Open-access First report of Patagonian toothfish (Dissostichus eleginoides) metabolic rate and its scaling on a surface culture system

Primeiro relato da taxa metabólica da merluza-negra (Dissostichus eleginoides) e sua escala no sistema de cultura de superfície

Abstract

Dissostichus eleginoides is a benthopelagic, carnivorous fish from circumpolar antarctic waters. It is a deep sea fish distributed up to 2500 m and reaching up to 200 kg, 2 m total length and over 50 years of lifespan. Although it is of commercial interest, with prices between 14-35 US$/kg, studies that allow its cultivation are scarce. D. eleginoides is considered to have a slow metabolism since it lives at low temperatures (2-11 °C) and high pressures (100-250 atmospheres). However, there are no records of their routine aerobic metabolism (or any in fact) and of their mass scaling in tanks captivity on the surface, being the aims of this study. Routine metabolism was measured in fish groups from 3 sizes, a) 2.31 ± 0.08 kg, b) 4.67 ± 0.06 kg and c) 8.97 ± 1.89 kg in two respirometry chambers allowing to perform closed respirometry. The average metabolic rate was 42.91 ± 0.48, 38.61 ± 2.64 and 35.35 ± 1.58 mg O2 kg-1 h-1 along fish sizes, with significant differences between sizes. The calculated scaling exponent was 0.85, similar to that reported for other cold-water fish species measured at the surface. Results show oxygen consumption rates, under surface pressure conditions, comparable to those of G. morhua and salmonids, which allows, preliminarily, to reject the initial hypothesis of a slow metabolism. Although the results are preliminary, they are the first to report on the routine metabolism of this species, making them relevant for future studies. Culture densities of 87.38, 57.77 and 64.92 kg m-3 were estimated for groups a, b and c presenting important advantages and new perspectives for the cultivation of D. eleginoides.

Keywords:
Dissostichus eleginoides; oxygen consumption; fish physiology; scaling

Resumo

Dissostichus eleginoides é um peixe bentopelágico, carnívoro, proveniente de águas profundas antárticas circumpolares até 2.500 m, podendo atingir até 200 kg, 2 m de comprimentoe 50 anos de vida. Embora tenha importância comercial com preços entre 14-35 US$/kg, estudos que permitam o seu cultivo são escassos. D. eleginoides é considerado de metabolismo lento, pois vive em baixas temperaturas (2-11 °C) e altas pressões (100-250 atmosferas). No entanto, não há registros de seu metabolismo aeróbico de rotina e de seu enorme crescimento em tanques de cativeiro na superfície, sendo o objetivo deste estudo. O metabolismo de rotina foi medido em grupos de peixes de três tamanhos, a) 2,31 ± 0,08 kg, b) 4,67 ± 0,06 kg e c) 8,97 ± 1,89 kg em duas câmaras seladas feitas sob medida por respirometria fechada. A taxa metabólica média foi de 42,91 ± 0,48, 38,61 ± 2,64 e 35,35 ± 1,58 mg O2 kg-1 h-1, com diferenças significativas entre os tamanhos. O expoente de escala calculado foi de 0,85, semelhante ao relatado para outras espécies de peixes de água fria medidas na superfície. Os resultados mostram consumo de oxigênio em condições de pressão superficial comparáveis aos de G. morhua e salmonídeos, o que permite, preliminarmente, rejeitar a hipótese inicial de metabolismo lento. Embora os resultados sejam preliminares, eles são os primeiros a relatar o metabolismo de rotina desta espécie, tornando-os relevantes para estudos futuros. Densidades de cultivo de 87,38, 57,77 e 64,92 kg m-3 foram estimadas para os grupos a, b e c, apresentando importantes vantagens e novas perspectivas para o cultivo de D. eleginoides.

Palavras-chave:
Dissostichus eleginoides; consumo de oxigênio; fisiologia dos peixes; escala

1. Introduction

Dissostichus eleginoides (Smitt, 1898), is a deep-water notothenioid fish, belonging to the suborder Perciformes, and commercially known as “Chilean sea bass” or “Patagonian toothfish” (Collins et al., 2010; Reyes et al., 2012). This benthopelagic carnivorous, slow-moving and seemingly solitary fish, inhabits along the Antarctic Polar Front (APF) on the Southern Hemisphere. The bathymetric distribution of this fish ranges from the continental shelf down to 2,500 m depth, depending on water temperatures (Eastman, 1993; Collins et al., 2010; Reyes et al., 2012; Aramayo, 2016; Canales-Aguirre et al., 2018). It has a circumpolar Antarctic distribution, between 45-65 °S latitude on the southern Chilean Patagonia and sub-Antarctic islands. Yet, in the Pacific Ocean, it has been captured between 20 °S off Chile in the North, down to 75°40’S (Eastman, 1993; Laptikhovsky et al., 2006; Collins et al., 2010). Incidentally, it has also been captured near equatorial latitudes, 4 °S off Peru (Aramayo, 2016) and in northwest Atlantic waters near Greenland (Møller et al., 2003).

D. eleginoides fishery operates at around 1000 m depth, and reports significant landings in the APF zone (Collins et al., 2010; Aramayo, 2016; Canales-Aguirre et al., 2018). Exploratory captures first started in the 50’s, but targeted fisheries began in the mid 80's due to its elevated price. Currently, market prices range from US $ 14 to 34 per kg (Grilly et al., 2015; Chile, 2023a). The international fishery of this resource is regulated by the Convention for the Conservation of Antarctic Marine Living Resources (CCAMLR) (Constable et al., 2001) and the main fishing gears are the demersal longline, traps, the autoline system and the Spanish or double-line system with 7,000 hooks (Collins et al., 2010). Catches at CCAMLR zones in 2018 were 11,409 t (from 12,613 authorized) (Constable et al., 2001) and in Chile captures in 2017 were of 4,171 t (1,365 t without CCAMLR Chilean catches) (Chile, 2018). Mean catches among 2009-2014 in Chile were 3,700 t (Chile, 2015), being an important fishery (Arana et al., 1994; Cubillos and Araya, 2007). However, due to overfishing it is considered as vulnerable species to, because of its size and long-life span (Canales-Aguirre et al., 2018). In fact, since 2019 it is considered overexploited, leading to the establishment of a fishing quota of 1,730 t for 2024 within Chilean waters (Chile, 2023b). In recent years, significant efforts have been made to develop the farming technology of D. eleginoides, as to decrease fishing pressure. However, most of the available knowledge is restricted to its taxonomy, biology and ecology, mainly based on its fishery in the wild, but no technology on commercial culture, nor relevant physiological information is available so far, except at experimental scale (Parada, 2010; Reyes et al., 2012).

The Patagonian toothfish can reach over 200 cm length (Collins et al., 2010; Reyes et al., 2012, Canales-Aguirre et al., 2018; Eastman, 2019), with an initial fast growth, and reaching between 30 to 40 cm length at first recruitment (Constable et al., 2001). The length at first maturity is around 98 cm (Pierre, 2017), with mature females normally found around 80–130 cm and males at 57-100 cm (Reyes et al., 2012). D. eleginoides maximum weights recorded are over 200 kg (Collins et al., 2010), with an average longevity of around 30-50 years, but reaching up to 55 years due to low natural mortality <0.2% per year (Constable et al., 2001; Collins et al., 2010; Reyes et al., 2012; Pierre, 2017). Although there is literature on the physiology, cold adaptation and possible effects of global ocean warming on nototenioid fishes, studies on D. eleginoides are scarce (Patarnello et al., 2011; Collins et al., 2010) due to the difficulties associated with its capture and maintenance, logistical challenges for captures at depths below 1,000 m, in addition to changes in pressure other physiological effects that affect survival. In the attempts made in Chile, there have been reported 75% survival rates of after capture and 13% survival per year in maintenance tanks (Reyes et al., 2012).

They live in deep-waters, ranging in temperature between 2-11 °C (and occasionally below 0 °C), and therefore regarded as a species with low metabolism at these low temperatures and high pressures (Johnston and Dunn, 1987; Seibel and Drazen, 2007). It has been reported that D. eleginoides has the capacity to tolerate temperatures below freezing point (-1.86 °C), due to the release of antifreeze molecules either peptides or glycopeptides to the extracellular fluids (Clarke and North, 1991; Eastman, 1993; Collins et al., 2010), which could be lethal for other fish species (Somero, 1991). Like the orange roughy (Hoplostethus atlanticus), the patagonian toothfish is neutrally buoyant (Eastman, 1993, 2019; Patarnello et al., 2011), despite lacking a gas-filled swim bladder (Eastman, 1993; Kloser et al., 1991; Collins et al., 2010). This is achieved by decreasing the mineralization of their skeleton, having only around 0.6% ash content of its whole body weight, and even substituting cartilage for bone in some areas (Collins et al., 2010).

Oxygen consumption is a key parameter in aquaculture to determine carrying capacity for species under intensive culture conditions, at certain temperatures for poikilothermic organisms (Dalvi et al., 2009). A normoxic environment reduces risk of oxygen shortages, ensuring normal growth and feed conversion rates (Encina-Montoya et al., 2011). In most studies, oxygen consumption is measured under conditions of routine metabolism when fish are food restricted (lacking Specific Dynamic Action: SDA), but performing spontaneous and normal activity. The relationship between the oxygen consumption rates (OC) and body mass (M) can be represented by the potential function (OC = aMb), where the intercept of OC is a and the slope of this scaling relationship is b (Schmidt-Nielsen, 1986; Encina-Montoya et al., 2011). As for any other ectotherm, temperature has a big effect on metabolic rates (Dickson and Kramer, 1971), and so metabolic scaling should be measured at a given temperature (Glazier et al., 2020). Yet, the effect of pressure on metabolic rates in marine animals is variable and published studies are less conclusive (Seibel and Drazen, 2007).

In recent years, significant efforts have been made in Chile to develop the farming technology of D. eleginoides in order to decrease fishing pressures (Parada, 2010; Reyes et al., 2012). There are several studies on D. eleginoides related to its fishery, distribution and reproduction, but no reports on routine metabolism, when fish are food restricted and performing a spontaneous, normal activity (Waller, 1992) and on its mass scaling on surface captivity. Such information is valuable for future ecological studies and for future fish farming attempts.

This study ought to provide the first report of D. eleginoides routine metabolism, and its mass scaling on fish maintained in tanks at surface pressures. Owing to it lives at low temperatures (2-11 °C) and high pressures (100-250 atmospheres), we hypothesise a low metabolism.

2. Materials and Methods

2.1. Specimen conditions

Specimens of Dissostichus eleginoides were caught by a fishing boat and brought for farming purposes to the Corporación de Educación La Araucana (FONDEF PDACH, DA09l1003 project) at the Quillaipe Experimental Facility, región de Los Lagos, Chile. Fish were kept for 2 years in 10 m3 fibre tanks at 5 °C, 33 PSU salinity and fed to satiety with fish meat and calamari biscuits every 2 days (Reyes et al., 2012). Fifteen individuals were not fed for a 60-h period prior oxygen consumption (OC) measurements, under a somewhat post absorptive stage, recognizing Specific Dynamic Action (SDA) might take longer at low temperatures (Secor, 2009). Due to farming practices and the high economic value of the fish, we were not allowed to starve the fish for longer, and so we acknowledge that some SDA (Specific Dynamic Action) might still have been present. Selected fish were arranged in three groups accordingly to their mass: a) 2.31 ± 0.08 kg (66.08 ± 0.30 cm), b) 4.67 ± 0.06 kg (71.33 ± 0.27 cm) and c) 8.97 ± 1.89 kg (99.50 ± 11.39 cm). For the size group a, three fish were used in each run, and the experiment was replicated 3 times with different fish. For the second and third group, OC measurements were conducted on individual fish, but also achieving three replicates. Densities of 66.45 kg m-3, 44.84 kg m-3 and 40.25 kg m-3 were achieved for the groups, respectively. All experimental procedures were performed in compliance with relevant laws and institutional guidelines and have been approved by the ethical institutional committee.

2.2. Experimental conditions for oxygen measurement

To measure oxygen consumption, two transparent acrylic rectangular chambers of 0.104 m3 for group a and 0.223 m3 for groups b and c were used. D. eleginoides specimens were acclimatized in the chambers for 2 hours by maintaining an open flow of seawater with an oxygen concentration above 80% air saturation (7.9 to 8.2 mg O2 L-1) and a salinity of 35 PSU. Subsequently, when no signs of stress (movement and gasping) were observed, water flow was stopped and dissolved oxygen was recorded every 5 minutes for 100 minutes or until oxygen saturation fall around 60% (5.7 to 5.9 mg L-1). The chambers were kept in the dark at an average temperature of 5.3 °C. Dissolved oxygen concentration in mg O2 L-1 was recorded with an YSI 550 A oxygen meter.

Routine oxygen consumption was estimated according to Encina-Montoya et al. (2011), using a linear regression of dissolved oxygen concentration records over time inside the chamber. The relationship between oxygen consumption and fish mass was estimated and graphed according to Schmidt-Nielsen, (1986), using the potential function (OC=aWb), where OC is Oxygen Consumption in mg O2 h-1, W is fish mass in kg, and “a” and “b” are the intercept and slope of the metabolic scaling, respectively. The effect of body mass on metabolic rate like oxygen consumption values was determinate using a generalized linear mixed model according Urbina and Glover (2013). Fish condition factor was determined as Fulton’s K index ( K=100*WL3), as the relationship between weight increase (g) and the cube of the fish body length (cm). The carrying capacity was calculated according to Encina-Montoya et al. (2011) using the oxygen consumption data for each average weight in a 1 m3 tank, with a 1,000 L hr-1 flow, an oxygen inlet concentration of 8.1 mg O2L-1 and a minimum outlet concentration of 5.6 mg O2L-1, in the following Equation 1:

O 2 o u t p u t = D O x Q O C x W V (1)

where O2 output was the oxygen in the tank water outlet (mg L-1), DO was the dissolved oxygen inlet (mg L-1), OC the fish oxygen consumption rate (mg O2kg-1h-1), Q the water flow (L h-1) and V was the water tank capacity in L.

2.3. Data analysis

Oxygen consumption rates among fish sizes were compared by an analysis of variance (ANOVA), when the variance normality and homogeneity assumptions were satisfied (Zar, 2010). A posteriori multiple comparisons were done using least significant difference (LSD) tests. Statistical analyses and graphs were conducted on XLSTA 2029.1.1 package for Windows.

3. Results

As expected, mass specific fish OC decreased as fish size increased (Figure 1). The first group had an average oxygen consumption of 42.91 ± 0.48 mg O2 kg-1 h-1, followed by an average value of 39.61 ± 2.64 mg O2 kg-1 h-1 for the second group and a mean of 35.35±1.58 mg O2 kg-1 h-1 the biggest size group. All groups presented a similar condition factor (Condition factor K group a: 0.88±0.02, group b: 1.02±0.01 and group c: 0.91±0.13), but there were significant differences (0.0019 p-value) in the mass specific oxygen consumption between size groups, with each size group being significantly different from each other.

Figure 1
Comparison of D. eleginoides oxygen consumption average in mgO2 kg-1 h-1.

The relationship between oxygen consumption (mg O2 h-1) and fish mass (kg) in D. eleginoides can be expressed as OC = 48.27 W0.85 with an r2 = 0.99 and p-value <0.0001 to the regression model (Figure 2a), the mass scaling exponent was estimated to be 0.85 (Figure 2b).

Figure 2
D. eleginoides metabolism as a function of mass. (a) Regression analysis between wet fish mass (WW, kg) and oxygen consumption (OC) expressed as mg O2 h-1 at 5.3 °C; (b) Regression analysis for the relationship between LN (WW, kg) and LN oxygen consumption (OC), slope (0.85) represents scaling exponent, and dashed lines represent the 95% confidence interval.

A mass balance was made for oxygen according to Encina-Montoya et al. (2011), using the oxygen consumption data for each average weight, a tank of 1 m3, flow of 1,000 L hr-1, O2 inlet concentration of 8.1 mg O2 L-1 and a minimum outlet concentration of 5.6 mg O2 L-1. The estimated culture densities of 87.38, 57.77 and 64.92 kg m-3 were estimated for groups a (2.31 kg), b (4.67 kg) and c (8.97 kg).

4. Discussion

The biology of D. eleginoides is so far poorly understood and studies mainly focused on aspects of its fishery or restricted to some specific topics of its biology and ecology in the natural environment (Reyes et al., 2012). The main problems when collecting and keeping wild fish in captivity stem from the serious injuries they suffer from trawling and the large changes in pressure when they are brought to the surface. In fact, obtaining and keeping fish in good condition was one the main challenges of this study. Besides that, fish turn sensitive to temperatures well above 5 °C, and so oxygen consumption measurements were carried out at an average temperature of 5.3 °C in all replicates (Cerezo and García, 2004; Sastre et al., 2016; Pirozzi and Booth, 2009; Dalvi et al., 2009; Uliano et al., 2010; Pang et al., 2011; Reyes et al., 2012).

There are several previous reports of routine metabolism in deep sea species at temperatures between 2.5 and 5 °C (Table 1). Our records show average oxygen consumption values ​​comparable to other Gadiforms, with Gadus morhua having a slightly higher OC (Claireaux et al., 2000) and Gadus ogac (Bushnell et al., 1994) and Gadus chalcogrammus (Seibel and Drazen, 2007) slightly lower rates for similar weights and at 5 °C. Methodological difficulties arise when trying to measure routine oxygen consumption in situ of these deep-sea fish, between 1.000 to 2.500 m depth and water pressures ranging from 100 to 250 atm. Our data were obtained at 5 °C, and at a surface pressure of 1 atm (OC= 42.9-35.4 mgO2 kg-1 h-1), with values greater than the ones obtained on other deep-sea fish but in situ at far greater pressures such as for Coryphaenoides armatus (6.72 mgO2 kg- 1 h-1) at the same temperature (Bailey et al., 2002) and Coryphaenoides acrolepis (1.92 mgO2 kg-1 h-1) (Drazen et al., 2005). Drazen and coworkers (Drazen et al., 2005) measured in situ at a depth of 4,000 m, obtaining much lower values evenusing smaller fish (1-1.5 kg). Bushnell et al. (1994), Bailey et al. (2002) and Drazen et al. (2005) highlight the need of conducting experiments considering the habitat and high pressures of these deep-sea fish, and while we agree, the lack of a deep sea in situ respirometer precluded us to do so. We can’t rule out that our somewhat elevated OC values are due to pressure effects, as we did not measure fish metabolism in situ at the depths of fish capture. However, since our fish were acclimated for several months at surface pressures, we can at least be sure that our OC measurements are representative of deep fish acclimated to surface pressures. We think these data are still valuable as in fact, this is the very first report of the aerobic metabolism and its preliminary scaling with the mass of D. eleginoides.

Table 1
Comparison of Oxygen Consumption (mgO2kg-1h-1) of D. eleginoides with other cold water fish species at routine metabolism and low temperatures.

According to the OC obtained here (Figure 2a), D. eleginoides seems to be an active species, comparable to other active species such as Salmo trutta (OC = 0.2 W0.877, Beamish, 1964) and Oncorhynchus rhodurus (OC = 0.30W0.9, Miura and Suzuki, 1976). Similarly, the mass scaling exponent for D. eleginoides was estimated to be 0.85 (Figure 2b), which is comparable with other active species and temperate environments with high growth rates such as O. mykkis (Dickson and Kramer, 1971; Constable et al., 2001). Based on the initially fast growth and a size of around 30 to 40 cm length at first recruitment reported (Constable et al., 2001), we hypothesize metabolism is primed to maximize outcomes at its polar distribution at this first stage. Despite its long-life span reported, D. eleginoides shows a metabolism comparable to other fast growth temperate species at this experimental surface pressure, and thus its scaling exponent should fall well above the two most widely accepted theoretical 0.66 and 0.75 scaling exponents. Another possibility, which might add to the former explanation, is that fish were simply not resting after the little 2 h acclimation to the respirometry chambers. This metabolism above resting rates might also contribute to the 0.85 scaling slope, quite unexpected for deep sea fish species such as in the early work from Smith Junior (1978) on rattails (Coryphaenoides armatus). Interestingly, on the very same study, Smith reported that MR remained elevated only during the first 20 to 95 minutes after capture and handling (and so the fish measured here might have reached acclimation to the respirometer), which might support our first explanation of an elevated scaling slope due to the use of young fish and a metabolism primed for polar waters.

Our major concern is not stress indeed, but the fact they are wild fish that have been kept 2.5 years in captivity at shallow water pressures and not in deep-sea. Furthermore, in the size one, fish were also grouped in the same respirometry chamber, which might have exacerbated fish interaction and thus metabolism. Longer acclimation should be considered for future experiments, even when in Notothenia neglecta metabolic rates of fasting and fed individuals, and the characteristics of the SDA were found to be independent of acclimation conditions (Johnston and Battram, 1993). According to Seibel and Drazen (2007) published studies of oxygen consumption have to satisfied a few basic criteria, although, given the general paucity of deep-sea data, we were not able to be highly selective with few fish we had available. In all experiments, spontaneous activity and the effects of feeding during measurement were minimized or specifically controlled. All measurements were made over at least 4 h and most experiments lasted 12–48 h with at least a 48-h period of food deprivation prior to measurement. Thus, we acknowledge that metabolism could have been not at resting, and so present data should be regarded as routine metabolism, but still valuable as it represents the very first values of metabolism and mass scaling on this polar and deep-sea fish species.

Our results show high rates of oxygen consumption, particularly on the smallest D. eleginoides (2 to 8 kg) under shallow water pressures, comparable to those of G. morhua and to highly active species such as salmonids, leading us to preliminarily reject the initial hypothesis of slow metabolism on this deep-sea species acclimated to shallow water pressures. In general, it is recommended for commercial fish farming to maintain oxygen concentration above 5 mg L-1, as there are evidence confirming that fish growth, food conversion rate efficiency and swimming are affected (Encina-Montoya et al., 2011) at low oxygen levels. To optimize fish farming densities, oxygen consumption must be complemented with other variables such as ammonia excretion, tolerance to CO2. Our results showed culture densities between 57.77 kg m-3 and 87.38 kg m-3 are feasible, considering oxygen consumption as the only limitation. So, these estimates present important advantages and new perspectives for D. eleginoides husbandry.

The results of this work are relevant and positive for the future farming of this species. In situ experiments must be done, at the depths of fish capture. It is also necessary to include a broader size range for future studies, and so to better capture the potentially slower metabolism of older fish. On the other hand, it is necessary to carry out studies under conditions of deep-water pressure to understand the metabolic adaptation strategies of this iconic southern hemisphere deep-sea fish.

This is the first report on routine metabolism and its scaling, with captive fish at the surface and performing normal and spontaneous activity with D. eleginoides and allows us to conclude that culture densities estimated based on metabolic rates offer significant advantages and new insights for the culture of D. eleginoides.

Acknowledgements

We thank the vice rectory for research and postgraduate studies at the Catholic University of Temuco and project MECESUP UCT 0804. This work was part of the project “Alternative preventive and therapeutic measures in Greek mariculture” which was funded by the call: Operational-Strategic Reference Framework, NSFR, Cooperation, Action I. General Secretariat for Research and Technology, Ministry of Education and Religious Affairs, Greece, and ANID FONDECYT 1210071. This work was part of the project “Alternative preventive and therapeutic measures in Greek mariculture” which was funded by the call: Operational-Strategic Reference Framework, NSFR, Cooperation, Action I. General Secretariat for Research and Technology, Ministry of Education and Religious Affairs, Greece, ANID FONDECYT 1210071.

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Publication Dates

  • Publication in this collection
    31 Jan 2025
  • Date of issue
    2024

History

  • Received
    17 Apr 2024
  • Accepted
    31 Aug 2024
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