen deficit (Moon & Foster, 1995; Suarez & Mommsen, 1997). It has been demonstrated that the lactate concentration in the blood increases after some stress; this is due to muscle glycolysis (Wood et al., 1985). Blood lactate values obtained from fish exposed to chase were very low. Thus, they used the aerobic metabolism even at temperatures from 20 to up to 29°C. Blood lactate values found were in the 1.2-1.8 range; this could be associated with constant values in blood, liver, and muscle (Frederich & Pörtner, 2000, 2001; Sokolova & Pörtner, 2002).

Under prolonged stress conditions such as a 20°C temperature, in which an organism spends more energy than the one available on its active metabolism, PU is forced to activate anaerobic pathways (Priede, 1977). When Ocyurus chrysurus was exposed to chase, it had lower blood lactate in the 20-26°C interval temperature and a higher lower blood lactate when they were exposed to 30 and 32°C, indicating that ATs affected its metabolism, probably because they were close to their upper threshold limit (Noyola et al., 2015).

Knowledge regarding the thermoregulatory behavior of PU provides important information for aquaculture and in selecting the places where the temperature is optimal for its growth. PU juveniles showed a high degree of eurythermicity and a positive response to thermal changes; and this leads us to conclude that PU will be grown successfully in a 26-32°C temperature range, having its greater performance at 29ºC, where the aerobic scope was at its maximum performance.

ACKNOWLEDGMENTS

We would like to thank CONACYT for the scholarship granted to Evnika Zarina Medina Romo and for providing the funds to support the expenses generated from this research. We also appreciate the collaboration of Emmanuel Garduño from Centro de Enseñanza, Investigación y Extensión de Ganadería Tropical (CIEGT-UNAM) who facilitated the organisms employed in this study and to Asael G. Arroyo Re for the English language editing of the manuscript.

REFERENCES

Abdel-Tawwab, M. & M. Wafeek. 2014. Influence of water temperature and waterborne cadmium toxicity on growth performance and metallothionein-cadmium distribution in different organs of Nile tilapia, Oreochromis niloticus (L.). J. Therm. Biol., 4: 157-162. [ Links ]

Alsop, D.H., J.D. Kieffer & C.M. Wood. 1999. The effects of temperature and swimming speed on instantaneous fuel use and nitrogenous waste excretion of the Nile tilapia. Physiol. Biochem. Zool., 72: 474-483. [ Links ]

Azaza, M.S., M.N. Dhraïef & M.M. Kraïem. 2008. Effects of water temperature on growth and sex ratio of juvenile Nile tilapia, Oreochromis niloticus (Linnaeus) reared in geothermal waters in southern Tunisia. J. Therm. Biol., 33: 98-105. [ Links ]

Beamish, F.W.H. 1981. Swimming performance and metabolic rate of three tropical fishes in relation to temperature. Hydrobiologia, 83: 245-254. [ Links ]

Beamish, F.W.H. & E.A. Trippel. 1990. Heat increment: a static, dynamic dimension in bioenergetics models? T. Amer. Fish. Soc., 119: 649-661. [ Links ]

Badenhuizen, T.R. 1967. Temperatures selected by Tilapia mossambica (Peters) in a test tank with a horizontal temperature gradient. Hydrobiologia, 30(3-4), 541-544. [ Links ]

Bennett, W.A. & T.L. Beitinger. 1997. Temperature tolerance of the sheepshead minnow, Cyprinodon variegatus. Copeia, 1997(1): 77-87. [ Links ]

Brett, J.R. 1952. Temperature tolerance of young Pacific salmon, genus Oncorhynchus. J. Fish. Res. Bd. Can., 9: 265-323. [ Links ]

Brooks, G.A., T.D. Fahey, T.P. White & K.M. Balwin. 1999. Exercise, atmospheric pressure, air pollution, and travel. Exercise physiology: human bioenergetics and its applications. Mayfield Publishing Company Mountain View, CA., pp. 504-536. [ Links ]

Chabot, D., J.F. Steffensen & A.P. Farrell. 2016. The determination of standard metabolic rate in fishes. J. Fish Biol., 88: 81-21. [ Links ]

Chatterjee, N., A.K. Pal, S.M. Manush, T. Das & S.C. Mukherjee. 2004. Thermal tolerance and oxygen consumption of Labeo rohita and Cyprinus carpio early fingerlings acclimated to three different temperatures. J. Therm. Biol., 29: 265-270. [ Links ]

Cherry, D.S., K.L. Dickson & J. Cairns Jr. 1975. Temperatures selected and avoided by fish at various acclimation temperatures. J. Fish. Res. Bd. Can., 32: 485-491. [ Links ]

Cincotta, D. & J.R. Stauffer Jr. 1984. Temperature preference and avoidance studies of six North Ameri-can freshwater fish species. Hydrobiologia, 109: 173-177. [ Links ]

Clark, T.D., E. Sandblom & F. Jutfelt. 2013. Aerobic scope measurements of fishes in an era of climate change: respirometry, relevance, and recommen-dations. J. Exp. Biol., 216: 2771-2782. [ Links ]

Claussen, D.L. 1977. Thermal acclimation in ambystomatid salamanders. Comp. Biochem. Physiol. A, 58: 333-340. [ Links ]

Cumillaf, J.P., J. Blanc, K. Paschke, P. Gebauer, F. Díaz, D. Re, M.E. Chimal, J. Vázquez & C. Rosas. 2016. Thermal biology of the sub-polar-temperate estuarine crab Hemigrapsus crenulatus (Crustacea: Decapoda: Varunidae). Biol. Open, 5: 220-228. [ Links ]

Currie, R.J., W.A. Bennett & T.L. Beitinger. 1998. Critical thermal minima and maxima of three freshwater game-fish species acclimated to constant temperatures. Environ. Biol. Fish., 51: 187- 200. [ Links ]

Dalvi, R.S., A.K. Pal, L.R. Tiwari, T. Das & K. Baruah. 2009. Thermal tolerance and oxygen consumption rates of the catfish Horabagrus brachysoma (Gunther) acclimated to different temperatures. Aquaculture, 295: 116-19. [ Links ]

Díaz, F., E. Sierra, F. Bückle & A. Garrido. 1998. Critical thermal maxima and minima of Macrobrachium rosenbergii (Decapoda: Palemonidae). J. Therm. Biol., 23: 381-385. [ Links ]

Díaz, F., A.D. Re-Araujo, E. Sierra & G. Amador. 2004. Behavioural thermoregulation and critical limits applied to the culture of red claw crayfish Cherax quadricarinatus (Von Martens). Fresh. Crayfish, 14: 90-98. [ Links ]

Díaz, F., A.D. Re, R.A. González, L.N. Sánchez, G. Leyva & F. Valenzuela. 2007. Temperature preference and oxygen consumption of the largemouth bass Micropterus salmoides (Lacépède) acclimated to different temperatures. Aquacult. Res., 38: 1387-1394. [ Links ]

El-Sayed, A.F.M. 2006. Environmental requirements. In: A.F.M. El-Sayed. (ed.). Tilapia culture. CABI Publishing, Oxfordshire, pp. 34-36. [ Links ]

Eme, J. & W.A. Bennett. 2009. Critical thermal tolerance polygons of tropical marine fishes from Sulawesi, Indonesia. J. Therm. Biol., 34(5): 220-225. [ Links ]

Farrell, A.P. 2013. Aerobic scope and its optimum temperature: clarifying their usefulness and limitations- correspondence on J. Exp. Biol., 216: 2771-2782. [ Links ]

Farrell, A.P. 2016. Pragmatic perspective on aerobic scope: peaking, plummeting, pejus and apportioning. J. Fish Biol., 88: 322-343. [ Links ]

Ferreira, E.O., K. Anttila & A.P. Farrell. 2014. Thermal optima and tolerance in the eurythermic goldfish (Carassius auratus): relationships between whole-animal aerobic capacity and maximum heart rate. Physiol. Biochem. Zool., 87: 599-611. [ Links ]

Frederich, M. & H.O. Pörtner. 2000. Oxygen limitation of thermal tolerance defined by cardiac and ventricular performance in the spider crab, Maja squinado. Am. J. Physiol., 279: 1531-1538. [ Links ]

Fry, F.E.J. 1947. Effects of the environment on animal activity. Ontario Fish. Res. Lab. Publn., 55: 1-62. [ Links ]

Fry, F.E.J. 1971. The effect of environmental factors on the physiology of fish. Fish. Physiol., 6: 1-98. [ Links ]

Golovanov, V.K., 2013. Ecophysiological patterns of distribution and behavior of freshwater fish in thermal gradients. J. Ichthyol., 53: 252-280. [ Links ]

González, R.A., F. Díaz, A. Licea, A.D. Re, L.N. Sánchez & Z. García-Esquivel. 2010. Thermal preference, tolerance and oxygen consumption of adult white shrimp Litopenaeus vannamei (Boone) exposed to different acclimation temperatures. J. Therm. Biol., 35: 218-224. [ Links ]

Gunderson, A.R. & J.H. Stillman. 2017. Plasticity in thermal tolerance has limited potential to buffer ectotherms from global warming. Proc. Roy. Soc. B, 282: 20150401. [ Links ]

He, Y., X. Wu, Y. Zhu, H. Li, X. Li & D. Yang. 2014. Effect of rearing temperature on growth and thermal tolerance of Schizothorax (Racoma) kozlovi larvae and juveniles. J. Therm. Biol., 46: 24-30. [ Links ]

Instituto Nacional de Estadística y Geografía (INEGI). 2015. Cuadernillos Municipales de Martínez de la Torre Veracruz, Record Meteorológico, Instituto Nacional de Estadística y Geografía, 10 pp. [ Links ]

Jobling, M. 1981. Temperature tolerance, and the final preferendum- rapid methods for assessment of optimum growth temperatures. J. Fish. Biol., 19: 439-455. [ Links ]

Johnson, J.A. & S.W. Kelsch. 1998. Effect of evolutionary thermal environment on temperature preference relationships in fish. Environ. Biol. Fish., 53: 447-458. [ Links ]

Jost, J.A., S.M. Podolski & M. Frederich. 2012. Enhancing thermal tolerance by eliminating the pejus range: a comparative study with three decapod crustaceans. Mar. Ecol. Prog. Ser., 444: 263-274. [ Links ]

Kelsch, S.W. 1996. Temperature selection and performance by bluegills: evidence for selection in response to available power. T. Am. Fish. Soc., 125: 948-955. [ Links ]

Kelsch, S.W. & W.H. Neill. 1990. Temperature prefe-rence versus acclimation in fishes: selection for changing metabolic optima. T. Am. Fish. Soc., 119: 601-610. [ Links ]

Kir, M., M. Can Sunar & B.C. Altindag. 2017. Thermal tolerance and preferred temperature range of juvenile meagre acclimated to four temperatures J. Therm. Biol., 65: 125-129. [ Links ]

Larios, E. 2014. Temperatura preferida, temperaturas, críticas y respuestas metabólicas de Lutjanus guttatus (Steindachner, 1869), ante diferentes temperaturas de aclimatación. Tesis Maestro en Ciencias, CICESE, B.C., Ensenada, 84 pp. [ Links ]

Lee, C.G., A.P. Farrel, A. Lotto, M.J.S. MacNutt, G. Hinch & M.C. Healey. 2003. The effect of the temperature on swimming performance and oxygen consumption in adult sockeye (Oncorhynchus nerka), and coho (O. kisutch) salmon stocks. J. Exp. Biol., 206: 3239-3251. [ Links ]

Lutterschmidt, W.I. & V.H. Hutchinson. 1997. The critical thermal maximum: history and critique. Can. J. Zool., 75: 1561-1574. [ Links ]

Moon, T.W. & G.G. Foster. 1995. Tissue carbohydrate metabolism, gluconeogenesis, and hormonal and environmental influences. In: P.W. Hochachka & T.P. Mommsen (eds.). Metabolic and adaptational biochemistry. Elsevier, Amsterdam, pp. 65-100. [ Links ]

Muñoz-Córdova, G. & M. Garduño-Lugo. 2003. Mejoramiento genético en tilapia: sistema de cruzamiento y mecanismos genéticos en la determinación del color. Universidad Nacional Autónoma de México, Sistema de Investigación del Golfo de México del Consejo Nacional de Ciencia y Tecnología, 84 pp. [ Links ]

Norin, T., H. Malte & T.D. Clark. 2014. Aerobic scope does not predict the performance of a tropical eurythermal fish at elevated temperatures. J. Exp. Biol., 217: 244-251. [ Links ]

Noyola, J., C. Caamal-Monsreal, F. Díaz, D. Re, A. Sánchez & C. Rosas. 2013. Thermopreference, tolerance and metabolic rate of early stages Octopus maya acclimated to different temperatures. J. Therm. Biol., 38: 14-19. [ Links ]

Noyola, J., M. Mascaro, F. Díaz, A.D. Re-Araujo, A. Sánchez-Zamora, C. Caamal-Monreal & C. Rosas. 2015. Thermal biology of prey (Melongena corona bispinosa, Strombus pugilis, Callinectes similis, Libinia dubia) and predators (Ocyurus chrysurus, Centropomus undecimalis) of Octopus maya from the Yucatan Peninsula. J. Therm. Biol., 53: 151-161. [ Links ]

Peak, S., C. Barth & R.S. McKinley. 1997. Effect of recovery parameters on critical swimming speed of juvenile rainbow trout (Oncorhynchus mykiss). Can. J. Zool., 75: 1724-1727. [ Links ]

Pérez, E., F. Díaz & S. Espina. 2003. Thermoregulatory behavior and critical thermal limits of the angelfish Pterophyllum scalare (Lichtenstein) (Pisces: Cichlidae). J. Therm. Biol., 28: 531-537. [ Links ]

Pörtner, H.O. 2001. Climate change and temperature-dependent biogeography: oxygen limitation of thermal tolerance in animals. Naturwissenschaften, 88: 137-146. [ Links ]

Pörtner, H.O. 2000. Oxygen-and capacity-limitation of thermal tolerance: a matrix for integrating climate-related stressor effects in marine ecosystems. J. Exp. Biol., 213: 881-893. [ Links ]

Priede, I.G. 1977. Natural selection for energetic efficiency and the relationship between activity level and mortality. Nature, 267: 610-611. [ Links ]

Ramírez-Paredes, J.G., M. Garduño-Lugo & G. Muñoz-Córdova. 2012. Productive performance of a new synthetic red tilapia population Pargo-UNAM compared with that of wild-type Nile tilapia (Oreochromis niloticus L.). Aquat. Res., 43: 870-878. [ Links ]

Rezende, E.L., L.E. Castañeda. & M. Santos. 2014. Tolerance landscape in thermal ecology. Funct. Ecol., 28: 799-809. [ Links ]

Reynolds, W.W. & M.E. Casterlin. 1979. Behavioral thermoregulation and the final preferendum paradigm. Am. Zool., 19: 211-224. [ Links ]

Roche, D., S.A. Binning, Y. Bosiger, J.L. Johansen & J.L. Rummer. 2013. Finding the best estimates of metabolic rates in a coral reef fish. J. Exp. Biol., 216: 2103-2110. [ Links ]

Rodríguez-Fuentes, G., M. Murua-Castillo, F. Díaz, C. Rosas, C. Caamal-Monsreal, A. Sánchez, K. Paschke & C. Pascual. 2017. Ecophysiological biomarkers defining the thermal biology of the Caribbean lobster Panulirus argus. Ecol. Indic., 78: 192-204. [ Links ]

Saavedra-Martínez, M.A. 2006. Manejo del cultivo de tilapia. Centro de Investigaciones de Ecosistemas Acuáticos (CIDEA-UCA), Managua, 23 pp. [ Links ]

Sokolova, I.M. & H.O. Pörtner. 2002. Metabolic plasticity and critical temperatures for an aerobic scope in eurythermal marine invertebrate (Littorina saxatilis, Gastropoda: Littorinidae) from different latitudes. J. Exp. Biol., 206: 195-207. [ Links ]

Sokolova, I.M., M. Frederich, R. Bagwe, G. Lanning & A.A. Sukhotin. 2012. Energy homeostasis as an integrative tool for assessing limits of environmental stress tolerance in aquatics invertebrates. Mar. Environ. Res., 79: 1-15. [ Links ]

Somero, G.N. 2004. Adaptation of enzymes to tempe-rature: searching for basic strategies. Comp. Biochem. Physiol. A, 100: 69-73. [ Links ]

Stauffer, J.R. Jr. 1986. Effects of salinity on preferred and lethal temperatures of the Mozambique tilapia, Oreochromis mossambicus (Peters). Water Res. Bull., 22: 205-208. [ Links ]

Suarez, R.K. & T.P. Mommsen. 1997. Gluconeogenesis in teleost fishes. Can. J. Zool., 65: 1869-1882. [ Links ]

Tukey, J.W. 1977. Exploratory data analysis. Addison-Wesley, London, 688 pp. [ Links ]

Watanabe, W.O., D.H. Ernst, M.P. Chassar, R.I. Wicklund & B.L. Olla. 1993. The effects of temperature and salinity on growth and feed utilization of juvenile, sex-reversed male Florida red tilapia cultured in a recirculating system. Aquaculture, 112: 309-320. [ Links ]

Wedemeyer, G.R., F.P. Meyer & L. Smith. 1976. Environmental stress and fish diseases. THF Publications, New Jersey, 192 pp. [ Links ]

Wood, C.M., S.F. Perry & T.W. Moon. 1985. Respiratory, circulatory, and metabolic adjustments to exercise in fish. In: R. Gilles (ed.). Circulation, respiration, metabolism. Springer-Verlag, Berlin, pp. 2-22. [ Links ]

Received: December 29, 2017; Accepted: April 25, 2018

*Corresponding author: Ana Denise Re-Araujo (denisre@cicese.mx)

Corresponding editor: Crisantema Hernández

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