Who-Seung Lee

Experimental demonstration of the growth rate–lifespan trade-off

The hypothesized negative relationship between growth rate and lifespan has proved very difficult to test robustly because of potentially confounding variables, particularly nutrient availability and final size. Here we provide, to our knowledge, the first rigorous experimental test of this hypothesis, and find dramatic changes in lifespan in the predicted direction in response to both upward and downward manipulations of growth rates. We used brief (less than 4% of median lifespan) exposure to relatively cold or warm temperatures early in life to deflect juvenile three-spined sticklebacks Gasterosteus aculeatus from their normal growth trajectories; this induced catch-up or slowed-down growth when ambient temperatures were restored, and all groups attained the same average adult size. Catch-up growth led to a reduction in median lifespan of 14.5 per cent, while slowed-down growth extended lifespan by 30.6 per cent. These lifespan effects were independent of eventual size attained or reproductive investment in adult life. Photoperiod manipulations showed that the effects of compensatory growth on lifespan were also influenced by time available for growth prior to breeding, being more extreme when less time was available. These results demonstrate the growth–lifespan trade-off. While growing more slowly can increase longevity, the optimal resolution of the growth–lifespan trade-off is influenced by time constraints in a seasonal environment.

The pattern of early growth trajectories affects adult breeding performance

Early environmental conditions can influence the pattern of growth and development. While poor conditions generally cause slower growth, normal adult size can still be reached if growth accelerates or is prolonged once conditions improve, but such catch-up growth may have deleterious effects later in life. Here we investigate for the first time how decelerating as well as accelerating growth trajectories, manipulated independently of food supply, affect subsequent breeding performance. In order to alter growth rates we subjected juvenile three-spined sticklebacks Gasterosteus aculeatus to a short period of altered environmental temperature (high, intermediate, or low), after which all fish had the same (intermediate) temperature regime. In addition, the perceived time stress (until the onset of the spawning season) was manipulated by conducting the experiment twice (in the winter and in the spring immediately prior to breeding) and by exposing half of the fish in each experiment to a delayed photoperiod (two months behind ambient). We found that fish showed full growth compensation, such that in all treatments they were of the same average size by the start of the breeding season. However, those compensating for low temperatures earlier in life (i.e., who then showed an accelerated growth trajectory) had reduced reproductive investment over the following two breeding seasons (males, reduced sexual ornaments and speed of building nests; females, reduced first clutch size, mean egg size, and eggs produced per year). Moreover, these deleterious effects were strongest when the perceived time available for growth compensation prior to breeding was shortest. In contrast, those fish with a decelerating growth trajectory as a result of exposure to high temperatures early in life showed an improved breeding performance compared to steadily growing controls. These results clearly demonstrate that both the shape of the growth trajectory (independent of food supply) and the time available for growth compensation have broad-reaching and prolonged effects on breeding performance, with ecological conditions that prompt catch-up growth just prior to the breeding season being especially damaging for both sexes.

The trade-off between growth rate and locomotor performance varies with perceived time until breeding

SUMMARY Environmental circumstances can cause changes in early growth patterns that subsequently affect the adult phenotype. Here we investigated how different growth trajectories affected subsequent locomotor performance, and how such effects were influenced by the perceived time until the key life-history event of reproduction. Using juvenile three-spined sticklebacks Gasterosteus aculeatus, we show that a brief period of manipulated temperature in early life (independent of food supply) caused effects on skeletal growth trajectory not only during the manipulation itself, but also during a subsequent compensatory phase. The outcome of these changes was that fish in all treatment groups reached the same average size by sexual maturity, despite having different growth patterns. However, their growth trajectory had impacts on both pre-breeding swimming endurance and its decline over the course of the breeding season, such that swimming ability was negatively correlated with skeletal growth rate during the compensation period. We also show for the first time that ‘negative compensation’ (i.e. a decelerating growth trajectory) led to an improved swimming performance compared with steadily growing controls. Replicate experiments and photoperiod manipulations, moreover, revealed that the effects of growth rate on subsequent swimming performance were greater when the perceived time until the breeding season was shorter. These results show that the costs of accelerated or decelerated growth can last well beyond the time over which growth rates differ, and are affected by the time available until an approaching life history event such as reproduction, possibly because of the time available to repair the damage.

Egg survival is related to the colour matching of eggs to nest background in Black-tailed Gulls

A long-standing hypothesis posits that, for species with exposed nests, a close match between the colour of the eggs and that of the nest in which they are laid should enhance egg survival, but this has rarely been tested in a rigorous manner. Here, we demonstrate the effects of egg–nest colour matching on egg survival in Black-tailed Gulls (Larus crassirostris) on Hongdo Island, Korea. We quantified the ground colour of eggshells and that of the nest background using a digital camera and computerized RGB and greyscale colour systems. We show that a close match of eggshell ground colour and nest background colour was associated with increased chances of eggs surviving through to hatching. In particular, there were strong survival advantages for eggs matching the nest colour in sites with poor concealment, whereas there was no effect of eggshell ground colour in nests that were more concealed by vegetation. Our findings support the hypothesis that egg colour functions to make eggs cryptic and that egg colouration may be a significant factor affecting egg loss.

A Comparison of Dynamic-State-Dependent Models of the Trade-Off Between Growth, Damage, and Reproduction

Fast growth can be costly, so trade-offs between growth and fitness are to be predicted when organisms adjust their growth to compensate for earlier environmental conditions. We developed four generic models of increasing complexity with different processes to predict the indeterminate growth of vertebrate ectotherms, which is sensitive to ambient temperature even when food is not limiting. We contrast the predictions of the models with observed experimental data on growth trajectories, feeding activity, and reproductive investment of three-spined sticklebacks and inferred patterns of accumulation of biomolecular damage arising from activity and growth. All models predicted observed patterns of compensatory growth (both accelerating and decelerating) in response to earlier temperature perturbations, but the more complex models provided the best fit to experimental data. Growth trajectories influenced future reproductive investment regardless of final body size at breeding. Our findings suggest that while models with fewer parameters can predict basic patterns of growth in stable conditions, they cannot capture the costly long-term effects of deviations from steady growth trajectories. In contrast, models in which foraging activity is assumed to carry costs are capable of predicting the complex patterns of feeding, growth, and reproductive investment seen in animals, with the cost of a heightened mortality risk (e.g., through predation) being more important than the cost of increased physiological damage.

Perturbations in growth trajectory due to early diet affect age‐related deterioration in performance

Summary Fluctuations in early developmental conditions can cause changes in growth trajectories that subsequently affect the adult phenotype. Here, we investigated whether compensatory growth has long‐term consequences for patterns of senescence. Using three‐spined sticklebacks (Gasterosteus aculeatus), we show that a brief period of dietary manipulation in early life affected skeletal growth rate not only during the manipulation itself, but also during a subsequent compensatory phase when fish caught up in size with controls. However, this growth acceleration influenced swimming endurance and its decline over the course of the breeding season, with a faster decline in fish that had undergone faster growth compensation. Similarly, accelerated growth led to a more pronounced reduction in the breeding period (as indicated by the duration of sexual ornamentation) over the following two breeding seasons, suggesting faster reproductive senescence. Parallel experiments showed a heightened effect of accelerated growth on these age‐related declines in performance if the fish were under greater time stress to complete their compensation prior to the breeding season. Compensatory growth led to a reduction in median life span of 12% compared to steadily growing controls. While life span was independent of the eventual adult size attained, it was negatively correlated with the age‐related decline in swimming endurance and sexual ornamentation. These results, complementary to those found when growth trajectories were altered by temperature rather than dietary manipulations, show that the costs of accelerated growth can last well beyond the time over which growth rates differ and are affected by the time available until an approaching life‐history event such as reproduction.

Early growth trajectories affect sexual responsiveness.

The trajectory of an animals growth in early development has been shown to have long-term effects on a range of life-history traits. Although it is known that individual differences in behaviour may also be related to certain life-history traits, the linkage between early growth or development and individual variation in behaviour has received little attention. We used brief temperature manipulations, independent of food availability, to stimulate compensatory growth in juvenile three-spined sticklebacks Gasterosteus aculeatus. Here, we examine how these manipulated growth trajectories affected the sexual responsiveness of the male fish at the time of sexual maturation, explore associations between reproductive behaviour and investment and lifespan and test whether the perceived time stress (until the onset of the breeding season) influenced such trade-offs. We found a negative impact of growth rate on sexual responsiveness: fish induced (by temperature manipulation) to grow slowest prior to the breeding season were consistently quickest to respond to the presence of a gravid female. This speed of sexual responsiveness was also positively correlated with the rate of development of sexual ornaments and time taken to build a nest. However, after controlling for effects of growth rate, those males that had the greatest sexual responsiveness to females had the shortest lifespan. Moreover, the time available to compensate in size before the onset of the breeding season (time stress) affected the magnitude of these effects. Our results demonstrate that developmental perturbations in early life can influence mating behaviour, with long-term effects on longevity.

Evaluation of environmental factors to predict breeding success of Black-tailed Gulls

Abstract This study demonstrated prediction of breeding success of Black-tailed Gulls in relation to the selected environmental factors through evaluation of relative importance in determining breeding success. The data were obtained from the 258 selected and 120 non-selected sites for breeding of the gulls during the breeding periods in 2002–2003. Breeding success at the selected sites, and environmental factors such as vegetation cover, vegetation height, rock cover, nest-wall, nearest distance between neighbors and slope, were measured at each sampling site. For predicting breeding success of Black-tailed Gulls, we used two different artificial neural networks in this study: self-organizing map (SOM) and multilayer perceptron (MLP). SOM was used to classify the sampling sites based on the environmental factors, whereas MLP was implemented to prediction of breeding success of the gulls at the non-selected sites based on environmental conditions. In our results, SOM discriminated clearly the sampling sites and presented differences in environmental factors between the selected and non-selected sites. Subsequently, the breeding success was accordingly predicted by MLP. Nest-wall was considered the most important environmental factor in determining survival status of the gulls. An increase in nest-wall and vegetation cover was required to support breeding of the specimens for managing the habitats for Black-tailed Gulls.

Habitat Selection by Black-tailed Gulls on Hongdo Island, Korea

Abstract Habitat selection in Black-tailed Gulls (Larus crassirostris) on Hongdo Island, Korea, was studied during the breeding period in 2002-2003. To compare topographical advantages and disadvantages on breeding, we examined two habitats on the island: rocky-cliffs (lower and edge) and grassy (upper and inside) for differences in breeding biology and feeding frequency. In rocky-cliff habitat, Black-tailed Gulls had higher clutch size, faster laying and hatching date, and higher hatching and fledging success. Topographically, rocky-cliff habitat had two advantages-it was closer to sea and difficult to access. Proximity to the sea allowed higher feeding frequency whereas difficult access restricted predators. Conversely, grassy habitat was farther from the sea and allowed easier access to predators, but a lot of grass covered nests to protect eggs and chicks. These disadvantages caused low feeding frequency and higher hatching failure. Egging by fisherman was also a disadvantage of grassy habitat because of easy access from landing places. Therefore, our results suggested that rocky-cliff habitat was more profitable habitat than grassy habitat and this profitability was related to topographical difference between habitats.