David J. McKenzie

Environmental stressors alter relationships between physiology and behaviour.

Although correlations have frequently been observed between specific physiological and behavioural traits across a range of animal taxa, the nature of these associations has been shown to vary. Here we argue that a major source of this inconsistency is the influence of environmental stressors, which seem capable of revealing, masking, or modulating covariation in physiological and behavioural traits. These effects appear to be mediated by changes in the observed variation of traits and differential sensitivity to stressors among phenotypes. Considering that wild animals routinely face a range of biotic and abiotic stressors, increased knowledge of these effects is imperative for understanding the causal mechanisms of a range of ecological phenomena and evolutionary responses to stressors associated with environmental change.

Aerobic capacity influences the spatial position of individuals within fish schools

The schooling behaviour of fish is of great biological importance, playing a crucial role in the foraging and predator avoidance of numerous species. The extent to which physiological performance traits affect the spatial positioning of individual fish within schools is completely unknown. Schools of juvenile mullet Liza aurata were filmed at three swim speeds in a swim tunnel, with one focal fish from each school then also measured for standard metabolic rate (SMR), maximal metabolic rate (MMR), aerobic scope (AS) and maximum aerobic swim speed. At faster speeds, fish with lower MMR and AS swam near the rear of schools. These trailing fish required fewer tail beats to swim at the same speed as individuals at the front of schools, indicating that posterior positions provide hydrodynamic benefits that reduce swimming costs. Conversely, fish with high aerobic capacity can withstand increased drag at the leading edge of schools, where they could maximize food intake while possibly retaining sufficient AS for other physiological functions. SMR was never related to position, suggesting that high maintenance costs do not necessarily motivate individuals to occupy frontal positions. In the wild, shifting of individuals to optimal spatial positions during changing conditions could influence structure or movement of entire schools.

Fuel, fasting, fear: routine metabolic rate and food deprivation exert synergistic effects on risk-taking in individual juvenile European sea bass

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.

Individual variation and repeatability in aerobic and anaerobic swimming performance of European sea bass, Dicentrarchus labrax.

SUMMARY Studies of inter-individual variation in fish swimming performance may provide insight into how selection has influenced diversity in phenotypic traits. We investigated individual variation and short-term repeatability of individual swimming performance by wild European sea bass in a constant acceleration test (CAT). Fish were challenged with four consecutive CATs with 5 min rest between trials. We measured maximum anaerobic speed at exhaustion (UCAT), gait transition speed from steady aerobic to unsteady anaerobic swimming (Ugt), routine metabolic rate (RMR), post-CAT maximum metabolic rate (MMR), aerobic scope and recovery time from the CATs. Fish achieved significantly higher speeds during the first CAT (UCAT=170 cm s–1), and had much more inter-individual variation in performance (coefficient of variation, CV=18.43%) than in the subsequent three tests (UCAT=134 cm s–1; CV=7.3%), which were very repeatable among individuals. The individual variation in UCAT in the first trial could be accounted for almost exclusively by variation in anaerobic burst-and-coast performance beyond Ugt. The Ugt itself varied substantially between individuals (CV=11.4%), but was significantly repeatable across all four trials. Individual RMR and MMR varied considerably, but the rank order of post-CAT MMR was highly repeatable. Recovery rate from the four CATs was highly variable and correlated positively with the first UCAT (longer recovery for higher speeds) but negatively with RMR and aerobic scope (shorter recovery for higher RMR and aerobic scope). This large variation in individual performance coupled with the strong correlations between some of the studied variables may reflect divergent selection favouring alternative strategies for foraging and avoiding predation.

Physiological mechanisms underlying a trade-off between growth rate and tolerance of feed deprivation in the European sea bass (Dicentrarchus labrax)

SUMMARY The specific growth rate (SGR) of a cohort of 2000 tagged juvenile European sea bass was measured in a common tank, during two sequential cycles comprising three-weeks feed deprivation followed by three-weeks ad libitum re-feeding. After correction for initial size at age as fork length, there was a direct correlation between negative SGR (rate of mass loss) during feed deprivation and positive SGR (rate of compensatory growth) during re-feeding (Spearman rank correlation R=0.388, P=0.000002). Following a period of rearing under standard culture conditions, individuals representing ‘high growth’ phenotypes (GP) and ‘high tolerance of feed deprivation’ phenotypes (DP) were selected from either end of the SGR spectrum. Static and swimming respirometry could not demonstrate lower routine or standard metabolic rate in DP to account for greater tolerance of feed deprivation. Increased rates of compensatory growth in GP were not linked to greater maximum metabolic rate, aerobic metabolic scope or maximum cardiac performance than DP. When fed a standard ration, however, GP completed the specific dynamic action (SDA) response significantly faster than DP. Therefore, higher growth rate in GP was linked to greater capacity to process food. There was no difference in SDA coefficient, an indicator of energetic efficiency. The results indicate that individual variation in growth rate in sea bass reflects, in part, a trade-off against tolerance of food deprivation. The two phenotypes represented the opposing ends of a spectrum. The GP aims to exploit available resources and grow as rapidly as possible but at a cost of physiological and/or behavioural attributes, which lead to increased energy dissipation when food is not available. An opposing strategy, exemplified by DP, is less ‘boom and bust’, with a lower physiological capacity to exploit resources but which is less costly to sustain during periods of food deprivation.

Reflex cardioventilatory responses to hypoxia in the flathead gray mullet (Mugil cephalus) and their behavioral modulation by perceived threat of predation and water turbidity.

In hypoxia, gray mullet surface to ventilate well‐oxygenated water in contact with air, an adaptive response known as aquatic surface respiration (ASR). Reflex control of ASR and its behavioral modulation by perceived threat of aerial predation and turbid water were studied on mullet in a partly sheltered aquarium with free surface access. Injections of sodium cyanide (NaCN) into either the bloodstream (internal) or ventilatory water stream (external) revealed that ASR, hypoxic bradycardia, and branchial hyperventilation were stimulated by chemoreceptors sensitive to both systemic and water O2 levels. Sight of a model avian predator elicited bradycardia and hypoventilation, a fear response that inhibited reflex hyperventilation following external NaCN. The time lag to initiation of ASR following NaCN increased, but response intensity (number of events, time at the surface) was unchanged. Mullet, however, modified their behavior to surface under shelter or near the aquarium edges. Turbid water abolished the fear response and effects of the predator on gill ventilation and timing of ASR following external NaCN, presumably because of reduced visibility. However, in turbidity, mullet consistently performed ASR under shelter or near the aquarium edges. These adaptive modulations of ASR behavior would allow mullet to retain advantages of the chemoreflex when threatened by avian predators or when unable to perceive potential threats in turbidity.

Root Effect Hemoglobin May Have Evolved to Enhance General Tissue Oxygen Delivery

Holding Your Breath Hemoglobin and myoglobin are widely responsible for oxygen transport and storage (see the Perspective by Rezende). The ability of diving mammals to obtain enough oxygen to support extended dives and foraging is largely dependent on muscle myoglobin (Mb) content. Mirceta et al. (p. 1303) found that in mammalian lineages with an aquatic or semiaquatic lifestyle, Mb net charge increases, which may represent an adaptation to inhibit self-association of Mb at high intracellular concentrations. Epistasis results from nonadditive genetic interactions and can affect phenotypic evolution. Natarajan et al. (p. 1324) found that epistatic interactions were able to explain the increased hemoglobin oxygen-binding affinity observed in deer mice populations at high altitude. In mammals, the offloading of oxygen from hemoglobin is facilitated by a reduction in the bloods pH, driven by metabolically produced CO2. However, in fish, a reduction in blood pH reduces oxygen carrying capacity of hemoglobin. Rummer et al. (p. 1327) implanted fiber optic oxygen sensors within the muscles of rainbow trout and found that elevated CO2 levels in the water led to acidosis and elevated oxygen tensions. The evolutionary origin of the unloading of oxygen at low pH is traced back to teleosts. [Also see Perspective by Rezende] The Root effect is a pH-dependent reduction in hemoglobin-O2 carrying capacity. Specific to ray-finned fishes, the Root effect has been ascribed specialized roles in retinal oxygenation and swimbladder inflation. We report that when rainbow trout are exposed to elevated water carbon dioxide (CO2), red muscle partial pressure of oxygen (PO2) increases by 65%—evidence that Root hemoglobins enhance general tissue O2 delivery during acidotic stress. Inhibiting carbonic anhydrase (CA) in the plasma abolished this effect. We argue that CA activity in muscle capillaries short-circuits red blood cell (RBC) pH regulation. This acidifies RBCs, unloads O2 from hemoglobin, and elevates tissue PO2, which could double O2 delivery with no change in perfusion. This previously undescribed mechanism to enhance O2 delivery during stress may represent the incipient function of Root hemoglobins in fishes.

Fish swimming in schools save energy regardless of their spatial position.

For animals, being a member of a group provides various advantages, such as reduced vulnerability to predators, increased foraging opportunities and reduced energetic costs of locomotion. In moving groups such as fish schools, there are benefits of group membership for trailing individuals, who can reduce the cost of movement by exploiting the flow patterns generated by the individuals swimming ahead of them. However, whether positions relative to the closest neighbours (e.g. ahead, sided by side or behind) modulate the individual energetic cost of swimming is still unknown. Here, we addressed these questions in grey mullet Liza aurata by measuring tail-beat frequency and amplitude of 15 focal fish, swimming in separate schools, while swimming in isolation and in various positions relative to their closest neighbours, at three speeds. Our results demonstrate that, in a fish school, individuals in any position have reduced costs of swimming, compared to when they swim at the same speed but alone. Although fish swimming behind their neighbours save the most energy, even fish swimming ahead of their nearest neighbour were able to gain a net energetic benefit over swimming in isolation, including those swimming at the front of a school. Interestingly, this energetic saving was greatest at the lowest swimming speed measured in our study. Because any member of a school gains an energetic benefit compared to swimming alone, we suggest that the benefits of membership in moving groups may be more strongly linked to reducing the costs of locomotion than previously appreciated.

Effects of dietary fatty acids on the respiratory and cardiovascular physiology of fish

In animals, the composition of fatty acids (FAs) in body pools reflects dietary intake. This paper reviews evidence that the manipulation of tissue lipids of farmed fish, by feeding them different natural oils, can have significant effects on their respiratory and cardiovascular physiology. Sturgeon and eels with tissue lipids rich in highly unsaturated FAs of the n-3 series (n-3HUFAs, accumulated from dietary menhaden oil) had significantly lower metabolic rates than fish with tissues rich in saturated FAs (SFAs, from coconut oil), although they grew equally well. In sturgeon, the difference in metabolism influenced tolerance of hypoxia. Degrees of hypoxia that depressed oxygen uptake and spontaneous activity in fish rich in SFAs had no such effects on fish rich in n-3HUFAs. In the isolated sturgeon heart working in vitro, reduced oxygen supply depressed the performance of hearts with lipids rich in SFAs but not that of hearts rich in n-3HUFAs. In salmon fed diets with graded mixtures of menhaden and canola oils, there was no relationship between tissue n-3HUFA content (from menhaden oil) and any measured aspect of swimming performance, but a linear relationship between maximum sustainable swimming speed and muscle oleic acid levels (from canola oil). Such exploratory studies indicate that an animals responses to its environment may be profoundly affected by the oils and FAs it consumes in its diet.

Sub-lethal plasma ammonia accumulation and the exercise performance of salmonids

The proposal that plasma ammonia accumulation might impair the swimming performance of fish was first made over a decade ago, and has now proven to be the case for a number of salmonid species. The first experimental evidence was indirect, when a negative linear relationship between plasma ammonia concentrations and maximum sustainable swimming speed (U(crit)) was found following the exposure of brown trout (Salmo trutta) to sub-lethal concentrations of copper in soft acidic water. Since then, negative linear relationships between plasma ammonia concentration and U(crit) have been demonstrated following exposure of brown trout, rainbow trout (Oncorhynchus mykiss) and coho salmon (Oncorhynchus kisutch) to elevated water ammonia. For brown trout, the relationships between plasma ammonia and U(crit) were remarkably similar following either exposure to elevated water ammonia or to sub-lethal copper. This indicates that the impairment of swimming performance resulting from exposure to sub-lethal concentrations of heavy metals may be attributable in large part to an accumulation of endogenous ammonia. The negative relationship between plasma ammonia concentration and U(crit) was similar in size-matched rainbow and brown trout but, under similar regimes of ammonia exposure, rainbow trout were able to maintain a significantly lower plasma ammonia concentration, revealing inter-specific differences in ammonia permeability and/or transport. One primary mechanism by which ammonia accumulation may impair exercise performance is a partial depolarisation of membrane potential in tissues such as the brain and white muscle. This may prejudice the co-ordination of swimming movements and reduce or abolish the development of muscle tension, thus, compromising swimming efficiency and performance at the top end of the range.