Casual movement speed but not maximal locomotor capacity predicts mate searching success.

Maximal locomotor performance is often used as a proxy for fitness. Maximal speed may be important under high-threat conditions, such as during predator escape. However, animals do not always move at a speed that reflects their maximal physiological capacities when undisturbed. The physiological factors that determine the movement speed chosen by animals, such as minimization of energy use, may be independent from maximal performance. As a result, the casual speed at which individuals move when undisturbed in a given context may better represent an individual's motivation to move. The casual speed may therefore be a better predictor of fitness in natural contexts than maximal performance capacity. We tested the hypothesis that casual movement speed rather than maximal speed predicts fitness in the golden orb-web spider, Nephila plumipes. We measured fitness in two separate contexts, mate-searching success and the positional rank near a female. We show that casual but not maximal locomotor speed predicted both aspects of fitness. Casual speed was linearly related to maximal speed, indicating that casual speed is determined by physiological optimization. Size and metabolic scope were not related to either maximal or chosen speeds, indicating that the supply of ATP does not limit locomotor performance in this species. Overall, our results demonstrate that locomotor performance is related to fitness, but suggest that different types of performance and not necessarily maximal physiological capacities are most relevant for particular ecologically relevant tasks.

Injury-mediated decrease in locomotor performance increases predation risk in schooling fish.

The costs and benefits of group living often depend on the spatial position of individuals within groups and the ability of individuals to occupy preferred positions. For example, models of predation events for moving prey groups predict higher mortality risk for individuals at the periphery and front of groups. We investigated these predictions in sardine (Sardinella aurita) schools under attack from group hunting sailfish (Istiophorus platypterus) in the open ocean. Sailfish approached sardine schools about equally often from the front and rear, but prior to attack there was a chasing period in which sardines attempted to swim away from the predator. Consequently, all sailfish attacks were directed at the rear and peripheral positions of the school, resulting in higher predation risk for individuals at these positions. During attacks, sailfish slash at sardines with their bill causing prey injury including scale removal and tissue damage. Sardines injured in previous attacks were more often found in the rear half of the school than in the front half. Moreover, injured fish had lower tail-beat frequencies and lagged behind uninjured fish. Injuries inflicted by sailfish bills may, therefore, hinder prey swimming speed and drive spatial sorting in prey schools through passive self-assortment. We found only partial support for the theoretical predictions from current predator-prey models, highlighting the importance of incorporating more realistic predator-prey dynamics into these models.This article is part of the themed issue 'Physiological determinants of social behaviour in animals'.

Obesity-induced decreases in muscle performance are not reversed by weight loss.

BACKGROUND/OBJECTIVES: Obesity can affect muscle phenotypes, and may thereby constrain movement and energy expenditure. Weight loss is a common and intuitive intervention for obesity, but it is not known whether the effects of obesity on muscle function are reversible by weight loss. Here we tested whether obesity-induced changes in muscle metabolic and contractile phenotypes are reversible by weight loss. SUBJECTS/METHODS: We used zebrafish (Danio rerio) in a factorial design to compare energy metabolism, locomotor capacity, muscle isometric force and work-loop power output, and myosin heavy chain (MHC) composition between lean fish, diet-induced obese fish, and fish that were obese and then returned to lean body mass following diet restriction. RESULTS: Obesity increased resting metabolic rates (P<0.001) and decreased maximal metabolic rates (P=0.030), but these changes were reversible by weight loss, and were not associated with changes in muscle citrate synthase activity. In contrast, obesity-induced decreases in locomotor performance (P=0.0034), and isolated muscle isometric stress (P=0.01), work-loop power output (P<0.001) and relaxation rates (P=0.012) were not reversed by weight loss. Similarly, obesity-induced decreases in concentrations of fast and slow MHCs, and a shift toward fast MHCs were not reversed by weight loss. CONCLUSION: Obesity-induced changes in locomotor performance and muscle contractile function were not reversible by weight loss. These results show that weight loss alone may not be a sufficient intervention.

Increased aggression during pregnancy comes at a higher metabolic cost.

Aggressive behaviour is linked to fitness, but it is metabolically costly. Changes in metabolic demand during the reproductive cycle could constrain activity and thereby modulate behavioural phenotypes. We predicted that increased metabolic demands in late pregnancy would lead to reduced aggression and a lower metabolic cost of behaviour in the mosquitofish Gambusia holbrooki. Contrary to our prediction, females became more aggressive in late pregnancy, but metabolic scope (i.e. the metabolic energy available for activity and behaviour) decreased. Consequently, late-stage pregnant females spent significantly more of their available metabolic scope on aggressive behaviour. Hence, as pregnancy progressed, females showed increasingly risky behaviour by depleting metabolic resources available for activities other than fighting. We argue that the metabolic cost of behaviour, and possibly personality, is best expressed with reference to metabolic scope, rather than resting metabolic rates or concentrations of metabolites. This dependence on metabolic scope could render reproductive success sensitive to environmental changes.

Thermal acclimation and regulation of metabolism in a reptile (Crocodylus porosus): the importance of transcriptional mechanisms and membrane composition.

Energy metabolism is fundamental for animal fitness because it fuels locomotion, growth, and reproduction. Mitochondrial capacities often acclimate to compensate for negative thermodynamic effects. Our aim was to determine the importance of transcriptional regulation and membrane fatty acid composition in modulating oxidative capacities at body temperatures selected in a cold and a warm environment by a reptile (Crocodylus porosus). In the cool environment (mean selected T(b) = 21 degrees C), mRNA concentrations of the transcription factor peroxisome proliferator-activated receptor gamma (PPARgamma) and its coactivator PPARgamma coactivator 1 alpha (PGC-1alpha), as well as of the cytochrome c oxidase (COX) subunits COX1 and COX5, were significantly higher in the liver but not in skeletal muscle compared with animals in the warm environment (mean selected T(b) = 29 degrees C). F(O)F(1)-ATPase subunit alpha mRNA concentrations were significantly higher in both muscle and the liver in the cool animals. A positive relationship between PGC-1alpha and PPARgamma mRNA concentrations, with an indicator of mitochondrial density (16S rRNA) in muscle and COX and F(O)F(1)-ATPase subunit alpha mRNA concentrations in liver, suggest that these proteins regulate quantity increases of mitochondria during acclimation. The percent saturated fatty acids in liver membranes of cool animals was significantly lower, and the n3 fatty acid content was significantly higher, compared with in warm animals. The n3 fatty acid content was positively related to COX enzyme activity in the liver, and there was a negative relationship between n7 fatty acid content and COX activity in muscle. Hence, metabolic acclimation is mediated by both transcriptional regulation and membrane fatty acid composition. The importance of PGC-1alpha and PPARgamma in a reptile indicate that the mechanisms that regulate metabolism are conserved among vertebrates.

Can phenotypic plasticity facilitate the geographic expansion of the tilapia Oreochromis mossambicus?

Climate influences the distribution of organisms because of the thermal sensitivity of biochemical processes. Animals may compensate for the effects of variable temperatures, and plastic responses may facilitate radiation into different climates. The tropical fish Oreochromis mossambicus has radiated into climates that were thought to be thermally unsuitable. Here, we test the hypothesis that thermal acclimation will extend the locomotory and metabolic performance range of O. mossambicus. Juvenile fish were acclimated to 14 degrees, 17 degrees, and 22 degrees C. We measured responses to acclimation at three levels of organization: whole-animal performance (sustained swimming and resting and recovery rates of oxygen consumption), mitochondrial oxygen consumption in caudal muscle, and metabolic enzyme activities in muscle and liver at 12 degrees, 14 degrees, 17 degrees, 22 degrees, and 26 degrees C. Thermal optima of sustained swimming performance (U(crit)) changed significantly with acclimation, but acclimation had no effect on either resting or recovery oxygen consumption. Fish compensated for cold temperatures by upregulating state 3 mitochondrial oxygen consumption and increasing activity of lactate dehydrogenase in the liver. The capacity for phenotypic plasticity in O. mossambicus means that the fish would not be limited by its locomotor performance or metabolic physiology to expand its range into cooler thermal environments from its current distribution.

Compensation for environmental change by complementary shifts of thermal sensitivity and thermoregulatory behaviour in an ectotherm.

Thermoregulating animals are thought to have evolved a preferred body temperature at which thermally sensitive performance is optimised. Even during thermoregulation, however, many animals experience pronounced variability in body temperature, and may regulate to different body temperatures depending on environmental conditions. Here we test the hypothesis that there is a trade-off between regulating to lower body temperatures in cooler conditions and locomotory and metabolic performance. Animals (estuarine crocodiles, Crocodylus porosus) acclimated to cold (N=8) conditions had significantly lower maximum and mean daily body temperatures after 33 days than warm-acclimated animals (N=9), despite performing characteristic thermoregulatory behaviours. Concomitant with behavioural changes, maximum sustained swimming speed (U(crit)) shifted to the respective mean body temperatures during acclimation (cold=20 degrees C, warm=29 degrees C), but there was no difference in the maxima between acclimation groups. Mitochondrial oxygen consumption changed significantly during acclimation, and maximum respiratory control ratios coincided with mean body temperatures in liver, muscle and heart tissues. There were significant changes in the activities of regulatory metabolic enzymes (lactate dehydrogenase, citrate synthase, cytochrome c oxidase) and these were tissue specific. The extraordinary shift in behaviour and locomotory and metabolic performance shows that within individuals, behaviour and physiology covary to maximise performance in different environments.

Turtles (Chelodina longicollis) regulate muscle metabolic enzyme activity in response to seasonal variation in body temperature.

Fluctuations in the thermal environment may elicit different responses in animals: migration to climatically different areas, regulation of body temperature, modification of biochemical reaction rates, or assuming a state of dormancy. Many ectothermic reptiles are active over a range of body temperatures that vary seasonally. Here we test the hypothesis that metabolic enzyme activity acclimatises seasonally in freshwater turtles (Chelodina longicollis) in addition to, or instead of, behavioural regulation of body temperatures. We measured body temperatures in free-ranging turtles (n = 3) by radiotelemetry, and we assayed phosphofructokinase (PFK), lactate dehydrogenase (LDH), citrate synthase (CS) and cytochrome c oxidase (CCO) activities in early autumn (March, n = 10 turtles), late autumn (May, n = 7) and mid-winter (July, n = 7) over a range of assay temperatures (10 degrees C, 15 degrees C, 20 degrees C, 25 degrees C). Body temperatures were either not different from, or higher than expected from a theoretical null-distribution of a randomly moving animal. Field body temperatures at any season were lower, however, than expected from animals that maximised their sun exposure. Turtles maintained constant PFK, LDH and CCO activities in different months, despite body temperature differences of nearly 13.0 degrees C between March (average daily body temperature = 24.4 degrees C) and July (average = 11.4 degrees C). CS activity did not vary between March and May (average daily body temperature = 20.2 degrees C), but it decreased in July. Thus C. longicollis use a combination of behavioural thermoregulation and biochemical acclimatisation in response to seasonally changing thermal conditions. Ectothermic reptiles were often thought not to acclimatise biochemically, and our results show that behavioural attainment of a preferred body temperature is not mandatory for activity or physiological performance in turtles.

Changes in heart rate are important for thermoregulation in the varanid lizard Varanus varius.

Laboratory studies and a single field study have shown that heart rate in some reptiles is faster during heating than during cooling at any given body temperature. This phenomenon, which has been shown to reflect changes in peripheral blood flow, is shown here to occur in the lizard Varanus varius (lace monitor) in the wild. On a typical clear day, lizards emerged from their shelters in the morning to warm in the sun. Following this, animals were active, moving until they again entered a shelter in the evening. During their period of activity, body temperature was 34-36 degrees C in all six study animals (4.0-5.6 kg), but the animals rarely shuttled between sun and shade exposure. Heart rate during the morning heating period was significantly faster than during the evening cooling period. However, the ratio of heating to cooling heart rate decreased with increasing body temperature, being close to 2 at body temperatures of 22-24 degrees C and decreasing to 1.2-1.3 at body temperatures of 34-36 degrees C. There was a significant decrease in thermal time constants with increasing heart rate during heating and cooling confirming that changes in heart rate are linked to rates of heat exchange.

Control of heart rate during thermoregulation in the heliothermic lizard Pogona barbata: importance of cholinergic and adrenergic mechanisms.

During thermoregulation in the bearded dragon Pogona barbata, heart rate when heating is significantly faster than when cooling at any given body temperature (heart rate hysteresis), resulting in faster rates of heating than cooling. However, the mechanisms that control heart rate during heating and cooling are unknown. The aim of this study was to test the hypothesis that changes in cholinergic and adrenergic tone on the heart are responsible for the heart rate hysteresis during heating and cooling in P. barbata. Heating and cooling trials were conducted before and after the administration of atropine, a muscarinic antagonist, and sotalol, a beta-adrenergic antagonist. Cholinergic and beta-adrenergic blockade did not abolish the heart rate hysteresis, as the heart rate during heating was significantly faster than during cooling in all cases. Adrenergic tone was extremely high (92.3 %) at the commencement of heating, and decreased to 30.7 % at the end of the cooling period. Moreover, in four lizards there was an instantaneous drop in heart rate (up to 15 beats min(-1)) as the heat source was switched off, and this drop in heart rate coincided with either a drop in beta-adrenergic tone or an increase in cholinergic tone. Rates of heating were significantly faster during the cholinergic blockade, and least with a combined cholinergic and beta-adrenergic blockade. The results showed that cholinergic and beta-adrenergic systems are not the only control mechanisms acting on the heart during heating and cooling, but they do have a significant effect on heart rate and on rates of heating and cooling.

Heat transfer in a microvascular network: the effect of heart rate on heating and cooling in reptiles (Pogona barbata and Varanus varius).

Thermally-induced changes in heart rate and blood flow in reptiles are believed to be of selective advantage by allowing animal to exert some control over rates of heating and cooling. This notion has become one of the principal paradigms in reptilian thermal physiology. However, the functional significance of changes in heart rate is unclear, because the effect of heart rate and blood flow on total animal heat transfer is not known. I used heat transfer theory to determine the importance of heat transfer by blood flow relative to conduction. I validated theoretical predictions by comparing them with field data from two species of lizard, bearded dragons (Pogona barbata) and lace monitors (Varanus varius). Heart rates measured in free-ranging lizards in the field were significantly higher during heating than during cooling, and heart rates decreased with body mass. Convective heat transfer by blood flow increased with heart rate. Rates of heat transfer by both blood flow and conduction decreased with mass, but the mass scaling exponents were different. Hence, rate of conductive heat transfer decreased more rapidly with increasing mass than did heat transfer by blood flow, so that the relative importance of blood flow in total animal heat transfer increased with mass. The functional significance of changes in heart rate and, hence, rates of heat transfer, in response to heating and cooling in lizards was quantified. For example, by increasing heart rate when entering a heating environment in the morning, and decreasing heart rate when the environment cools in the evening a Pogona can spend up to 44 min longer per day with body temperature within its preferred range. It was concluded that changes in heart rate in response to heating and cooling confer a selective advantage at least on reptiles of mass similar to that of the study animals (0. 21-5.6 kg).

Field test of a paradigm: hysteresis of heart rate in thermoregulation by a free-ranging lizard (Pogona barbata).

The discovery that changes in heart rate and blood flow allow some reptiles to heat faster than they cool has become a central paradigm in our understanding of reptilian thermoregulation. However, this hysteresis in heart rate has been demonstrated only in simplistic laboratory heating and cooling trials, leaving its functional significance in free-ranging animals unproven. To test the validity of this paradigm, we measured heart rate and body temperature (Tb) in undisturbed, free-ranging bearded dragons (Pogona barbata), the species in which this phenomenon was first described. Our field data confirmed the paradigm and we found that heart rate during heating usually exceeded heart rate during cooling at any Tb. Importantly, however, we discovered that heart rate was proportionally faster in cool lizards whose Tb was still well below the 'preferred Tb range' compared to lizards whose Tb was already close to it. Similarly, heart rate during cooling was proportionally slower the warmer the lizard and the greater its cooling potential compared to lizards whose Tb was already near minimum operative temperature. Further, we predicted that, if heart rate hysteresis has functional significance, a 'reverse hysteresis' pattern should be observable when lizards risked overheating. This was indeed the case and, during heating on those occasions when Tb reached very high levels (> 40 degrees C), heart rate was significantly lower than heart rate during the immediately following cooling phase. These results demonstrate that physiological control of thermoregulation in reptiles is more complex than has been previously recognized.

Behavioural postures and the rate of body temperature change in wild freshwater crocodiles, Crocodylus johnstoni.

I recorded body temperature and behaviour of eight Crocodylus johnstoni in the wild over a 2-yr period in order to quantify the effect of posturing on body temperature and to provide a mechanistic explanation of how behaviour affects body temperature. Behaviour was categorised according to the proportion of a crocodile's surface area exposed from the water (0% exposed [=diving] to 100% exposed [=basking]). Crocodiles did not simply shuttle between the extremes of 100% exposed and diving but showed an array of intermediate postures. Rates of body temperature change were negative for exposures less than 40% and positive for 60%-100% exposed. This was due to the difference between operative temperature and body temperature, which was negative during diving but increased with the percentage of exposure, up to 25 degrees-30 degrees C during basking. For any particular posture, the rate of body temperature change decreased with increasing mass. Thermal time constants were shortest during diving and longest during basking. A heat-transfer equation predicted the rate of body temperature change well, except that it underestimated the rate of body temperature change during 80% and 100% exposed. Exposing only a small part of their body when in water (20%) slowed heat loss considerably, allowing crocodiles to spend more time in the water while maintaining body temperature within their preferred body temperature range.

Crocodiles as dinosaurs: behavioural thermoregulation in very large ectotherms leads to high and stable body temperatures

Empirical field data describing daily and seasonal cycles in body temperature (Tb) of free-ranging Crocodylus porosus (32-1010 kg) can be predicted by a mathematical analysis. The analysis provides a mechanistic explanation for the decreased amplitude of daily cycles in Tb and the increase in 'average' Tb with increasing mass. Assessments of 'average' daily Tb were made by dividing the integral of the difference between measured values of Tb and minimum operative temperature by the period of integration, to yield a thermal index expressing relative 'warmth' of crocodiles. The average daily Tb of a 1010 kg crocodile was 3.7 degreesC warmer than that of a 42 kg individual in summer and 1.9 degreesC warmer than that of a 32 kg individual in winter. The success of this mathematical approach confirms that crocodiles are simple ectotherms and that there is unlikely to be a significant contribution to their thermal biology from physiological mechanisms. Behaviour, however, is very important even in large individuals. Crocodiles in the field typically move daily between land and water in cycles that vary seasonally. We predicted Tb for the reverse of these behavioural cycles, which more than doubled seasonal fluctuations in Tb compared with the observed fluctuations. We were also able to predict the Tb of very large, dinosaur-sized crocodiles in a similar climate to that at our study site. A 10 000 kg 'crocodile', for example, would be expected to have a Tb of 31 degreesC in winter, varying by less than 0.1 degreesC during a day when operative temperatures varied by nearly 20 degreesC, from 20 to 38 degreesC. The study confirms that, in low latitudes at least, large dinosaurs must have had an essentially high and stable value of Tb, without any need for endothermy. Also, access to shade or water must have been crucial for the survival of large dinosaurs at low latitudes. Furthermore, the finding of increasing 'average' Tb as ectotherms grow larger may have implications for the metabolic rates of very large reptiles, because the Q10 effect could counteract the downscaling of metabolic rate with mass, an effect that seems not to have been recognised previously.