Age‐related breeding success in little penguins: a result of selection and ontogenetic changes in foraging and phenology

Abstract

Reproductive performance typically improves with age, reaching a plateau at middle age and subsequently declining in older age classes (senescing individuals). Three potential non-exclusive mechanisms can explain the improvement in reproductive performance with age: (1) selection (poor quality individuals are removed from the population with increasing age), ( 2) constraint (individual efficiency increases through experience), and (3) restraint (reproductive investment increases with age as the residual reproductive value decreases). While all three mechanisms received strong empirical support, few studies have aimed at teasing apart those hypotheses and understanding their underlying functioning. In little penguins (Eudyptula minor), we used a 19-yr longitudinal dataset on breeding and foraging of more than 450 individuals to investigate the effect of age on breeding success. We separated within-individual from among-individual age effects using state-of-the-art statistical methods (within-subject centering and population change decomposition). We then assessed whether within-individual changes in breeding resulted from ontogenetic changes in foraging performances, breeding phenology or access to mates and nest sites. Fidelity and assortative pairing explained the high correlation in male and female ages within a pair. Breeding performances followed a typical bell-shaped curve with performance increasing up to 8 yr old, before reaching a plateau and subsequently declining after age 16. Both selection and within-individual processes occurred, although within-individual changes dominated differences in age-dependent breeding success. The selective appearance had almost no effect (apart from ages 2-3), and selective disappearance mostly affected changes at old ages (above 16), although they were also responsible for the slight increase in reproductive performances from ages 5-8. Focusing on within-individual changes, birds exhibited higher performances at middle ages, with birds foraging better, laying earlier and changing partner and nest less often. Their reproductive investment did not vary with age for females and slightly decreased for males. This supports the constraint hypothesis but not the restraint one. Finally, the increase in breeding performances at young ages was explained by the age-related increase in foraging performances during chick-rearing and advancement of laying. In contrast, reproductive senescence was defined by a general decrease in bird performances.

High-resolution recording of foraging behaviour over multiple annual cycles shows decline in old Adélie penguins' performance

“…R. Soc. B 290: 20222480 acute survival bottlenecks are most likely [47], and/or during the first reproductive event [48], and late in life [14]. Importantly, foraging dive frequency and foraging depth were most affected by the different periods of the annual life cycle, with dive frequency greatest at the times of highest energetic demand, i.e.…”

“…[5]), where no evidence for senescence was found, such ontogenetic change in performance may have been concealed by the selective disappearance (i.e. increased mortality over time) of underperforming individuals [14].…”

“…To disentangle the effect of the time elapsed since initial device attachment (reflecting ageing within age classes and coded as an integer from 1 to 3) from the year-to-year variations generated by environmental fluctuations, we centred individual foraging dive frequency, maximum depth and descent rate of foraging dives within each year by subtracting the yearly average value excluding the Incubation and Chick-rearing periods for which there are no data in 2016/17 [4,14]. This procedure removed year-to-year variation as well as potential biases linked to covariation between time since initial device attachment and year.…”

“…By contrast to early life improvement, evidence for agerelated variation in foraging performance later in life is scarce [8]. Among the recent studies quantifying the effect of true age on the foraging performance of seabirds [5,[9][10][11][12][13][14], only two of these detected signs of foraging senescence [12,14] and all but one [14] were cross-sectional, breeding season-focused studies.…”

“…While comparative analyses showed that senescence in survival and reproduction is widespread in terrestrial birds and mammals [15], the onset of senescence might be difficult to detect in the wild because (1) high levels of extrinsic mortality (e.g. through predation) could remove individuals from the population before senescence becomes evident [16]although ageing theory also predicts that species with high extrinsic mortality deteriorate faster [15]; (2) old individuals could adjust their behaviour to compensate for decreased performance due to physiological decline [9]; and/or (3) a decrease in performance due to senescence might be partially masked by selective disappearance when conducting studies at the population scale [14]. Resolving these issues is possible through the collection of high-temporal-resolution data, encompassing more than just the breeding season (when individuals are more likely to adjust their behaviour to maximize their reproductive output) within a longitudinal framework.…”