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Article

Comparison of Metabolic Rates of Young of the Year Beluga (Huso huso), Sterlet (Acipenser ruthenus) and Bester Hybrid Reared in a Recirculating Aquaculture System

by
Mirela Crețu
1,2,
Raluca-Cristina Guriencu
1,2,*,†,
Lorena Dediu
1,2,*,† and
Maria-Desimira Stroe
3
1
Faculty of Food Science and Engineering, “Dunărea de Jos” University of Galați, 800008 Galați, Romania
2
Romanian Center for Modelling Recirculating Aquaculture Systems, “Dunărea de Jos” University of Galați, 800008 Galați, Romania
3
Research-Development Institute for Aquatic Ecology, Fisheries and Aquaculture, 800211 Galați, Romania
*
Authors to whom correspondence should be addressed.
These authors contributed equally to this work.
Fishes 2021, 6(4), 46; https://doi.org/10.3390/fishes6040046
Submission received: 23 August 2021 / Revised: 6 October 2021 / Accepted: 7 October 2021 / Published: 9 October 2021

Abstract

:
In the present study, oxygen consumption of two sturgeon species, beluga (Huso huso), sterlet (Acipenser ruthenus), and their hybrid reared in a recirculating aquaculture system were compared over body intervals from 54–107 g to determine the interspecific variation of metabolic rate. Metabolic rates were measured using the intermittent-flow respirometry technique. Standard oxygen consumption rates (SMR, mg O2 h−1) of sterlet were 30% higher compared with beluga and 22% higher compared with bester hybrid. The routine metabolic rate (RMR, mg O2 h−1) averaged 1.58 ± 0.13 times the SMR for A. ruthenus, 1.59 ± 0.3 for H. huso, and 1.42 ± 0.15 for the hybrid bester. However, the study revealed no significant differences (p > 0.05) between mean values of SMR and RMR for beluga and bester hybrid. The scaling coefficient reflected a closed isometry for the hybrid (b = 0.97), while for the purebred species the coefficient of 0.8 suggests a reduction in oxygen consumption with increasing body mass. These findings may contribute to understanding the differences in growth performances and oxygen requirements of the studied species reared in intensive aquaculture system.

Graphical Abstract

1. Introduction

Aquaculture is ultimately a multidisciplinary industry that benefits from several scientific disciplines, including biology, ecology, animal behavior, and engineering [1]. The fast development of highly intensive production systems such as recirculating aquaculture systems (RAS) was possible as a result of the common scientific effort of both engineering science, to optimize system design or waste management [2,3], and biological science, aiming to understand the physiological requirements of the cultivated species under intensive conditions. Considering the relatively high cost of water pumping or oxygen generation in recirculating aquaculture systems, it is important to understand the oxygen requirements of cultivated species under intensive conditions [4]. Chebanov et al., 2011 [5], suggests that the equipment for thermoregulation, water degassing, aeration and oxygenation, part of the rearing systems, should be incorporated at sufficient capacity, precalculated based on species’s metabolic rates.
Standard metabolic rate (SMR) is defined for whole organisms exhibiting minimal functional activity, i.e., in the total absence of voluntary muscular movements and when no food was being digested or absorbed [6]. However, whenever subjects show some minor activity in a respirometer (swimming or maintaining position) many authors prefer the term routine metabolic rate (RMR), which includes a minor cost of the activity [7,8]. Generally, SMR is correlated with growth trajectories, maximum aerobic performance, and some behaviors [9,10] and has an important role in ecological fitness.
The metabolic rates of fish are influenced by multiple factors [11,12]. Between those factors, the most important are body weight and temperature [13]. In general, body weight increase leads to the resizing of the whole body. This change corresponds to the growth of body muscles, which efficiently transfer the energy, optimizing the locomotion and routine activity of the body [14]. On the other hand, body mass constrains the metabolic rate and assimilated energy, thus influencing the entire life cycle of a species, including their growth, reproduction, and survival [15,16,17].
In aquaculture, respirometry targets several purposes. Some examples may include the fish body’s ability to interact with the husbandry conditions (e.g., diet, temperature, water quality, stocking density, and live transport) [5]. Others are related to the construction of the bioenergetic models, which are widely used as an analytical tool to address a broad range of questions in physiology, ecology, aquaculture, and fisheries management (e.g., feeding and growth of fish at different life stages, evaluation of the impact of invasive species on aquatic ecosystems, contaminant accumulation by fish, effects of climate change on foraging, growth, and mortality of fishes, etc.) [18,19,20].
It is well known that the Acipenserides are famous for their large size, superior meat quality, and their fish product, caviar [21,22]. That is why, in the last decade, the production of sturgeon in aquaculture has rapidly increased, aside to cover the market demands [23], but also to respond to the restocking purposes under international conservation programs [24]. Most of the respirometry studies of sturgeon species have followed also the relationships between MO2 and body mass [25], temperature [26,27,28], or feeding management [29]. However, few species have been subjected to routine metabolic rate evaluation: A. brevirostrum [26,30], A. medirostris [31,32], A. naccarii [33], A. oxyrinchus [34] and currently large variability in the data exists due to different fish sizes analyzed, rearing conditions or methodology used. Regarding Ponto–Caspian sturgeon species or hybrids, there are no comparative studies about metabolic traits available according to our knowledge.
Sometimes in some farms, different species of sturgeon are bred in intensive conditions, within the same RAS, without considering different physiological requirements for oxygen or having sufficient insight into their metabolic rates. Hence, in the present research, we aimed to assess the interspecific variability of metabolic rates represented as Standard metabolic rate (SMR) and Routine metabolic rate (RMR) of beluga, sterlet, and their hybrid (Huso huso × Acipenser ruthenus) reared in the specific conditions of a RAS. Thus, measured metabolic rates serve for comparison and their relationship to body mass will be discussed within the framework of existing data available on other sturgeon species. Knowledge of oxygen consumption patterns of the three species will provide basic information for further studies on sturgeon physiology with higher applicability in RAS design for the aquaculture of sturgeon.

2. Materials and Methods

2.1. Fishes

Fishes were obtained from a private fish farm, Danube Research Consulting Company (DRC) from Tulcea County, Romania. Before the experiment, fishes were raised for 30 days in a recirculating aquaculture system, at the Romanian Center for the Modeling of Recirculating Aquaculture Systems (MoRAS, www.moras.ugal.ro, accessed on 5 June 2021), a facility of University Dunărea de Jos, Galați, România (Supplementary Figure S1).
During the accommodation period, fish were fed twice per day (at 8:00 and 16:00), at a feeding level of 2% body weight (% BW day−1), with a commercial feed (1 mm diameter, 54% protein, 15% lipids, 0.5% fiber, ash, and 21.1 kJ g−1; Alltech Coppens, Leende, The Netherlands). During the experiment duration, a 11:13 h light:dark cycle was maintained. All the fishes were growing in the same technological condition at a stocking density of 4.50 kg m−3. At the start of the experiment, all the fishes were seven months old.
Additionally, during this period, water quality was monitored daily, with the help of the sensors integrated into the RAS, for temperature (22.04 ± 1.16 °C), dissolved oxygen (7.38 ± 1.09 mg L−1), pH (7.53 ± 1.27 pH units), and ammonium (0.27 ± 0.2 mg L−1). The concentrations of nitrite (0.03 ± 0.01 mg L−1) and nitrates (33.45 ± 9.23 mg L−1) were confirmed weekly with Spectrophotometer Nova 400, compatible with Merck kits (Merck, Darmstadt, Germany).
After one month, nine fishes from each species were randomly selected in such a manner to have more or less the same size range among species (Table 1).

2.2. Respirometry Tests

The measurements of oxygen consumption MO2 (mg O2 kg−1 h−1) were assessed through the intermittent-flow respirometry technique. Intermittent-flow combines the principles of closed-system and open-system respirometry [26,35,36].
The respirometer system (Loligo® Systems, Viborg, Denmark) contains four acrylic chambers with a volume of 2.6 L each, and was placed in an isolated room to diminish any fish disturbance which could lead to erroneous records of oxygen consumption. The chambers were submerged in a black tank with a volume of 200 L (Figure 1). Special barriers made from black plexiglass were placed to avoid visual contact between experimental fish in the chambers. Fish were placed in three chambers of the respirometer, while the fourth was left empty in order to measure the background respiration. The chambers were connected to a computer through a DAQ m instrument (Loligo® Systems, Viborg, Denmark) which is used for data acquisitions and relay controlling in combination with Loligo software (Loligo® Systems, Viborg, Denmark).
The respirometry system comprised also a flush pump, recirculation pump, oxygen electrodes, temperature probe and a steel coil for water temperature control. The oxygen electrodes and temperature probe were connected to the Witrox equipment (Loligo® Systems, Viborg, Denmark). The recirculation pump runs continuously to ensure the proper mixing of the water inside the metabolic chambers and the passage of water through the oxygen electrode, while the flush pump exchanges water from inside the respirometer with water from the ambient tank between the measurement intervals. During the periods of oxygen consumption measurements, the flush pump was turned off while the recirculation pump remained on. After this interval, the flush pump turns on and flushes out the water from the respirometer, by replenishing it with ambient tank water [26]. One complete measurement cycle (loop) consists of an open-system flush period (F—120 s) and a closed-system, metabolism determination cycle, which itself is made up of a waiting period (W—60 s) and a measurement period (M—240 s) [36].
Oxygen content (% air saturation; O2 saturation) of the water in the tank was controlled using air stones and the oxygenation level was kept over 95% O2 saturation. During all respirometer experiments, the water temperature was 22.09 ± 0.54 °C. Before each test, the oxygen sensors from the respirometer system were calibrated under 100% oxygen saturated water and the chambers were cleaned and disinfected.
The fishes used in the respirometry experiments were in a postabsorptive state, feeding being stopped 24 h before testing. Before fish testing, the body weight and length were measured. All measurements were performed under anesthesia with phenoxyethanol (8 mL 40 L−1 of water for 5 min) [37] and all efforts were made to minimize suffering and reduce the number of fish used.

2.3. RMR and SMR Calculations

Using the automatic values taken during each measuring phase, the program calculates the mass-specific oxygen rates (mg O2 kg−1 h−1), according to the equations:
MO2 = ([O2]in − [O2] out) × F/BW
where: F = water flow rate (L h−1); [O2] in = oxygen content in water inflow (mg O2 L−1); [O2] out = oxygen content in water outflow (mg O2 L−1); BW = body-weight of the fish introduced in the experiment (kg).
From all the obtained measurements only oxygen consumption rates with a regression coefficient greater than 0.95 [38,39] were taken into consideration to calculate the routine and standard metabolism. For each test group, the routine metabolic rates (RMR) were calculated as the average of the data after the first 4h of accommodation was excluded, while SMR was calculated as the average of the lowest 10% from the measurements of MO2 values [27,40].

2.4. Statistical Analyses

All the obtained data were analyzed using SPSS 21 (SPSS Inc., Chicago, IL, USA). The values in tables are presented as an average ± standard error. The normality of the data used for statistical analysis was determined by Kolmogorov–Smirnov tests. One-way ANOVA was used to detect the differences in SMR and RMR mean values of different sturgeons. If differences among species were recorded, a Duncan test was performed. A p-value lower than 0.05 was considered statistically significant.
Slopes and intercepts of linear regressions describing the relationship of mass to respiration rate were assessed across the three species, after log10 transformation of the data. Regression analyses were used to generate parameters for predictive models of oxygen consumption, according to the equation:
SMR = a × Mb
where “a” is the scaling coefficient (intercept) and “b” is the scaling exponent (slope).

3. Results

Each fish was kept in the respirometer for 24 h. Due to the stress installed during handling, after the transfer to the respirometer, the oxygen consumption of the fish was higher for about 3 h. However, for the validity of the measurements, the adaptation phase was set at 4 h. When the measurements were made, the fish were quiet, the oxygen consumption remaining constant during the respirometry tests. This fact indicates a rapid adaptation of fish to the metabolic chambers.
During the respirometry trial the background respiration measured in the empty chamber was insignificant (<5% of total measured metabolism). RMR was calculated as the mean of all the MO2 measurements during the 20-h respirometry period (after removing the first four hours), and SMR was calculated by taking the mean of the lowest 10% of the MO2 measurements. If abnormal outliers were identified (higher oxygen consumptions) due to the spontaneous activity, we removed these values from the calculations [7] (Figure 2).
The mean values of standard (SMR-mg O2 kg−1 h−1) and routine metabolic rates (RMR-mg O2 kg−1 h−1) for the experimental variants are presented in Figure 3. Mean SMR values were 276.49 ± 27.37 mg O2 kg−1 h−1 for sterlet, 211.64 ± 17.26 mg O2 kg−1 h−1 for beluga, and 226.9 ± 9.51 mg O2 kg−1 h−1 for bester hybrid.
Mean RMR values were 437.49 ± 59.21 mg O2 kg−1 h−1 for sterlet, 338.37 ± 71.38 mg O2 kg−1 h−1 for beluga, and 320.35 ± 25.76 mg O2 kg−1 h−1 for bester hybrid. The statistical analysis ANOVA showed significant differences (p ˂ 0.05) between the obtained data for the RMR and SMR between the sterlet and the other two species (beluga and bester). No significant values (p > 0.05) were recorded between the obtained RMR and SMR of beluga and the hybrid.
The mean SMR values were around 17 mg O2 h−1 for Beluga and hybrid while for Sterlet was approximately 20% higher. The routine metabolic rate averaged 1.58 ± 0.13 times the SMR for Sterlet, 1.59 ± 0.3 for Beluga, and 1.42 ± 0.15 for the hybrid (Table 2).
The relationships between standard metabolic rate and body mass for the three species are presented in Figure 4. All obtained data were log10 transformed and the regression analysis was used to describe the relationship between mass and fish respiration rate.
The scaling coefficients and the scaling exponents for all of these relationships are listed in Table 3. Slopes from the regressions were not statistically different between bester and beluga, but were statistically higher in the case of sterlet sturgeon. Additionally, it can be observed that large fish consume more oxygen, which is reflected in higher metabolic rates than small fish, but on a unit weight basis, small fish will consume more oxygen than larger fish [41].

4. Discussion

In recirculating aquaculture systems, due to high operational costs, oxygen supplementation must be judiciously estimated in order to cover both the physiological needs of the cultured species [42] and the chemical and biological consumption of oxygen due to the transformation processes of metabolites [43]. Understanding the metabolism of sturgeons is therefore relevant for improving RAS profitability.
The results of the present study revealed significant differences in the metabolism of the sterlet sturgeon, beluga, and the bester hybrid. Observations of higher locomotor activity of the sterlet were confirmed by a higher standard and routine metabolic rates measured during trials. The RMR (mg O2 kg−1 h−1) values obtained in our experiment are slightly higher compared with those reported by other authors for sturgeon species (Table 4). However, it is noteworthy that the used experimental conditions (fish weight, feeding regime, temperatures) were different than those from the present trial.
Among other authors quantifying RMR in sturgeons, Burggren and Randall [44] also reported RMR values around 270 mg O2 kg−1 h−1 for the Acipenser transmontanus, with a body weight of 80 g. Similarly, Zhang et al. in 2017 [30] reported a routine metabolism of 253 ± 18 mg O2 kg−1 h−1 for Acipenser brevirostrum, with a body weight of 100 g (Table 4).
The results of the present study, and other similar studies (Table 4), emphasize the lessening of metabolism with the increase of body weight. However, the metabolic rate variation does not depend only on weight but rather on of a series of intrinsic and extrinsic factors [41]. For example, some authors consider that a lower metabolic rate of some sturgeon species could partially be assigned to their depressed swimming ability [45]. The exposed aspects reinforce the idea that sturgeons represent a distinct group of fish, intermediates between sharks and more evolved bony fish (subclass Neopterygii), with special morphophysiology, which requires more complex studies [45]. The high diversity of data is reflected also by the high variability of measurement conditions (different sizes, temperatures, feeding regime) and therefore to the above-mentioned controversy.
Regarding interspecific oxygen consumption, the higher oxygen consumption of sterlet compared to beluga and bester may illustrate a different allocation of energy in the body [52]. This hypothesis is supported by Biro and Stamps [53] who reported a positive relationship between metabolism and movement, explained by the fact that individuals that display intrinsically higher levels of activity may also develop an increased physiological capacity to facilitate the increased rate of movement. Sterlet, unlike anadromous migratory fish that perform long migrations a in limited time, is a potadromous species that resides in freshwater for its whole lifecycle, making only short migrations for spawning [54,55]. Thus, the higher swimming capacity of Danube sterlet could be regarded as a physiological adaptation to cope with the strong currents of the river. Beluga and bester hybrid showed a similar pattern of oxygen consumption, with no significant differences (p > 0.05) for both SMR and RMR. Therefore, the bester hybrid showed an apparent paternal inheritance of some physiological metabolic traits, demonstrated also for Salmo salar [56].
Because SMR is energetically expensive [15], a lower SMR could be considered more adaptive because the energy excess is directed for growth and reproduction. The lower SMR and RMR of beluga may be attributed to their flexible adaptation to environmental conditions during the nonmigratory phase, but this hypothesis should be confirmed by future studies.
The findings of the present study showed an inversely proportional relationship between the metabolic rate (SMR and RMR expressed as mg O2 kg−1 h−1) and body mass. This trend is also reported by other authors [4,57,58,59], which state that the oxygen absorption capacity per unit mass is lower in larger fish compared to smaller ones.
Large animals generally have higher absolute metabolic rates than small animals, but on a mass-specific basis, small animals usually out-pace larger animals in their rates of energy expenditure [60]. Metabolic rate (MR), therefore, changes allometrically with body mass (M) according to the equation MR = a × Mb, where a is the scaling coefficient (intercept), and b is the scaling exponent. Usually, the value of scaling exponents, calculated for some species of bonefish varies between 0.4 and 1 [61]. According to Glazier 2005 [62], an organism with an isometric scaling coefficient (“1”) benefits from a direct proportionality between body mass and different physiological processes, especially respiration, as the rate of oxygen consumption of an organism is an interaction between a multitude of processes (substrates that perform metabolic combustion, waste disposal, physical activity or cellular respiration at the level of various organs) [63]. The majority of the authors reported a scaling exponent for fish between 0.7 and 0.88 [64,65].
In this study, the values of the scaling coefficient are lower than those reported for other species. For example, Patterson et al., 2013 [51], which also reported the same trend of decreasing oxygen consumption with increasing body weight, shows a value of 0.91 calculated for the species Polyodon spathula. This aspect indicates a reduction in specific oxygen consumption, but it is not so pronounced as in the case of bony fish. For example, for flatfish, lower exponents (b between 0.5–0.7) were reported [66]. Mayfield and Cech [31], reported a value greater than 1 (1.1 to 11 °C) for Acipenser medirostris, which shows a proportional increase in oxygen consumption per measure unit area (grams). In our study, the scaling coefficient reflects a near isometry for the hybrid (b = 0.97) while for the purebred species the coefficient of 0.8 suggests a reduction in oxygen consumption with increasing body mass. Thus, there is an interspecific variability in the relationship between the standard metabolic rate and body mass, which is a variability also reported by other authors [64].
This finding may also have importance in understanding the fate of some sturgeon species in nature, in the context of climate change. Rising temperature is the main factor for oxygen limitation in aquatic ecosystems, and in this context, aerobic metabolism may be a fundamental mechanism driving the response of fish species to climate warming [67].

5. Conclusions

The present study focused on assessing metabolic traits of two different sturgeon species and their hybrid reared in recirculating aquaculture systems. The results emphasized that sterlet exhibited 22–30% higher oxygen consumption rates when compared with hybrid bester and beluga.
For RAS operation, the oxygen supply is correlated with the production cost and therefore producers have to be aware of the metabolic differences among species. In the purebred species, the scaling coefficient suggests a more pronounced reduction in oxygen consumption with an increase in body mass, while for the hybrid, for the body mass range tested here, a near isometry was recorded. These results also contribute to the knowledge of the physioecology of sturgeons, and bring new insights for the conservation of wild populations. Understanding hybrid’s metabolic traits inheritance patterns is also important both for aquaculture and conservation ecology, since the presence of hybrids is also reported in natural waters.

Supplementary Materials

The following are available online at https://www.mdpi.com/article/10.3390/fishes6040046/s1: Figure S1: The scheme of the recirculating aquaculture system.

Author Contributions

Conceptualization, M.C., R.-C.G. and L.D.; methodology, R.-C.G. and L.D.; formal analysis, R.-C.G.; investigation, R.-C.G., M.C. and M.-D.S.; writing—M.C., L.D. and R.-C.G. All authors have read and agreed to the published version of the manuscript.

Funding

This paper was supported by the project CNFIS-FDI-2021- 0443. Active measures to increase and streamline the capacity for research, development, innovation and technology transfer at the “Dunărea de Jos” University of Galati—CEREX-UDJG_2021. The equipment used in this study belong to the infrastructure of UDJ Research Center MoRAS (www.moras.ugal.ro, accessed on 5 June 2021).

Institutional Review Board Statement

The procedures presented in this study were approved by the Ethics Committee of the University in accordance with the Experimental Certificate of Animal Use (no. 200/14). The study was conducted according to the guidelines of the EC Directive 86/609/EEC regarding the protection of animals used for experimental and other scientific purposes.

Data Availability Statement

All the data are available from the first author, and can be delivered if required.

Acknowledgments

The authors would like to thank the Ministry of Agriculture and Rural Development of România for financially supporting this research under budget code ADER 13.1.2.

Conflicts of Interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

References

  1. Pillay, T.V.R.; Kutty, M.N. Aquaculture: Principles and Practices, 2nd ed.; Blackwell Publishing: Hoboken, NJ, USA, 2005; pp. 7–41. [Google Scholar]
  2. Badiola, M.; Mendiola, D.; Bostock, J. Recirculating Aquaculture Systems (RAS) analysis: Main issues on management and future challenges. Aquac. Eng. 2012, 51, 26–35. [Google Scholar] [CrossRef] [Green Version]
  3. Xiao, R.; Wei, Y.; An, D.; Li, D.; Ta, X.; Wu, Y.; Ren, Q. A review on the research status and development trend of equipment in water treatment processes of recirculating aquaculture systems. Rev. Aquac. 2019, 11, 863–895. [Google Scholar] [CrossRef]
  4. Cook, J.T.; McNiven, M.A.; Sutterlin, A.M. Metabolic rate of pre-smolt growth-enhanced transgenic Atlantic salmon (Salmo salar). Aquaculture 2000, 188, 33–45. [Google Scholar] [CrossRef]
  5. Chebanov, M.; Rosenthal, H.; Gessner, J.; van Anrooy, R.; Doukakis, P.; Pourkazemi, M.; Williot, P. Sturgeon hatchery practices and management for release—Guidelines. FAO Fish. Aquac. 2011, 110. [Google Scholar]
  6. Paschke, K.; Agüero, J.; Gebauer, P.; Díaz, F.; Mascaró, M.; López-Ripoll, E. Comparison of aerobic scope for metabolic activity in aquatic ectotherms with temperature related metabolic stimulation: A novel approach for aerobic power budget. Front. Physiol. 2018, 9, 1438. [Google Scholar] [CrossRef]
  7. Chabot, D.; Steffensen, J.F.; Farrell, A.P. The determination of standard metabolic rate in fishes. J. Fish Biol. 2016, 88, 81–121. [Google Scholar] [CrossRef] [PubMed]
  8. Blanco, E.; Reglero, P.; Ortega, A.; Folkvord, A.; Gándara, F.; de Rojas, A.H.; Moyano, M. First estimates of metabolic rate in Atlantic bluefin tuna larvae. J. Fish Biol. 2020, 97, 1296–1305. [Google Scholar] [CrossRef] [PubMed]
  9. Burton, T.; Killen, S.S.; Armstrong, J.D.; Metcalfe, N.B. What causes intraspecific variation in resting metabolic rate and what are its ecological consequences? Proc. R. Soc. B 2011, 278, 3465–3473. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  10. Norin, T.; Clark, T.D. Measurement and relevance of maximum metabolic rate in fishes. J. Fish Biol. 2016, 88, 122–151. [Google Scholar] [CrossRef] [PubMed]
  11. Zupa, W.; Alfonso, S.; Gai, F.; Gasco, L.; Spedicato, M.T.; Lembo, G.; Carbonara, P. Calibrating Accelerometer Tags with Oxygen Consumption Rate of Rainbow Trout (Oncorhynchus mykiss) and Their Use in Aquaculture Facility: A Case Study. Animals 2021, 11, 1496. [Google Scholar] [CrossRef]
  12. Nelson, J. Oxygen consumption rate v. rate of energy utilization of fishes: A comparison and brief history of the two measurements. J. Fish Biol. 2016, 88, 10–25. [Google Scholar] [CrossRef] [Green Version]
  13. Gillooly, J.F.; Charnov, E.L.; West, G.B.; Savage, V.M.; Brown, J.H. Effects of size and temperature on developmental time. Nature 2002, 417, 70–73. [Google Scholar] [CrossRef]
  14. Helfman, G.S.; Collette, B.B.; Facey, D.E.; Bowen, B.W. The diversity of fishes. Biology, Evolution, and Ecology, 2nd ed.; John Wiley & Sons: Hoboken, NJ, USA, 2009; pp. 57–165. [Google Scholar]
  15. Nagy, K.A.; Girard, I.A.; Brown, T.K. Energetics of free ranging mammals, reptiles, and birds. Annu. Rev. Nutr. 1999, 19, 247–277. [Google Scholar] [CrossRef]
  16. Lovegrove, B.G. The zoogeography of mammalian basal metabolic rate. Am. Nat. 2000, 156, 201–219. [Google Scholar] [CrossRef]
  17. Schaefer, J.; Walters, A. Metabolic cold adaptation and developmental plasticity in metabolic rates among species in the Fundulus notatus species complex. Funct. Ecol. 2010, 24, 1087–1094. [Google Scholar] [CrossRef] [Green Version]
  18. Armstrong, J.B.; Schindler, D.E. Excess digestive capacity in predators reflects a life of feast and famine. Nature 2011, 476, 84–87. [Google Scholar] [CrossRef]
  19. Madenjian, C.P. Encyclopedia of Fish. Physiology: From Genome to Environment, 1st ed.; Academic Press: Oxford, UK, 2011; pp. 1675–1680. [Google Scholar]
  20. Canale, R.P.; Breck, J.E.; Shearer, K.D.; Neely, K.G. Validation of a bioenergetic model for juvenile salmonid hatchery production using growth data from independent laboratory feeding studies. Aquaculture 2013, 416–417, 228–237. [Google Scholar] [CrossRef]
  21. Hallajian, A.; Abdolhay, H.; Shadparvar, A.; Yarmohammadi, M.; Yazdanisadati, M. A factorial experiment for heritability estimation of the reproductive traits of the wild Persian sturgeon, Acipenser persicus. Iran. J. Fish. Sci. 2020, 19, 1954–1966. [Google Scholar] [CrossRef]
  22. Safabakhsh, M.; Mohseni, M.; Bahri, A.; Mohammadizadeh, F. Effect of dietary selenium on growth performance, survival rate and biochemical-blood profile of farmed juvenile Beluga (Huso huso). Iran. J. Fish. Sci. 2020, 19, 2077–2088. [Google Scholar] [CrossRef]
  23. Bronzi, P.; Rosenthal, H. Present and future sturgeon and caviar production and marketing: A global market overview. J. Appl. Ichthyol. 2014, 30, 1536–1546. [Google Scholar] [CrossRef]
  24. Ludwig, A.; Lippold, S.; Debus, L.; Reinartz, R. First evidence of hybridization between endangered Sterlets (Acipenser ruthenus) and exotic Siberian sturgeons (Acipenser baerii) in the Danube River. Biol. Invasions 2009, 11, 753–760. [Google Scholar] [CrossRef] [Green Version]
  25. Gisbert, E.; Cech, J.J.; Doroshov, S.I. Routine metabolism of larval green sturgeon (Acipenser medirostris Ayres). Fish Physiol. Biochem. 2001, 25, 195–200. [Google Scholar] [CrossRef]
  26. Kieffer, J.D.; Penny, F.M.; Papadopoulos, V. Temperature has a reduced effect on routine metabolic rates of juvenile shortnose sturgeon (Acipenser brevirostrum). Fish Physiol. Biochem. 2014, 40, 551–559. [Google Scholar] [CrossRef]
  27. Svendsen, J.C.; Genz, J.; Anderson, W.G.; Stol, J.A.; Watkinson, D.A.; Enders, E.C. Evidence of circadian rhythm, oxygen regulation capacity, metabolic repeatability and positive correlations between forced and spontaneous maximal metabolic rates in lake sturgeon Acipenser fulvescens. PLoS ONE 2014, 9, e94693. [Google Scholar] [CrossRef] [Green Version]
  28. Andrei, R.C.; Cristea, V.; Creţu, M.; Dediu, L.; Mogodan, A. The effect of temperature on the standard and routine metabolic rates of young of the year sterlet sturgeon (Acipenser ruthenus). Aquac. Aquar. Conserv. Legis. 2018, 11, 1467–1475. [Google Scholar]
  29. Stiller, K.T.; Vanselow, K.H.; Moran, D.; Riesen, G.; Koppe, W.; Dietz, C.; Schulz, C. The effect of diet, temperature and intermittent low oxygen on the metabolism of rainbow trout. Br. J. Nutr. 2007, 117, 784–795. [Google Scholar] [CrossRef] [Green Version]
  30. Zhang, Y.; Kieffer, D.J. The effect of temperature on the resting and post-exercise metabolic rates and aerobic metabolic scope in shortnose sturgeon Acipenser brevirostrum. Fish Physiol. Biochem. 2017, 43, 1245–1252. [Google Scholar] [CrossRef]
  31. Mayfield, R.B.; Cech, J.J. Temperature Effects on Green Sturgeon Bioenergetics. Trans. Am. Fish. Soc. 2004, 133, 961–970. [Google Scholar] [CrossRef]
  32. Allen, P.J.; Cech, J.J. Age/size effects on juvenile green sturgeon, Acipenser medirostris, oxygen consumption, growth, and osmoregulation in saline environments. Environ. Biol. Fishes 2007, 79, 211–229. [Google Scholar] [CrossRef]
  33. McKenzie, D.; Cataldi, E.; Romano, P.; Owen, S.F.; Taylor, E.W.; Bronzi, P. Effects of acclimation to brackish water on the growth, respiratory metabolism, and swimming performance of young-of-the-year Adriatic sturgeon (Acipenser naccarii). Can. J. Fish. Aquat. Sci. 2001, 58, 1104–1112. [Google Scholar] [CrossRef]
  34. Secor, D.H.; Gunderson, T.E. Effects of hypoxia and temperature on survival, growth, and respiration of juvenile Atlantic sturgeon, Acipenser oxyrinchus. Fish. Bull. 1998, 96, 603–613. [Google Scholar]
  35. Rosewarne, P.J.; Wilson, J.M.; Svendsen, J.C. Measuring maximum and standard metabolic rates using intermittent-flow respirometry: A student laboratory investigation of aerobic metabolic scope and environmental hypoxia in aquatic breathers. J. Fish Biol. 2016, 88, 265–283. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  36. Svendsen, M.B.; Bushnell, S.P.G.; Steffensen, J.F. Design and setup of intermittent-flow respirometry system for aquatic organisms. J. Fish Biol. 2016, 88, 26–50. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  37. Jahanbakhshi, A.; Shaluei, F.; Baghfalaki, M.; Ramazi, F.G.; Ahmadvand, S. Efficacy of 2-phenoxyethanol as an Anesthetic for Two Size of Persian Sturgeon, Acipenser persicus. J. Walailak. 2012, 9, 31–36. [Google Scholar]
  38. Svendsen, M.B.S.; Bushnell, P.G.; Christensen, E.A.F.; Steffensen, J.F. Sources of variation in oxygen consumption of aquatic animals demonstrated by simulated constant oxygen consumption and respirometers of different sizes. J. Fish Biol. 2016, 88, 51–64. [Google Scholar] [CrossRef]
  39. Svendsen, M.B.S.; Andersen, N.R.; Hansen, P.J.; Steffensen, J.F. Effects of Harmful Algal Blooms on Fish: Insights from Prymnesium parvum. Fishes 2018, 3, 11. [Google Scholar] [CrossRef] [Green Version]
  40. Rosewarne, P.J.; Svendsen, J.C.; Mortimer, R.J.G.; Dunn, A.M. Muddied waters: Suspended sediment impacts on gill structure and aerobic scope in an endangered native and an invasive freshwater crayfish. Hydrobiologia 2014, 722, 61–74. [Google Scholar] [CrossRef] [Green Version]
  41. Urbina, M.A.; Glover, C.N. Relationship between fish size and metabolic rate in the oxy conforming inanga Galaxias maculatus reveals size-dependent strategies to withstand hypoxia. Physiol. Biochem. Zool. 2013, 86, 740–749. [Google Scholar] [CrossRef] [PubMed]
  42. Seginer, I.; Mozes, N. A note on oxygen supply in RAS: The effect of water temperature. Aquac. Eng. 2012, 50, 46–54. [Google Scholar] [CrossRef]
  43. Summerfelt, S.T.; Vinci, B.J. Better management practices for recirculating aquaculture systems. In Environmental Best Management Practices for Aquaculture; Tucker, C.S., Hargreaves, J.A., Eds.; John Wiley & Sons: Hoboken, NJ, USA, 2008; Volume 297, pp. 389–426. [Google Scholar] [CrossRef]
  44. Burggren, W.W.; Randall, D.J. Oxygen uptake during hypoxic exposure in the sturgeon Acipenser transmontanus. Respir. Physiol. 1978, 34, 171–183. [Google Scholar] [CrossRef]
  45. Peake, S.J. Swimming and respiration. In Sturgeons and Paddlefish of North America; Le Breton, G.T.O., Beamish, F.W.H., McKinley, R.S., Eds.; Kluwer Academic Publishers: Dordrecht, The Netherlands, 2004; pp. 147–166. [Google Scholar]
  46. Cai, L.; Johnson, D.; Fang, M.; Mandal, P.; Tu, Z.; Huang, Y. Effects of feeding, digestion and fasting on the respiration and swimming capability of juvenile Sterlet sturgeon (Acipenser ruthenus, Linnaeus 1758). Fish Physiol. Biochem. 2016, 43, 279–286. [Google Scholar] [CrossRef] [PubMed]
  47. McKenzie, D.; Piraccini, G.; Papini, N.; Galli, C.; Bronzi, P.; Bolis, C.G.; Taylor, E.W. Oxygen consumption and ventilatory reflex responses are influenced by dietary lipids in sturgeon. Fish Physiol. Biochem. 1997, 16, 365–379. [Google Scholar] [CrossRef]
  48. Cai, L.; Johnson, D.; Mandal, P.; Gan, M.; Yuan, X.; Tu, Z.; Huang, Y. Integrating water flow, locomotor performance and respiration of Chinese sturgeon during multiple fatigue recovery cycles. PLoS ONE 2014, 9, e94345. [Google Scholar] [CrossRef]
  49. Cai, L.; Johnson, D.; Mandal, P.; Gan, M.; Yuan, X.; Tu, Z.; Huang, Y. Effect of exhaustive exercise on the swimming capability and metabolism of juvenile Siberian sturgeon. Trans. Am. Fish. Soc. 2015, 144, 532–538. [Google Scholar] [CrossRef]
  50. Cai, L.; Taupier, R.; Johnson, D.; Tu, Z.; Liu, G.; Huang, Y. Swimming capability and swimming behavior of juvenile Acipenser schrenckii. J. Exp. Zool. A Ecol. Integr. Physiol. 2013, 319, 149–155. [Google Scholar] [CrossRef]
  51. Patterson, J.T.; Mims, S.D.; Wright, R.A. Effects of body mass and temperature on routine metabolism of American paddlefish Polyodon spathula. J. Fish Biol. 2013, 82, 1269–1280. [Google Scholar] [CrossRef] [PubMed]
  52. Steyermark, A.C. A high standard metabolic rate constrains juvenile growth. Zoology 2002, 105, 147–151. [Google Scholar] [CrossRef] [PubMed]
  53. Biro, P.A.; Stamps, J.A. Do consistent individual differences in metabolic rate promote consistent individual differences in behavior? Trends Ecol. Evol. 2010, 25, 653–659. [Google Scholar] [CrossRef]
  54. Gesner, J.; Chebanov, M.; Freyhof, J. Huso huso. The IUCN Red List of Threatened Species 2010: E.T10269A3187455. Available online: https://dx.doi.org/10.2305/IUCN.UK.2010-1.RLTS.T10269A3187455.en (accessed on 13 June 2021).
  55. Furdean, S.; Lalescu, D.; Mihailov, S.A.; Grozea, A. Growth dynamic of the main morphological traits in a sterlet (Acipenser ruthenus) population reared into recirculating aquaculture system, from 2 to 6 months old. Res. J. Agric. Sci. 2017, 49, 128–134. [Google Scholar]
  56. Pakkasmaa, S.; Penttinen, O.P.; Piironen, J. Metabolic rate of Artic charr eggs depends on their parentage. J. Comp. Physiol. B 2006, 176, 387–391. [Google Scholar] [CrossRef]
  57. Brick, M.E.; Cech, J.J. Metabolic responses of juvenile striped bass to exercise and handling stress with various recovery environments. Trans. Am. Fish. Soc. 2002, 131, 855–864. [Google Scholar] [CrossRef]
  58. Enders, E.C.; Boisclair, D.; Boily, P.; Magnan, P. Effect of body mass and water temperature on the standard metabolic rate of juvenile yellow perch, Perca flavescens (Mitchill). Environ. Biol. Fishes 2006, 76, 399–407. [Google Scholar] [CrossRef]
  59. Tran-Duy, A.; Schrama, J.W.; Van Dam, A.A.; Verreth, J.A.J. Effects of oxygen concentration and body weight on maximum feed intake, growth and hematological parameters of Nile tilapia, Oreochromis niloticus. Aquaculture 2008, 275, 152–162. [Google Scholar] [CrossRef]
  60. Schmidt, N.K. Scaling: Why Is Animal Size So Important? Cambridge University Press: Cambridge, UK, 1984; pp. 7–32. [Google Scholar] [CrossRef]
  61. Mitz, S.V.; Newman, M.C. Allometric relationship between oxygen consumption and body weight of mosquitofish, Gambusia affinis. Environ. Biol. Fishes 1989, 24, 267–273. [Google Scholar] [CrossRef]
  62. Glazier, D.S. Beyond the ‘3/4-power law’: Variation in the intra- and interspecific scaling of metabolic rate in animals. Biol. Rev. Camb. Philos. Soc. 2005, 80, 611–662. [Google Scholar] [CrossRef]
  63. Labra, F.A.; Marquet, P.A.; Bozinovic, F. Scaling metabolic rate fluctuations. Proc. Natl. Acad. Sci. USA 2007, 104, 10900–10903. [Google Scholar] [CrossRef] [Green Version]
  64. Clarke, A.; Johnston, N.M. Scaling of metabolic rate with body mass and temperature in teleost fish. J. Anim. Ecol. 1999, 68, 893–905. [Google Scholar] [CrossRef]
  65. White, C.R.; Phillips, N.F.; Seymour, R.S. The scaling and temperature dependence of vertebrate metabolism. Biol. Lett. 2006, 2, 125–127. [Google Scholar] [CrossRef] [Green Version]
  66. Jobling, M. A study of some factors affecting rates of oxygen consumption of plaice, Pleuronectes platessa L. J. Fish Biol. 2006, 20, 501–516. [Google Scholar] [CrossRef]
  67. Rubalcaba, J.G.; Verberk, W.C.; Hendriks, A.J.; Saris, B.; Woods, H.A. Oxygen limitation may affect the temperature and size dependence of metabolism in aquatic ectotherms. Proc. Natl. Acad. Sci. USA 2020, 117, 31963–31968. [Google Scholar] [CrossRef]
Figure 1. The diagram of the intermittent-flow respirometer and the experimental design.
Figure 1. The diagram of the intermittent-flow respirometer and the experimental design.
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Figure 2. Example of oxygen consumption for beluga sturgeon (body weight 79 g). The first four hours and outliners “●” were excluded from the calculation of RMR and SMR.
Figure 2. Example of oxygen consumption for beluga sturgeon (body weight 79 g). The first four hours and outliners “●” were excluded from the calculation of RMR and SMR.
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Figure 3. Mean SMR ± SE (mg kg−1 h−1) and RMR±SE (mg kg−1 h−1) values of sturgeon species during static respirometry trials. Different symbols */** indicate significant differences between values of SMR/ RMR of the studied species.
Figure 3. Mean SMR ± SE (mg kg−1 h−1) and RMR±SE (mg kg−1 h−1) values of sturgeon species during static respirometry trials. Different symbols */** indicate significant differences between values of SMR/ RMR of the studied species.
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Figure 4. Relationships of log10 standard metabolic rate to log10 body mass for different sturgeon species during respirometry trials. Data are presented on log10 axes.
Figure 4. Relationships of log10 standard metabolic rate to log10 body mass for different sturgeon species during respirometry trials. Data are presented on log10 axes.
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Table 1. Mean ± standard error, minimum and maximum values for body mass and length of the tested fishes.
Table 1. Mean ± standard error, minimum and maximum values for body mass and length of the tested fishes.
SpeciesFish Weight (g) Total Length (cm)
Mean ± SEMinimumMaximumMean ± SEMinimumMaximum
Acipenser ruthenus77.33 ± 5.3654.0099.0028.2 ± 1.4023.1029.93
Huso huso84.78 ± 4.4267.00107.0030.2 ± 1.2327.1232.71
Bester75.33 ± 2.5065.0089.0027.9 ± 1.2427.2429.22
No significant differences (p ˃ 0.05) were recorded between individual weight and length of the three sturgeon species (ANOVA).
Table 2. Mean (±SE), minimum and maximum values for SMR and RMR (mg h−1) of sturgeon species during static respirometry trials.
Table 2. Mean (±SE), minimum and maximum values for SMR and RMR (mg h−1) of sturgeon species during static respirometry trials.
SpeciesSMRRMR
Mean ± SEMinMaxMean ± SEMinMax
A. ruthenus21.04 ± 0.96 **17.3324.5133.06 ± 1.17 **29.6338.52
H. huso17.78 ± 0.60 *15.7318.8624.23 ± 1.32 *20.2831.25
Bester17.03 ± 0.38 *15.7318.8624.23 ± 1.32 *20.2831.25
*—No statistical differences (p > 0.05); **—Statistical differences (p ˂ 0.05).
Table 3. Relationship between oxygen uptake and mass of sturgeon species. β and r2 were determined using data in Figure 4 (n = number of tested fish).
Table 3. Relationship between oxygen uptake and mass of sturgeon species. β and r2 were determined using data in Figure 4 (n = number of tested fish).
SpeciesRegression Equations
y = oxygen uptake (mg h−1);
x = mass (g)
r2n
Acipenser ruthenusy = 0.76x0.850.869
H. husoy = 0.69x0.880.789
Bestery = 0.66x0.90.899
Table 4. Mean routine metabolic rate RMR (mg O2 kg−1 h−1) of some sturgeon species.
Table 4. Mean routine metabolic rate RMR (mg O2 kg−1 h−1) of some sturgeon species.
Species Body
Weight (g)
RMR
(mg O2 kg−1 h−1)
Experimental ConditionsReference
T
(°C)
Rearing
System
Fasting Period before Trial
(hours)
Photoperiod
(hours)
Acclimatization Period before Trial
(hours)
A. brevirostrum11309 ± 3325FTS24natural4[26]
100127 ± 8.815FTS24 12 L/12 D2[30]
100199 ± 320 FTS2412 L/12 D12[30]
100253 ± 18 25FTS2412 L/12 D12[30]
A. ruthenus14.58 ± 2.81approx. 32020FTS48natural2[46]
A. oxyrinchus219.35 ± 2.2217 ± 0.02419.7 ± 0.05RAS12natural-[34]
approx. 69200 to 30019.26RAS12natural-[34]
A. naccarii198 ± 0.015110 ± 923 ± 1RAS-natural10[47]
100216 ± 2523 ± 1RAS22natural22[33]
A. sinensis8.38 ± 0.27266.6 ± 30.9419.3–20.8RAS8--[48]
A. baeri14.5 ± 0.8168.29 ± 2.2920 ± 0.5RAS48natural1[49]
A. fulvescens30.51 ± 1.2188.44 ± 3.5417 ± 1FTS4812 L/12 D20[27]
A. medirostris145.7 ± 3.863.36 ± 6.0212 ± 0.01RAS72natural-[32]
30.3 ± 17.527024RAS24natural6[31]
A. schrenckii32.7 ± 1.2295.38 ± 10.4220 ± 0.5RAS7212 L/12 D2[50]
P. spathula500 ± 130157.49 ± 22.5421 ± 0.3P72natural1[51]
Legend: FTS—flow-through system; RAS—recirculating aquaculture system; P—ponds; 12 L/12 D—12 h light/12 h dark.
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Crețu, M.; Guriencu, R.-C.; Dediu, L.; Stroe, M.-D. Comparison of Metabolic Rates of Young of the Year Beluga (Huso huso), Sterlet (Acipenser ruthenus) and Bester Hybrid Reared in a Recirculating Aquaculture System. Fishes 2021, 6, 46. https://doi.org/10.3390/fishes6040046

AMA Style

Crețu M, Guriencu R-C, Dediu L, Stroe M-D. Comparison of Metabolic Rates of Young of the Year Beluga (Huso huso), Sterlet (Acipenser ruthenus) and Bester Hybrid Reared in a Recirculating Aquaculture System. Fishes. 2021; 6(4):46. https://doi.org/10.3390/fishes6040046

Chicago/Turabian Style

Crețu, Mirela, Raluca-Cristina Guriencu, Lorena Dediu, and Maria-Desimira Stroe. 2021. "Comparison of Metabolic Rates of Young of the Year Beluga (Huso huso), Sterlet (Acipenser ruthenus) and Bester Hybrid Reared in a Recirculating Aquaculture System" Fishes 6, no. 4: 46. https://doi.org/10.3390/fishes6040046

APA Style

Crețu, M., Guriencu, R. -C., Dediu, L., & Stroe, M. -D. (2021). Comparison of Metabolic Rates of Young of the Year Beluga (Huso huso), Sterlet (Acipenser ruthenus) and Bester Hybrid Reared in a Recirculating Aquaculture System. Fishes, 6(4), 46. https://doi.org/10.3390/fishes6040046

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