Neil B. Metcalfe

Compensation for a bad start: grow now, pay later?

Nutritional conditions during key periods of development, when the architecture and modus operandi of the body become established, are of profound importance in determining the subsequent life-history trajectory of an organism. If developing individuals experience a period of nutritional deficit, they can subsequently show accelerated growth should conditions improve, apparently compensating for the initial setback. However, recent research suggests that, although compensatory growth can bring quick benefits, it is also associated with a surprising variety of costs that are often not evident until much later in adult life. Clearly, the nature of these costs, the timescale over which they are incurred and the mechanisms underlying them will play a crucial role in determining compensatory strategies. Nonetheless, such effects remain poorly understood and largely neglected by ecologists and evolutionary biologists.

Oxidative stress as a mediator of life history trade-offs: mechanisms, measurements and interpretation

The concept of trade-offs is central to our understanding of life-history evolution. The underlying mechanisms, however, have been little studied. Oxidative stress results from a mismatch between the production of damaging reactive oxygen species (ROS) and the organisms capacity to mitigate their damaging effects. Managing oxidative stress is likely to be a major determinant of life histories, as virtually all activities generate ROS. There is a recent burgeoning of interest in how oxidative stress is related to different components of animal performance. The emphasis to date has been on immediate or short-term effects, but there is an increasing realization that oxidative stress will influence life histories over longer time scales. The concept of oxidative stress is currently used somewhat loosely by many ecologists, and the erroneous assumption often made that dietary antioxidants are necessarily the major line of defence against ROS-induced damage. We summarize current knowledge on how oxidative stress occurs and the different methods for measuring it, and highlight where ecologists can be too simplistic in their approach. We critically review the potential role of oxidative stress in mediating life-history trade-offs, and present a framework for formulating appropriate hypotheses and guiding experimental design. We indicate throughout potentially fruitful areas for further research.

Modelling the proximate basis of salmonid life-history variation, with application to Atlantic salmon, Salmo salar L.

Summary The great diversity of life-history patterns in the salmonids has stimulated many theoretical studies. However, virtually all studies are based on ultimate considerations, in which predictions are made by comparing the expected reproductive success of diAerent developmental or life-history pathways and choosing the one (or ones) with the highest fitness. Such models are post hoc because they attribute fitness to individuals at the completion of the particular phase of the life cycle and do not attempt to characterize the mechanisms that animals use to achieve the life-history pattern. We describe a model, based on proximate considerations, for salmonid life histories, focused on Atlantic salmon Salmo salar L. The model involves identification of the times at which developmental conversions are initiated or inhibited and the connection between physiological states and the thresholds for such conversions. Developmental paths are based on the comparison of the current physiological status of the fish (and its change of state) with a genetic threshold. The state of the fish and rate of change of state are determined by environmental opportunity, but the threshold is genetic. This approach therefore immediately generates a genotype‐environment interaction. We use expected reproductive success to determine the fitness of individuals with diAerent genetically determined thresholds. Instead of finding an optimal life history, our theory generates fitness surfaces for diAerent life histories, so that variation is inherent in this approach. We describe and explain the structure of the model and present evidence on which this structure is based, thus providing a framework within which one can understand how ecology relates to the physiological mechanisms leading to the developmental changes of smolt metamorphosis and maturation.

Large–scale geographical variation confirms that climate change causes birds to lay earlier

Advances in the phenology of organisms are often attributed to climate change, but alternatively, may reflect a publication bias towards advances and may be caused by environmental factors unrelated to climate change. Both factors are investigated using the breeding dates of 25 long–term studied populations of Ficedula flycatchers across Europe. Trends in spring temperature varied markedly between study sites, and across populations the advancement of laying date was stronger in areas where the spring temperatures increased more, giving support to the theory that climate change causally affects breeding date advancement.

Telomere length in early life predicts lifespan

The attrition of telomeres, the ends of eukaryote chromosomes, is thought to play an important role in cell deterioration with advancing age. The observed variation in telomere length among individuals of the same age is therefore thought to be related to variation in potential longevity. Studies of this relationship are hampered by the time scale over which individuals need to be followed, particularly in long-lived species where lifespan variation is greatest. So far, data are based either on simple comparisons of telomere length among different age classes or on individuals whose telomere length is measured at most twice and whose subsequent survival is monitored for only a short proportion of the typical lifespan. Both approaches are subject to bias. Key studies, in which telomere length is tracked from early in life, and actual lifespan recorded, have been lacking. We measured telomere length in zebra finches (n = 99) from the nestling stage and at various points thereafter, and recorded their natural lifespan (which varied from less than 1 to almost 9 y). We found telomere length at 25 d to be a very strong predictor of realized lifespan (P < 0.001); those individuals living longest had relatively long telomeres at all points at which they were measured. Reproduction increased adult telomere loss, but this effect appeared transient and did not influence survival. Our results provide the strongest evidence available of the relationship between telomere length and lifespan and emphasize the importance of understanding factors that determine early life telomere length.

Early Social Status and the Development of Life-History Strategies in Atlantic Salmon

Atlantic salmon have a variable life cycle. In good growing conditions, underyearling fish may metamorphose into the migratory smolt phase during their second spring, or delay at least a further year. The strategy adopted by particular fish appears to become fixed during their first summer. This paper examines whether either feeding efficiency or dominance in mid-summer correlates with the life-history strategy adopted. Eighty fish were individually marked and their feeding efficiency ( = mean handling time for food items) and dominance rank measured under laboratory conditions in mid-July. Growth rates of the fish were then monitored over the next three months, until developmental strategies became apparent. Discriminant and logistic regression analyses revealed that both dominance rank and size attained by July were independent, significant predictors of future developmental pattern (the age at metamorphosis being correctly predicted on the basis of rank and size in 84% of cases) whereas feeding efficiency had no effect. Thus fish that were dominant or larger two months after first feeding or both had a greater probability of migrating after only one year in freshwater than those more subordinate or smaller or both.

What causes intraspecific variation in resting metabolic rate and what are its ecological consequences

Individual differences in the energy cost of self-maintenance (resting metabolic rate, RMR) are substantial and the focus of an emerging research area. These differences may influence fitness because self-maintenance is considered as a life-history component along with growth and reproduction. In this review, we ask why do some individuals have two to three times the ‘maintenance costs’ of conspecifics, and what are the fitness consequences? Using evidence from a range of species, we demonstrate that diverse factors, such as genotypes, maternal effects, early developmental conditions and personality differences contribute to variation in individual RMR. We review evidence that RMR is linked with fitness, showing correlations with traits such as growth and survival. However, these relationships are modulated by environmental conditions (e.g. food supply), suggesting that the fitness consequences of a given RMR may be context-dependent. Then, using empirical examples, we discuss broad-scale reasons why variation in RMR might persist in natural populations, including the role of both spatial and temporal variation in selection pressures and trans-generational effects. To conclude, we discuss experimental approaches that will enable more rigorous examination of the causes and consequences of individual variation in this key physiological trait.

The influence of predation risk on the feeding motivation and foraging strategy of juvenile Atlantic salmon

Juvenile Atlantic salmon, Salmo salar, changed their foraging strategy markedly after a brief exposure to a model trout predator, in ways that reduced their conspicuousness and hence risk of being preyed upon. After seeing the predator, the salmon were less likely to orientate to passing food particles, and having orientated, were less likely to attack them. They also reduced the extent of their movements, by only attacking those food particles that came close to them, and by delaying attacks until the food had reached its closest point. They were slower to orientate to approaching food items, possibly because more visual attention was switched to scanning for predators and less to feeding. However, there was no change in the outcome of attacks, indicating that the reduced food intake was not caused by a reduction in appetite. The relative priority given to foraging and predator avoidance varied with time elapsed since the predator was last sighted; as a consequence, intake rates in the 20 min following the predator presentation averaged only 33% of the pre-predator level, but had increased to 57% 20 min later, and had recovered completely within 2 h.

The effects of habitat on the vigilance of shorebirds: Is visibility important?

Abstract Previous studies of vigilance have concentrated on situations where the prey species has an unimpaired view of its surroundings. Here the effects of reduced visibility caused by objects adjacent to the prey are studied in two species of shorebird. A reduction in visibility causes an increase in the level of vigilance, indicating an increase in vulnerability despite the greater degree of camouflaging. This increase is due to individuals being less able to see both approaching predators and their neighbours. Turnstones, Arenaria interpres , and purple sandpipers, Calidris maritima , show very similar increases in the level of vigilance with decreasing visibility, but achieve these increases by different means: turnstones lengthen the duration of each vigilant scan, while purple sandpipers scan more often. Increasing scanning rate produces a shortened interval between scans, which reduces the risk of being caught unawares by an approaching predator. However, it may also reduce feeding efficiency, and it is suggested that this might be more serious in turnstones due to greater handling times for food items, so causing them to adopt a different strategy to increase vigilance.

Changing priorities: the effect of pre-migratory fattening on the trade-off between foraging and vigilance

SummaryMany birds accumulate fat reserves prior to departure on long distance migration. Since there will be an increased food requirement during the pre-migratory period, it is to be expected that more time will be invested in foraging, at the expense of other activities. The allocation of time to anti-predatory behavior in migratory ruddy turnstones (adults) was found to decrease prior to migration (Fig. 1); non-migratory individuals (juveniles) showed no decrease over the same time period (Fig. 2). This is interpreted as a change in the optimal adult behavior, the cost of a reduced rate of resource accumulation outweighing the additional risk of predation which results from the decrease in vigilance.