Age effects on Nazca booby foraging performance are largely constant across variation in the marine environment: Results from a 5-year study in Galápagos.

Foraging outcomes dictate the nutritional resources available to an organism and may vary with intrinsic factors, like age. Thus, understanding how age affects foraging performance, alone or in interaction with extrinsic factors (like environmental quality), improves our understanding of aging processes in the wild. We examined how foraging traits, measured across five breeding seasons, change with age, environmental variation, and their interaction in Nazca boobies (Sula granti), a pelagic seabird in Galápagos. We evaluated the hypotheses that (1) foraging performance is better in middle-aged birds than in young ones, and that (2) foraging performance is better in middle-aged birds than in old ones. Furthermore, favorable environmental conditions will either (3) attenuate age differences in foraging performance (by relieving constraints on young, inexperienced and old, senescent age classes), or (4) accentuate age differences (if middle-aged birds can exploit abundant resources better than other age classes can). Incubating birds tagged with GPS loggers (N = 815) provided data on foraging performance (e.g., total distance traveled, mass gained) to evaluate interactions between age and environmental variation (e.g., sea surface temperature). Poor environmental conditions associated with the cool phase of the El Niño-Southern Oscillation increased foraging effort, including foraging distance and duration, for example. Across age classes, foraging boobies responded similarly to environmental variation except for female mass gain rate: age-related declines in mass gain rate were reduced under favorable environmental conditions. Birds of different ages also searched in somewhat distinct areas in the poor conditions of 2016, but not in other years. In several foraging traits, including foraging duration and distance, female boobies showed predicted early-life improvement and late-life decline, following the established pattern for reproductive traits in this species. Thus, deficits in resource acquisition (this study) may contribute to the poor survival and reproductive outcomes previously observed in old Nazca boobies, particularly in females.

Los resultados del forrajeo determinan los recursos nutricionales disponibles de un organismo, los cuales pueden variar por factores intrínsecos, como la edad. Por lo tanto, el entendimiento de cómo la edad afecta el rendimiento de forrajeo, sola o en interacción con factores extrínsecos (como la calidad ambiental), mejora nuestro entendimiento de los procesos del envejecimiento en la naturaleza. Nosotros examinamos como las características de forrajeo, a lo largo de cinco temporadas reproductivas, cambian con la edad, la variabilidad ambiental y sus interacciones en el Piquero de Nazca (Sula granti), un ave marina pelágica en las Islas Galápagos. Evaluamos las hipótesis que (1) el desempeño de búsqueda de alimentación es mejor en aves adultas que en las jóvenes, y que (2) este desempeño es mejor en aves adultas que en las viejas. Además, las condiciones ambientales favorables (3) atenuaran las diferencias de edades en el rendimiento de forrajeo (aliviando las restricciones en los jóvenes, inexpertos, y viejos), o (4) acentuaran las diferencias de edad (sí los adultos pueden explotar recursos abundantes de mejor forma que otros grupos etarios). Colocamos dispositivos GPS en aves incubadoras (N = 815), para colectar datos sobre el rendimiento del forrajeo (p. ej. distancia total de viaje, incremento de peso) para evaluar las interacciones entre edad y la variación ambiental (p. ej. temperatura superficial del mar). Las condiciones ambientales adversas relacionadas a la fase fría de El Niño Oscilación del Sur incrementaron el esfuerzo de forrajeo (la distancia de forrajeo y su duración, por ejemplo). En todos los grupos etarios, los piqueros respondieron de forma similar a la variación ambiental, excepto la tasa de ganancia de peso de las hembras. Las reducciones relacionadas a la edad en la tasa de ganancia de peso fueron menores durante condiciones ambientales favorables. Las aves de diferentes grupos etarios buscaron alimento en zonas levemente diferentes durante las condiciones adversas de 2016, pero no en otros años. En varias características de forrajeo, incluyendo la duración y la distancia, las hembras mostraron un esperado mejoramiento en los primeros años y un declive en su vida tardía, mostrando el patrón establecido en rasgos reproductivos en esta especie. Por lo tanto, el déficit en la adquisición de recursos (este estudio), puede contribuir a la reducida supervivencia y los resultados reproductivos previamente observados en piqueros de Nazca viejos, especialmente en las hembras.

Breeding responses to environmental variation are age- and trait-dependent in female Nazca boobies.

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.

Effects of age, sex, and ENSO phase on foraging and flight performance in Nazca boobies.

Age-related changes in survival and reproduction are common in seabirds; however, the underlying causes remain elusive. A lack of experience for young individuals, and a decline in foraging performance for old birds, could underlie age-related variation in reproduction because reproductive success is connected closely to provisioning offspring. For seabirds, flapping flight during foraging trips is physiologically costly; inexperience or senescent decline in performance of this demanding activity might cap delivery of food to the nest, providing a proximate explanation for poor breeding success in young and old age, respectively. We evaluated the hypothesis that young and old Nazca boobies (Sula granti), a Galápagos seabird, demonstrate deficits in foraging outcomes and flight performance. We tagged incubating male and female adults across the life span with both accelerometer and GPS loggers during the incubation periods of two breeding seasons (years), during the 2015 El Niño and the following weak La Niña. We tested the ability of age, sex, and environment to explain variation in foraging outcomes (e.g., mass gained) and flight variables (e.g., wingbeat frequency). Consistent with senescence, old birds gained less mass while foraging than middle-aged individuals, a marginal effect, and achieved a slower airspeed late in a foraging trip. Contrary to expectations, young birds showed no deficit in foraging outcomes or flight performance, except for airspeed (contingent on environment). Young birds flew slower than middle-aged birds in 2015, but faster than middle-aged birds in 2016. Wingbeat frequency, flap-glide ratio, and body displacement (approximating wingbeat strength) failed to predict airspeed and were unaffected by age. Sex influenced nearly all aspects of performance. Environment affected flight performance and foraging outcomes. Boobies' foraging outcomes were better during the extreme 2015 El Niño than during the 2016 weak La Niña, a surprising result given the negative effects tropical seabirds often experience during extreme El Niños.

Sex-specific patterns of senescence in Nazca boobies linked to mating system.

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.

Decadal-scale variation in diet forecasts persistently poor breeding under ocean warming in a tropical seabird.

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 Galápagos 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 Galápagos, 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.

Avian Pox Discovered in the Critically Endangered Waved Albatross (Phoebastria irrorata) from the Galápagos Islands, Ecuador.

The Waved Albatross (Phoebastria irrorata) is a critically endangered seabird in a rapidly shrinking population in the Galápagos Islands, Ecuador. The introduction of novel pathogens and parasites poses a threat to population persistence. Monitoring disease prevalence and guarding against the spread of such agents in endemic taxa are conservation priorities for the Galápagos, where recent increases in the prevalence of avian pox may have contributed to population declines and range contractions in other bird species. During November 2013-January 2014, we identified 14 Waved Albatross nestlings at our study site on Española Island with avian pox-like lesions and clinical signs. Other seabirds, landbirds, and adult Waved Albatrosses were apparently unaffected. Histopathology of tissue samples from five infected nestlings revealed inclusion bodies in all samples, consistent with avipoxvirus infection. We documented higher mortality (6 of 14 nestlings) in affected nestlings than in unaffected young in this small outbreak of avian pox, the first report of its kind in the world's only tropical albatross.

Yawning, acute stressors, and arousal reduction in Nazca booby adults and nestlings.

Yawning is a familiar and phylogenetically widespread phenomenon, but no consensus exists regarding its functional significance. We tested the hypothesis that yawning communicates to others a transition from a state of physiological and/or psychological arousal (for example, due to action of a stressor) to a more relaxed state. This arousal reduction hypothesis predicts little yawning during arousal and more yawning (above baseline) during and after down-regulation of arousal. Experimental capture-restraint tests with wild adult Nazca boobies (Sula granti), a seabird, increased yawning frequency after release from restraint, but yawning was almost absent during tests. Natural maltreatment by non-parental adults also increased yawning by nestlings, but only after the maltreatment ended and the adult left. CORT (corticosterone) was a logical a priori element of the stress response affecting the stressor-yawning relationship under the arousal reduction hypothesis, and cannot be excluded as such for adults in capture-restraint tests but is apparently unimportant for nestlings being maltreated by adults. The arousal reduction hypothesis unites formerly disparate results on yawning: its socially contagious nature in some taxa, its clear pharmacological connection to the stress response, and its temporal linkage to transitions in arousal between consciousness and sleep.