Energy demand of larval and juvenile Cape horse mackerels, Trachurus capensis, and indications of hypoxia tolerance as benefit in a changing environment

Physiological traits of five key fish species (Cape hake Merluccius spp., pelagic goby Sufflogobius bibarbatus, Cape horse mackerel Trachurus capensis, European anchovy Engraulis encrasicolus and sardine Sardinops sagax) from the northern Benguela upwelling system (NBUS) were compared during their larval stage by measurements of enzymatic activities of key metabolic enzymes (citrate synthase [CS] and pyruvate kinase [PK]). Two distinct age classes (early larvae: 8‒14 days old; late larvae: 22‒29 days old) for each species and from two areas were compared: Terrace Bay (20° S), the main spawning ground of Cape horse mackerel and anchovy, and Kunene (17° S), near the Angola–Benguela frontal zone, where warm and hypoxic water masses intrude into the NBUS. The results revealed significantly higher CS activity in both larval age classes in Cape horse mackerel, anchovy and sardine compared with Cape hake and pelagic goby. Pelagic goby and Cape horse mackerel had significantly higher PK activity compared with Cape hake, anchovy and sardine, apparent in both larval age classes and both areas. Results for anaerobic metabolism indicate higher capacity for pelagic goby and Cape horse mackerel to recover from oxygen debt built up in prey capture and predator escape behaviour and a higher potential for hypoxia tolerance when compared with Cape hake, anchovy and sardine. These results suggest higher survival probability for pelagic goby and Cape horse mackerel compared with the other species under conditions of a shoaling oxygen minimum zone and may explain their current dominance in the NBUS.

Early life history (ELH) traits are key to understand variable recruitment success and hence the stock size of marine fish. One of the currently most puzzling ecosystems in this regard is the northern part of the Benguela Current upwelling system off Namibia. Here, populations of the formerly dominant pelagic species, sardine and anchovy, failed to recover during the last three decades after a dramatic decline. In contrast, Cape horse mackerel, Trachurus capensis, maintained a constant population size. Warming of the system and shoaling of hypoxic zones together with feedback loops within an altered foodweb are discussed to be responsible for this regime shift. In this study, we address the role of larval traits for the successful performance of the T. capensis population under the present environmental conditions with the focus on feeding ecology. We investigated seasonal variations of the geographical distribution, growth rate, feeding ecology, and nutritional condition of their ELH stages and examined relationships with water temperature, dissolved oxygen concentration, and micro-zooplankton composition. T. capensis' ELH stages showed a wide spatial and seasonal distribution, a preference for higher water temperatures (18–21°C) and presence over a wide range of dissolved oxygen concentrations (0.13–6.35 ml O2 l−1). Feeding success was high and mainly different groups of Copepoda were targeted, which were strongly size selected. The high dietary importance of micro-copepods during large parts of the larval phase indicates successful exploitation of this food source, which has increased in abundance during the last decade. It also explains observed best nutritional conditions at temperatures between 18 and 21°C, since these small copepods are commonly associated with warmer temperatures. Altogether, these traits enhance the species' probability to encounter suitable environments for the survival of their ELH stages, which is likely to lead to their high recruitment success in the northern Benguela ecosystem.

1. Individuals of the same species often exhibit consistent differences in metabolic rate, but the effects of such differences on ecologically important behaviours remain largely unknown. In particular, it is unclear whether there is a cause-and-effect relationship between metabolic rate and the tendency to take risks while foraging. Individuals with higher metabolic rates may need to take greater risks while foraging to obtain the additional food required to satisfy their energy requirements. Such a relationship could be exacerbated by food deprivation if a higher metabolic demand also causes greater mass loss and hunger. 2. We investigated relationships among metabolic rate, risk-taking and tolerance of food deprivation in juvenile European sea bass. Individual fish were tested for risk-taking behaviours following a simulated predator attack, both before and after a 7-day period of food deprivation. The results were then related to their routine metabolic rate (RMR), which was measured throughout the period of food deprivation. 3. The amount of risk displayed by individual fish before food deprivation showed no relationship with RMR. After food deprivation, however, the amount of risk among individuals was positively correlated with RMR. In general, most fish showed an increase in risk-taking after food deprivation, and the magnitude of the increase in risk-taking was correlated with the rate of individual mass loss during food deprivation, which was itself strongly correlated with RMR. 4. The observation that RMR was related to risk-taking behaviour after food deprivation, but not before, suggests that although RMR can influence risk-taking, the strength of the relationship is flexible and context dependent. The effects of RMR on risk-taking may be subtle or non-existent in regularly feeding animals, but may lead to variability in risk-taking among individuals when food is scarce or supply is unpredictable. This synergistic relationship between RMR and food deprivation could lead to an increased likelihood of being predated for individuals with a relatively high intrinsic energy demand during times when food is scarce.

Dover sole (Solea solea, Linneaus 1758) were raised from first feeding on brine shrimp (Artemia sp.) with different contents and compositions of the essential fatty acids (EFA) arachidonic acid (ARA, 20:4n − 6); eicosapentaenoic acid (EPA, 20:5n − 3), and docosahexaenoic acid (DHA, 22:6n − 3), and their metabolic rate and tolerance to hypoxia measured prior to and following metamorphosis and settlement. Four dietary Artemia preparations were compared: (1) un-enriched; (2) enriched with a commercial EFA mixture (Easy DHA SELCO Emulsion); (3) enriched with a marine fish oil combination (VEVODAR and Incromega DHA) to provide a high ratio of ARA to DHA, and (4) enriched with these fish oils to provide a low ratio of ARA to DHA. Sole fed un-enriched Artemia were significantly less tolerant to hypoxia than the other dietary groups. Larvae from this group had significantly higher routine metabolic rate (RMR) in normoxia, and significantly higher O2 partial pressure (PO2) thresholds in progressive hypoxia for their regulation of RMR (Pcrit) and for the onset of agitation, respiratory distress and loss of equilibrium. Metamorphosis was associated with an overall decline in RMR and increase in Pcrit, but juveniles fed on un-enriched Artemia still exhibited higher Pcrit and agitation thresholds than the other groups. Sole fed un-enriched Artemia had significantly lower contents of EFA in their tissues, both before and after settlement. Thus, enriching live feeds with EFA has significant effects on the respiratory physiology of sole early life stages and improves their in vivo tolerance to hypoxia. We found no evidence, however, for any effect of the ratio of ARA to DHA.

We measured the metabolic rates as a direct estimate of energy expenditure of individual Neolamprologus pulcher, a cooperatively breeding cichlid fish, when resting and when performing agonistic, submissive or digging behaviours in a respirometer. Standard and routine metabolic rates increased linearly with body mass (range 0.9–8.4 g) when plotted on a doubly logarithmic scale (linear regression equations: standard metabolic rate: log individual oxygen consumption rate = 0.65 + 0.86 log body mass; routine metabolic rate: log individual oxygen consumption rate = 0.75 + 0.86 log body mass). Routine metabolic rates were, on average, 30% higher than standard metabolic rates. Submissive and agonistic behaviours raised routine metabolic rates by factors of 3.3 and 3.9, respectively. Digging resulted in a 6.1-fold increase of routine metabolic rates. Differences in metabolic rates between active and resting rates were statistically significant. However, those between the three behaviours were not. Mean opercular beat frequencies correlated significantly with routine metabolic rates and with metabolic rates when performing specific behaviours, which offers methodological prospects for field measurements. In N. pulcher, the high energy expenditure for submissive behaviour may indicate that this is a reliable signal. The considerable energy expenditure involved in territory defence suggests that these costs should be considered in addition to risk in cost-benefit analyses. This is the first study in which the energy expenditures of specific social and territory maintenance behaviours of individual fish were measured directly by respirometry and within the usual social setting of the fish.

The effects of salinity and photoperiod on aerobic scope, hypoxia tolerance and swimming performance of coho salmon (Oncorhynchus kisutch) reared in recirculating aquaculture systems

The metabolic rate of aquatic animals is closely related to oxygen concentration and influenced by internal and external factors. Despite its high value as marine fish species in South Korea, information on rock bream Oplegnathus fasciatus metabolism is scarcely available. This study observed the standard metabolic rate (SMR), routine metabolic rate (RMR), and active metabolic rate (AMR) of rock bream Oplegnathus fasciatus subjected to different temperature settings. Another observation was performed to find out the maximum metabolic rate (MMR) on rock bream subjected to different salinity settings. Fish (TL: 26.86 ± 0.29 cm and BW: 469.40 ± 38.21 g for SMR, RMR, and AMR measurement; TL: 26.7 ± 0.4 cm and BW: 451.0 ± 44.4 g for MMR measurement) were observed using respirometer (dimension = 30 cm × 20 cm × 20 cm; volume: 10.4 L) inside a recirculation systems. SMR, RMR, and AMR were measured at 15°C, 20°C, and 25°C. Meanwhile, MMR was measured at 15, 25, and 35 psu. The results showed that SMR, RMR, and AMR increased linearly by increasing the temperatures (SMR: 58.7 ± 3.2, 102.7 ± 4.3, and 157.1 ± 4.1 mg O2/kg/h at 15°C, 20°C, and 25°C, respectively; RMR: 66.0 ± 8.6, 112.6 ± 10.2, and 175.2 ± 21.3 mg O2/kg/h at 15°C, 20°C, and 25°C, respectively; AMR: 73.4 ± 7.4, 122.0 ± 6.3, and 196.7 ± 15.4 mg O2/kg/h at 15°C, 20°C, and 25°C, respectively), whilst MMR decreased by lowering salinity (48.5 ± 5.2, 61.1 ± 5.5, and 89.3 ± 14.7 mg O2/kg/hour at salinity of 15, 25, and 35 psu, respectively).

The effect of normoxia exposure on hypoxia tolerance and sensory sampling in a swamp-dwelling mormyrid fish

Influence of temperature, oxygen and salinity on the metabolism of the European sea bass

Feed efficiency (FE) is the amount of body weight gain for a given feed intake. Improving FE through selective breeding is key for sustainable finfish aquaculture but its evaluation at individual level is technically challenging. We therefore investigated whether individual routine metabolic rate (RMR) was a predictor of individual FE in the European sea bass Dicentrarchus labrax, a major species in European mariculture. The European sea bass has three genetically distinct populations across its geographical range, namely Atlantic (AT), West Mediterranean (WM), and East Mediterranean (EM). We compared FE and RMR of fish from these three populations at 18 or 24 °C. We held 200 fish (62 AT, 66 WM, and 72 EM) in individual aquaria and fed them from ad libitum down to fasting. FI was assessed for an ad libitum feeding rate and for a fixed restricted ration (1% of metabolic body weight·day-1, with metabolic body weight = body weight0.8). After being refed 12 wk in a common tank, individual RMR was measured over 36 h by intermittent flow respirometry. There was a significant effect of temperature whereby fish at 18 °C had greater mean FE (P < 0.05) and lower RMR (P < 0.001). There was also a significant effect of population, where AT fish had lower FE (P < 0.05) and greater RMR (P < 0.001) than WM and EM, at both temperatures. Despite these differences in temperature and population means, individual FE and RMR were not significantly correlated (P > 0.05). Therefore, although the results provide evidence of an association between metabolic rate and FE, RMR was not a predictor of individual FE, for reasons that require further investigation.

Hypoxia tolerance in aquatic ectotherms involves a suite of behavioral and physiological responses at the organismal, tissue, and cellular levels. The current study evaluated two closely related killifish species (Fundulus heteroclitus, Fundulus majalis) to evaluate responses to acute moderate and acute severe hypoxia. Routine metabolic rate and loss of equilibrium were assessed, followed by analysis in skeletal muscle of markers of oxidative damage to proteins (2,4-DNPH), lipids (4-HNE), and DNA (8-OHdG), hypoxia signaling (HIF1α, HIF2α), cellular energy state (p-AMPK: AMPK), and protein degradation (Ubiquitin, LC3B, Calpain 2, Hsp70). Both species had a similar reduction in metabolic rate at low PO2. However, F. heteroclitus was the more hypoxia-tolerant species based on a lower PO2 at which there was loss of equilibrium, perhaps due in part to a lower oxygen demand at all oxygen tensions. Despite the differences in hypoxia tolerance between the species, skeletal muscle molecular markers were largely insensitive to hypoxia, and there were few differences in responses between the species. Thus, the metabolic depression observed at the whole animal level appears to limit perturbations in skeletal muscle in both species during the hypoxia treatments.

Temperature variation affects the growth performance of fish species due to growing constraints and trade-off on physiological functions. Here we experimentally investigated several metabolic and physiological parameters in Sinilabeo rendahli, an endemic fish species found in the Yangtze River in China. After a 14-day acclimation period, we measured routine metabolic rate (RMR), individual metabolic rate (MO2), temperature quotient (Q10), loss of equilibrium (LOE), and critical oxygen tension (Pcrit) at three different temperatures (15, 20, and 25°C). Moreover, we sampled the muscle tissue from juvenile S. rendahli under experimental conditions after 28 days of acclimation and performed transcriptome-RNA sequencing (RNA-seq). The Pcrit of the fish at the above acclimation temperatures were determined to be 1.07, 1.28, and 1.33 mg·L−1, respectively, and corresponded with increasing acclimation temperatures (15–25°C). RMR was positively correlated with Pcrit (r = 0.4711, P = 0.0201), negatively correlated with LOE (r = −0.4284, P = 0.0367), and significantly positively correlated with MRcrit (r = 0.8797, P &amp;lt; 0.001) at temperatures ranging from 15 to 25°C. In addition, a total of 4,710 differentially expressed genes (DEGs) were identified. The results of DEG analysis and KEGG clustering analysis indicated that energy metabolism played a central role in thermal stress in S. rendahli for the major upregulated genes. This was followed by autophagy, mitophagy, cardiac muscle contraction, extracellular matrix (ECM)-receptor interaction, and protein digestion and absorption. This study is significant for understanding the adaptive response of S. rendahli to thermal stress. Even more importantly, this study demonstrates that S. rendahli is more suitable for cold-water life.

AimMetabolic rate is a widely studied physiological species trait related to energetics, climate, and geographical distributions. Hypotheses have been proposed to explain variation in metabolic rate, but evidence has been mixed due to the limited sampling scope of intraspecific studies. Successful biological invasions offer a unique opportunity to examine the development of intraspecific physiological variation and how it relates to climate, invasive spread and species range limits. The aim of this study was to determine if metabolic rate variation across the spongy moth invasive range was consistent with a pattern of adaptation to local climate.LocationNortheastern United States of America.TaxonLymantria dispar dispar L. (Lepidoptera: Erebidae).MethodsLarvae were sourced from 14 populations across the invasion front and interior of the current L. d. dispar invasive range and were reared at a constant temperature. Routine metabolic rates (RMR) of larvae were assayed at three ecologically relevant temperatures. These data were analysed to determine if there were differences in RMR and temperature sensitivity of RMR among populations. Population‐level variation in RMR was then analysed as a function of local climate and geographical position to test for patterns consistent with local adaptation.ResultsLarval RMR showed significant variation among populations across all assay temperatures, but there was no difference in temperature sensitivity (i.e. slope). This variation followed a positive latitudinal cline with RMR increasing from the southern range to the north. This cline also showed a significant relationship with local climate variables.Main ConclusionsLarval metabolic rate variation was consistent with a pattern of adaptation by L. d. dispar to divergent climates across its invasive range. These results indicated that thermal adaptation of whole‐organism physiology may play a key role in promoting species spread and expansion for biological invasions like L. d. dispar.

Atlantic bluefin tuna is an iconic scombrid species with a high commercial and ecological value. Despite their importance, many physiological aspects, especially during the larval stages, are still unknown. Metabolic rates are one of the understudied aspects in scombrid larvae, likely due to challenges associated to larval handling before and during respirometry trials. Gaining reliable estimates of metabolic rates is essential to understand how larvae balance their high growth needs and activity and other physiological functions, which can be very useful for fisheries ecology and aquaculture. This is the first study to (a) estimate the relationship between routine metabolic rate (RMR) and larval dry weight (DW) (mass scaling exponent) at a constant temperature of 26°C, (b) measure the RMR under light and darkness and (c) test whether the interindividual differences in the RMR are related to larval nutritional status (RNA/DNA and DNA/DW). The RMR scaled nearly isometrically with body size (b = 0.99, 0.60-31.56 mg DW) in contrast to the allometric relationship observed in most fish larvae (average b = 0.87). The results show no significant differences in larval RMR under light and darkness, suggesting similar larval activity levels in both conditions. The size explained most of the variability in RMR (97%), and nutritional condition was unrelated to the interindividual differences in routine metabolism. This is the first study to report the metabolic rates of Atlantic bluefin tuna larvae and discuss the challenges of performing bioenergetic studies with early life stages of scombrids.

Insights into feeding interactions of shallow water cape hake (Merluccius capensis) and cape horse mackerel (Trachurus capensis) from the Northern Benguela (Namibia)