Neill A. Herbert

Anaemia adjusts the aerobic physiology of snapper (Pagrus auratus) and modulates hypoxia avoidance behaviour during oxygen choice presentations

SUMMARY The effect of altered oxygen transport potential on behavioural responses to environmental hypoxia was tested experimentally in snapper, Pagrus auratus, treated with a haemolytic agent (phenylhydrazine) or a sham protocol. Standard metabolic rate was not different between anaemic and normocythaemic snapper (Hct=6.7 and 25.7 g dl-1, respectively), whereas maximum metabolic rate, and hence aerobic scope (AS), was consistently reduced in anaemic groups at all levels of water PO2 investigated (P<0.01). This reduction of AS conferred a higher critical oxygen limit (Pcrit) to anaemic fish (8.6±0.6 kPa) compared with normocythaemic fish (5.3±0.4 kPa), thus demonstrating reduced hypoxic tolerance in anaemic groups. In behavioural choice experiments, the critical avoidance PO2 in anaemic fish was 6.6±2.5 kPa compared with 2.9±0.5 kPa for controls (P<0.01). Behavioural avoidance was not associated with modulation of swimming speed. Despite differences in physiological and behavioural parameters, both groups avoided low PO2 just below their Pcrit, indicating that avoidance was triggered consistently when AS limits were reached and anaerobic metabolism was unavoidable. This was confirmed by high levels of plasma lactate in both treatments at the point of avoidance. This is the first experimental demonstration of avoidance behaviour being modulated by internal physiological state. From an ecological perspective, fish with disturbed oxygen delivery potential arising from anaemia, pollution or stress are likely to avoid environmental hypoxia at a higher PO2 than normal fish.

Low O2 acclimation shifts the hypoxia avoidance behaviour of snapper (Pagrus auratus) with only subtle changes in aerobic and anaerobic function

SUMMARY It was hypothesised that chronic hypoxia acclimation (preconditioning) would alter the behavioural low-O2 avoidance strategy of fish as a result of both aerobic and anaerobic physiological adaptations. Avoidance and physiological responses of juvenile snapper (Pagrus auratus) were therefore investigated following a 6 week period of moderate hypoxia exposure (10.2–12.1 kPa PO2, 21±1°C) and compared with those of normoxic controls (PO2=20–21 kPa, 21±1°C). The critical oxygen pressure (Pcrit) limit of both groups was unchanged at ~7 kPa, as were standard, routine and maximum metabolic rates. However, hypoxia-acclimated fish showed increased tolerances to hypoxia in behavioural choice chambers by avoiding lower PO2 levels (3.3±0.7 vs 5.3±1.1 kPa) without displaying greater perturbations of lactate or glucose. This behavioural change was associated with unexpected physiological adjustments. For example, a decrease in blood O2 carrying capacity was observed after hypoxia acclimation. Also unexpected was an increase in whole-blood P50 following acclimation to low O2, perhaps facilitating Hb–O2 off-loading to tissues. In addition, cardiac mitochondria measured in situ using permeabilised fibres showed improved O2 uptake efficiencies. The proportion of the anaerobic enzyme lactate dehydrogenase, at least relative to the aerobic marker enzyme citrate synthase, also increased in heart and skeletal red muscle, indicating enhanced anaerobic potential, or in situ lactate metabolism, in these tissues. Overall, these data suggest that a prioritization of O2 delivery and O2 utilisation over O2 uptake during long-term hypoxia may convey a significant survival benefit to snapper in terms of behavioural low-O2 tolerance.

Correlates of choroid rete development with the metabolic potential of various tropical reef fish and the effect of strenuous exercise on visual performance

Abstract It is hypothesised that the transport of oxygen to the retinal cells of fish with Root effect haemoglobins (Hb) is impaired by strenuous exercise due to a proton load that drastically reduces arterial haemoglobin–oxygen affinity. Routinely active reef fishes have enhanced oxygen transport and anaerobic (i.e. blood lactate loading) potentials relative to inactive species. Surprisingly, the development of the choroid rete mirabile (employed as an oxygen concentrating apparatus in the eye) is directly correlated with post-exercise lactate loads rather than with the magnitude of the Root effect and suggests that an increased development is adaptive for fish with high anaerobic potentials. The hypothesis that visual performance is reduced by strenuous exercise was tested in Lutjanus carponotatus using the optomotor response. Moderate blood lactate loads (2 mmol l−1 blood lactate) and red cell swelling responses were induced by exercise, but the optomotor response threshold (180 min of arc) was maintained. A moderate metabolic disturbance does not therefore appear to be a liability for the visual performance of a tropical fish in possession of Root effect haemoglobins.

Disrupted flow sensing impairs hydrodynamic performance and increases the metabolic cost of swimming in the yellowtail kingfish, Seriola lalandi

SUMMARY The yellowtail kingfish, Seriola lalandi, shows a distribution of anaerobic and aerobic (red and pink) muscle fibres along the trunk that is characteristic of active pelagic fishes. The athletic capacity of S. lalandi is also shown by its relative high standard metabolic rate and optimal (i.e. least cost) swimming speed. To test the hypothesis that lateral line afferent information contributes to efficient locomotion in an active pelagic species, the swimming performance of S. lalandi was evaluated after unilateral disruption of trunk superficial neuromasts (SNs). Unilaterally disrupting the SNs of the lateral line impaired both swimming performance and energetic efficiency. The critical swimming speed (Ucrit; mean ± s.d., N=12) for unilaterally SN-disrupted fish was 2.11±0.96 fork lengths (FL) s−1, which was significantly slower than the 3.66±0.19 FL s−1 Ucrit of sham SN-disrupted fish. The oxygen consumption rate (mg O2 kg−1 min−1) of the unilaterally SN-disrupted fish in a speed range of 1.0–2.2 FL s−1 was significantly greater than that of the sham SN-disrupted fish. The least gross cost of transport (GCOT; N=6) for SN-disrupted fish was 0.18±0.06 J N−1 m−1, which was significantly greater than the 0.11±0.03 J N−1 m−1 GCOT for sham SN-disrupted fish. The factorial metabolic scope (N=6) of the unilaterally SN-disrupted fish (2.87±0.78) was significantly less than that of sham controls (4.14±0.37). These data show that an intact lateral line is important to the swimming performance and efficiency of carangiform swimmers, but the functional mechanism of this effect remains to be determined.

Temperature acclimation of mitochondria function from the hearts of a temperate wrasse (Notolabrus celidotus)

Understanding how mitochondrial function alters with acclimation may provide insight to the limits these organelles place on temperate fish hearts facing seasonal temperature fluctuations. This investigation determined if compromised cardiac mitochondrial function contributed to heart failure (HF) in the New Zealand wrasse Notolabrus celidotus acclimated at their mean summer and winter ocean temperatures. To test this hypothesis, fish were acclimated to cold (CA, 15°C) and warm (WA, 21°C) temperatures. The temperature of HF was determined by Doppler sonography and mitochondrial function in permeabilised cardiac fibres was tested using high resolution respirometry. Heat stress mediated HF occurred at a THF of 26.7±0.4°C for CA fish, and at 28.2±0.6°C for WA fish. Biochemical analyses also revealed that WA fish had elevated resting plasma lactate indicating an increased dependence on anaerobic pathways. When cardiac fibres were tested with increasing temperatures, apparent breakpoints in the respiratory control ratio (RCR-I) with substrates supporting complex I (CI) oxygen flux occurred below the THF for both acclimated groups. While WA cardiac mitochondria were less sensitive to increasing temperature for respirational flux supported by CI, Complex II, and chemically uncoupled flux, CA fish maintained higher RCRs at higher temperatures. We conclude that while acclimation to summer temperatures does alter cardiac mitochondrial function in N. celidotus, these changes need not be beneficial in terms of oxidative phosphorylation efficiency and may come at an energetic cost, which would be detrimental in the face of further habitat warming.

Low O2 avoidance is associated with physiological perturbation but not exhaustion in the snapper (Pagrus auratus: Sparidae)

It is already known that the New Zealand snapper (Pagrus auratus, Sparidae) does not avoid hypoxia until reaching an oxygen partial pressure (PO(2)) of 3.1±1.2 kPa at 18 °C. Avoidance at this level of PO(2) and temperature is below the critical oxygen partial pressure of the species (P(crit)=5.8±0.6 kPa, 43.5±4.5 mmHg) and is therefore expected to result in major physiological stress. Results from the current study showed that avoidance was associated with numerous physiological perturbations, including a significant endocrine response, haematological changes, osmoregulatory disturbance and metabolic adjustments in the heart, liver and muscle. Snapper clearly experienced physiological stress at the point of avoidance but they were not however in a state of physiological exhaustion since some fuel reserves were still available. In addition to avoidance, snapper also showed a subtle reduction in swimming speed - this energy-saving response may have helped snapper minimise the physiological challenge of low O(2) residence. It is therefore concluded that snapper can reside in water below their P(crit) threshold for brief periods of time and, without any evidence of physiological exhaustion at the point of avoidance, fish should recover quickly once normoxia is selected. Lastly, with signs of anaerobic metabolism in cardiac tissue at the point of avoidance, we tentatively suggest that snapper may leave hypoxia to protect heart function.

Accommodating the cost of growth and swimming in fish-the applicability of exercise-induced growth to juvenile hapuku (Polyprion oxygeneios).

Induced-swimming can improve the growth and feed conversion efficiency of finfish aquaculture species, such as salmonids and Seriola sp., but some species, such as Atlantic cod, show no or a negative productivity response to exercise. As a possible explanation for these species-specific differences, a recent hypothesis proposed that the applicability of exercise training, as well as the exercise regime for optimal growth gain (ERopt growth), was dependent upon the size of available aerobic metabolic scope (AMS). This study aimed to test this hypothesis by measuring the growth and swimming metabolism of hapuku, Polyprion oxygeneios, to different exercise regimes and then reconciling the metabolic costs of swimming and specific dynamic action (SDA) against AMS. Two 8-week growth trials were conducted with ERs of 0.0, 0.25, 0.5, 0.75, 1, and 1.5 body lengths per second (BL s−1). Fish in the first trial showed a modest 4.8% increase in SGR over static controls in the region 0.5–0.75 BL s−1 whereas the fish in trial 2 showed no significant effect of ER on growth performance. Reconciling the SDA of hapuku with the metabolic costs of swimming showed that hapuku AMS is sufficient to support growth and swimming at all ERs. The current study therefore suggests that exercise-induced growth is independent of AMS and is driven by other factors.

Unilateral ablation of trunk superficial neuromasts increases directional instability during steady swimming in the yellowtail kingfish Seriola lalandi

Detailed swimming kinematics of the yellowtail kingfish Seriola lalandi were investigated after unilateral ablation of superficial neuromasts (SNs). Most kinematic variables, such as tail-beat frequency, stride length, caudal fin-beat amplitude and propulsive wavelength, were unaffected but lateral amplitude at the tip of the snout (A0 ) was significantly increased in SN-disrupted fish compared with sham-operated controls. In addition, the orientation of caudal fin-tip relative to the overall swimming direction of SN-disrupted fish was significantly deflected (two-fold) in comparison with sham-operated control fish. In some fish, SN disruption also led to a phase distortion of the propulsive body-wave. These changes would be expected to increase both hydrodynamic drag and thrust production which is consistent with the finding that SN-disrupted fish had to generate significantly greater thrust power when swimming at ≥1·3 fork lengths (LF ) s(-1) . In particular, hydrodynamic drag would increase as a result of any increase in rotational (yaw) perturbation and sideways slip resulting from the sensory disturbance. In conclusion, unilateral SN ablation produced directional instability of steady swimming and altered propulsive movements, suggesting a role for sensory feedback in correcting yaw and slip disturbances to maintain efficient locomotion.

No evidence of shelter providing a metabolic advantage to the false clown anemonefish Amphiprion ocellaris

There was no evidence that shelter conveyed a metabolic advantage to the false clown anemonefish Amphiprion ocellaris in terms of standard and routine rates of oxygen uptake. The metabolic and fitness benefit of shelter might not, therefore, be widespread among all fish species.

Gill structural change in response to turbidity has no effect on the oxygen uptake of a juvenile sparid fish

The effect of suspended sediments on the oxygen uptake of a sparid fish was examined. Pagrus auratus showed gill damage to suspended sediments over 30 days, as well as decreased somatic growth. However, gill damage as a result of turbidity exposure was not associated with a change in aerobic capacity.