Under life‐history theories of ageing, increased senescence should follow relatively high reproductive effort. This expectation has rarely been tested against senescence varying between and within the two sexes, although such an approach may clarify the origins of sex‐specific ageing in the context of a given mating system. Nazca boobies (Sula granti; a seabird) practise serial monogamy and biparental care. A male‐biased population sex ratio results in earlier and more frequent breeding by females. Based on sex‐specific reproductive schedules, females were expected to show faster age‐related decline for survival and reproduction. Within each sex, high reproductive effort in early life was expected to reduce late‐life performance and accelerate senescence. Longitudinal data were used to (a) evaluate the sex specificity of reproductive and actuarial senescence and then (b) test for early‐/late‐life fitness trade‐offs within each sex. Within‐sex analyses inform an interpretation of sex differences in senescence based on costs of reproduction. Analyses incorporated individual heterogeneity in breeding performance and cohort‐level differences in early‐adult environments. Females showed marginally more intense actuarial senescence and stronger age‐related declines for fledging success. The opposite pattern (earlier and faster male senescence) was found for breeding probability. Individual reproductive effort in early life positively predicted late‐life reproductive performance in both sexes and thus did not support a causal link between early‐reproduction/late‐life fitness trade‐offs and sex differences in ageing. A high‐quality diet in early adulthood reduced late‐life survival (females) and accelerated senescence for fledging success (males). This study documents clear variation in ageing patterns—by sex, early‐adult environment and early‐adult reproductive effort—with implications for the role mating systems and early‐life environments play in determining ageing patterns. Absent evidence for a disposable soma mechanism, patterns of sex differences in senescence may result from age‐ and condition‐dependent mate choice interacting with this population's male‐biased sex ratio and mate rotation.
Climate change effects on population dynamics of natural populations are well documented at higher latitudes, where relatively rapid warming illuminates cause-effect relationships, but not in the tropics and especially the marine tropics, where warming has been slow. Here we forecast the indirect effect of ocean warming on a top predator, Nazca boobies in the equatorial Galá pagos Islands, where rising water temperature is expected to exceed the upper thermal tolerance of a key prey item in the future, severely reducing its availability within the boobies' foraging envelope. From 1983 to 1997 boobies ate mostly sardines, a densely aggregated, highly nutritious food. From 1997 until the present, flying fish, a lower quality food, replaced sardines. Breeding success under the poor diet fell dramatically, causing the population growth rate to fall below 1, indicating a shrinking population. Population growth may not recover: rapid future warming is predicted around Galá pagos, usually exceeding the upper lethal temperature and maximum spawning temperature of sardines within 100 years, displacing them permanently from the boobies' island-constrained foraging range. This provides rare evidence of the effect of ocean warming on a tropical marine vertebrate.
We present the first nitrogen isotope (δ15N) measurements of planktic foraminifera, paleoceanographically important zooplankton, from the nutrient‐rich waters of the modern Southern Ocean. Foraminifera were collected from net tows in the Subantarctic and Polar Frontal Zones (SAZ and PFZ, respectively) south of Africa during winter 2015 and late summer 2016. In late summer, consistent with preferential uptake of 14N‐nitrate and the progressive, northward depletion of nitrate by phytoplankton across the Southern Ocean, foraminifer tissue and shell‐bound δ15N rise equatorward along with nitrate δ15N. However, foraminifer δ15N is ~3‰ lower than expected for heterotrophs relying on photosynthetic biomass generated directly from nitrate. This discrepancy appears to originate with the particulate organic N (PON) in late‐summer surface waters, the δ15N of which is lowered by ammonium recycling. In winter, when overall productivity and foraminifer production are reduced, foraminifer δ15N is higher (by 4.6 ± 0.8‰ for tissue and by 4.0 ± 1.5‰ for shell‐bound N compared to late summer) and exhibits no clear north‐south trend. These characteristics can also be explained by the feeding‐driven connection of foraminifera to PON, which is elevated in δ15N by net degradation in winter. Therefore, foraminifer δ15N is more closely tied to PON δ15N than to nitrate δ15N in the Southern Ocean mixed layer. Combining our isotope data with previously reported sediment trap fluxes from the western Pacific SAZ/PFZ suggests that, under modern conditions, the late‐summer ammonium recycling signal outweighs that of wintertime decomposition on the annually integrated δ15N of sinking foraminifera.
Age and environment are important determinants of reproductive parameters in long‐lived organisms. These factors may interact to determine breeding responses to environmental change, yet few studies have examined the environmental dependence of aging patterns across the entire life span. We do so, using a 20‐yr longitudinal data set of reproductive phenotypes in long‐lived female Nazca boobies (Sula granti), a monogamous seabird breeding in the eastern tropical Pacific. Young and old females may suffer from inexperience and senescence, respectively, and/or practice reproductive restraint. Breeding performance (for breeding participation, breeding date, clutch size, egg volume, and offspring production) was expected to be lower in these age classes, particularly under environmental challenge, in comparison with middle‐aged breeders. Sea surface temperature anomalies (SSTA) represented interannual variation in the El Niño–Southern Oscillation (ENSO) and were one proxy for environmental quality (a population count of clutch initiations was a second). Although only females lay eggs, both sexes care for eggs and nestlings, and the male partner’s age, alone or in interaction with female age, was evaluated as a predictor of breeding performance. Middle‐aged females performed better than young and old birds for all reproductive traits. Pairing with a young male delayed breeding (particularly for old females) and reduced clutch size, and pairing with an old male reduced offspring production. Challenging environments increased age effects on breeding probability and breeding date across young to middle ages and for offspring production across middle to old ages. However, important exceptions to the predicted patterns for clutch size and fledging success across young to middle ages suggested that trade‐offs between fitness components may complicate patterns of trait expression across the life span. Relationships between breeding participation, environment, and individual quality and/or experience in young females may also contribute to unexpected patterns for clutch size and fledging success, traits expressed only in breeders. Finally, independent of age, breeding responses of female Nazca boobies to the ENSO did not follow expectations derived from oceanic forcing of primary productivity. During El Niño‐like conditions, egg‐laying traits (clutch size, breeding date) improved, but offspring production declined, whereas La Niña‐like conditions were “poor” environments throughout the breeding cycle.
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