The effect of climate change on avian offspring production: A global meta-analysis.

Climate change affects timing of reproduction in many bird species, but few studies have investigated its influence on annual reproductive output. Here, we assess changes in the annual production of young by female breeders in 201 populations of 104 bird species (N = 745,962 clutches) covering all continents between 1970 and 2019. Overall, average offspring production has declined in recent decades, but considerable differences were found among species and populations. A total of 56.7% of populations showed a declining trend in offspring production (significant in 17.4%), whereas 43.3% exhibited an increase (significant in 10.4%). The results show that climatic changes affect offspring production through compounded effects on ecological and life history traits of species. Migratory and larger-bodied species experienced reduced offspring production with increasing temperatures during the chick-rearing period, whereas smaller-bodied, sedentary species tended to produce more offspring. Likewise, multi-brooded species showed increased breeding success with increasing temperatures, whereas rising temperatures were unrelated to reproductive success in single-brooded species. Our study suggests that rapid declines in size of bird populations reported by many studies from different parts of the world are driven only to a small degree by changes in the production of young.

Lack of age-related mosaic loss of W chromosome in long-lived birds.

Females and males often exhibit different survival in nature, and it has been hypothesized that sex chromosomes may play a role in driving differential survival rates. For instance, the Y chromosome in mammals and the W chromosome in birds are often degenerated, with reduced numbers of genes, and loss of the Y chromosome in old men is associated with shorter life expectancy. However, mosaic loss of sex chromosomes has not been investigated in any non-human species. Here, we tested whether mosaic loss of the W chromosome (LOW) occurs with ageing in wild birds as a natural consequence of cellular senescence. Using loci-specific PCR and a target sequencing approach we estimated LOW in both young and adult individuals of two long-lived bird species and showed that the copy number of W chromosomes remains constant across age groups. Our results suggest that LOW is not a consequence of cellular ageing in birds. We concluded that the inheritance of the W chromosome in birds, unlike the Y chromosome in mammals, is more stable.

Seasonal weather effects on offspring survival differ between reproductive stages in a long-lived neotropical seabird.

Weather conditions can profoundly affect avian reproduction. It is known that weather conditions prior to and after the onset of reproduction can affect the breeding success of birds. However, little is known about how seasonal weather variability can affect birds' breeding performance, particularly for species with a slow pace of life. Long-term studies are key to understanding how weather variability can affect a population's dynamics, especially when extreme weather events are expected to increase with climate change. Using a 32-year population study of the Blue-footed booby (Sula nebouxii) in Mexico, we show that seasonal variation in weather conditions, predominantly during the incubation stage, affects offspring survival and body condition at independence. During most of the incubation period, warm sea surface temperatures were correlated with low hatching success, while rainfall in the middle of the incubation stage was correlated with high fledging success. In addition, chicks from nests that experienced warm sea surface temperatures from the pre-laying stage to near-fledging had lower body condition at 70 days of age. Finally, we show that variable annual SST conditions before and during the incubation stage can impair breeding performance. Our results provide insight into how seasonal and interannual weather variation during key reproductive stages can affect hatching success, fledging success, and fledgling body condition in a long-lived neotropical seabird.

Pacific Decadal and El Niño oscillations shape survival of a seabird.

Understanding and modeling population change is urgently needed to predict effects of climate change on biodiversity. High trophic-level organisms are influenced by fluctuations of prey quality and abundance, which themselves may depend on climate oscillations. Modeling effects of such fluctuations is challenging because prey populations may vary with multiple climate oscillations occurring at different time scales. The analysis of a 28-yr time series of capture-recapture data of a tropical seabird, the Nazca Booby (Sula granti), in the Galápagos, Ecuador, allowed us to test for demographic effects of two major ocean oscillations occurring at distinct time-scales: the inter-annual El Niño Southern Oscillation (ENSO) and inter-decadal oscillations. As expected for a tropical seabird, survival of fledgling birds was highly affected by extreme ENSO events; by contrast, neither recruitment nor breeding participation were affected by either ENSO or decadal oscillations. More interesting, adult survival, a demographic trait that canalizes response to environmental variations, was unaffected by inter-annual ENSO oscillations yet was shaped by the Pacific Decadal Oscillation and small pelagic fish regime. Adult survival decreased during oceanic conditions associated with higher breeding success, an association probably mediated in this species by costs of reproduction that reduce survival when breeding attempts end later. To our knowledge, this is the first study suggesting that survival of a vertebrate can be vulnerable to a natural multidecadal oscillation.

Female infidelity is constrained by El Niño conditions in a long-lived bird.

Explaining the remarkable variation in socially monogamous females' extrapair (EP) behaviour revealed by decades of molecular paternity testing remains an important challenge. One hypothesis proposes that restrictive environmental conditions (e.g. extreme weather, food scarcity) limit females' resources and increase EP behaviour costs, forcing females to reduce EP reproductive behaviours. For the first time, we tested this hypothesis by directly quantifying within-pair and EP behaviours rather than inferring behaviour from paternity. We evaluated whether warmer sea surface temperatures depress total pre-laying reproductive behaviours, and particularly EP behaviours, in socially paired female blue-footed boobies (Sula nebouxii). Warm waters in the Eastern Pacific are associated with El Niño Southern Oscillation and lead to decreased food availability and reproductive success in this and other marine predators. With warmer waters, females decreased their neighbourhood attendance, total copulation frequency and laying probability, suggesting that they contend with restricted resources by prioritizing self-maintenance and committing less to reproduction, sometimes abandoning the attempt altogether. Females were also less likely to participate in EP courtship and copulations, but when they did, rates of these behaviours were unaffected by water temperature. Females' neighbourhood attendance, total copulation frequency and EP courtship probability responded to temperature differences at the between-season scale, and neighbourhood attendance and EP copulation probability were affected by within-season fluctuations. Path analysis indicated that decreased EP participation was not attributable to reduced female time available for EP activities. Together, our results suggest that immediate time and energy constraints were not the main factors limiting females' infidelity. Our study shows that El Niño conditions depress female boobies' EP participation and total reproductive activity. In addition to increasing general self-maintenance and reproductive costs, warm waters may increase costs specific to EP behaviours including divorce, reduced male parental care, or pathogen exposure. Our results suggest that female boobies strategically refrained from EP behaviours to avoid these or other longer-term costs, rather than being compelled by immediate constraints. This study demonstrates that current environmental conditions affect females' mating decisions, contributing to variation in EP behaviours, even in a long-lived, iteroparous species that can buffer against temporary adversity.

Behaviorally Induced Camouflage: A New Mechanism of Avian Egg Protection.

When animals potentially occupy diverse microhabitats, how can camouflage be achieved? Here we combine descriptive and experimental methods to uncover a novel form of phenotypic plasticity in the camouflage of bird eggs that may be present in other avian taxa. Soil from the bare substrate adheres to the blue-footed booby's (Sula nebouxii's) pale eggs, which parents manipulate both under and on top of their webs. Analysis of digital images confirmed that dirtiness increases progressively during the first 16 days of the incubation period, making eggs more similar to the nest substrate. Observations of 3,668 single-egg clutches showed that the probability of egg loss declines progressively over the same time frame and then remains low for the rest of the 41-day incubation period. An experiment showed that when chicken eggs are soiled and exposed in artificial booby nests, they are less likely to be taken by Heermann's gulls (Larus heermanni) than clean eggs.

Better stay together: pair bond duration increases individual fitness independent of age-related variation.

Prolonged pair bonds have the potential to improve reproductive performance of socially monogamous animals by increasing pair familiarity and enhancing coordination and cooperation between pair members. However, this has proved very difficult to test robustly because of important confounds such as age and reproductive experience. Here, we address limitations of previous studies and provide a rigorous test of the mate familiarity effect in the socially monogamous blue-footed booby, Sula nebouxii, a long-lived marine bird with a high divorce rate. Taking advantage of a natural disassociation between age and pair bond duration in this species, and applying a novel analytical approach to a 24 year database, we found that those pairs which have been together for longer establish their clutches five weeks earlier in the season, hatch more of their eggs and produce 35% more fledglings, regardless of age and reproductive experience. Our results demonstrate that pair bond duration increases individual fitness and further suggest that synergistic effects between a male and female's behaviour are likely to be involved in generating a mate familiarity effect. These findings help to explain the age- and experience-independent benefits of remating and their role in life-history evolution.

Parental overproduction allows siblicidal bird to adjust brood size to climate-driven prey variation.

Parental overproduction is hypothesized to hedge against uncertainty over food availability and stochastic death of offspring and to improve brood fitness. Understanding the evolution of overproduction requires quantifying its benefits to parents across a wide range of ecological conditions, which has rarely been done. Using a multiple hypotheses approach and 30 years of data, we evaluated the benefits of overproduction in the Blue-footed booby, a seabird that lays up to three eggs asynchronously, resulting in an aggressive brood hierarchy that facilitates the death of last-hatched chicks under low food abundance. Results support the resource-tracking hypothesis, as low prey abundance (estimated from sea surface temperature and chlorophyll-a concentration) led to rapid brood reduction. The insurance hypothesis was supported in broods of three, where last-hatched chicks' survival increased after a sibling's death. Conversely, in broods of two, results suggested that parents abandoned last-hatched chicks following first-hatched chicks' deaths. No direct evidence supported the facilitation hypothesis: the presence of a last-hatched chick during development did not enhance its sibling's fitness in the short or long term. The value of last-hatched offspring to parents, as "extra" or "insurance" varied with indices of food abundance, brood size, and parental age. Ninety percent of overproduction benefits came from enabling parents to capitalize on favorable conditions by fledging additional offspring. Our study provides insight into the forces driving overproduction, explaining the adaptiveness of this apparently wasteful behavior and allowing us to better predict how overproduction's benefits might be modified by ocean warming.

Apparent absence of avian malaria and malaria-like parasites in northern blue-footed boobies breeding on Isla Isabel.

Haemosporidian parasites are common in birds but are seldom reported in seabirds. The absence of vectors or genetic resistance to infection have been proposed to explain this pattern. However, screening of blood parasites in many seabirds has been done only by visual inspection of blood smears, which can miss low-intensity infections, and molecular detection of blood parasites must be supported by detection in blood smears to confirm the presence of haemosporidians and avoid false positive cases. Here, we tested for the presence of blood parasites of the genera Plasmodium, Haemoproteus and Leucocytozoon, combining inspection of blood smears and PCR-based detection methods in a highly philopatric colony of blue-footed boobies (Sula nebouxii) in the Tropical North Pacific. Our results indicate that adults in this colony are likely free of these blood parasites, probably due to unsuitable conditions for insect vectors in booby breeding sites, although potential genetic resistance of blue-footed boobies to infection deserves examination. Apparent absence of blood parasites in Isla Isabel boobies indirectly adds to the growing evidence of variation in parasite infections among avian host species that coexist locally.

El Niño in the warm tropics: local sea temperature predicts breeding parameters and growth of blue-footed boobies.

1. There is increasing interest in the impacts of El Niño Southern Oscillation (ENSO) on reproduction of apical predators such as seabirds and marine mammals. Long-term studies documenting ENSO effects on reproduction of seabirds in the warm tropics are scarce, and differential sensitivity of breeding parameters to ENSO has rarely been explored. 2. Analysis of 18 years of breeding data from a colony of the blue-footed booby Sula nebouxii (Milne-Edwards) showed a delay in onset of breeding when the global Southern Oscillation Index was negative; each unit of the atmospheric pressure differential (hPa) across the Pacific Ocean meant a delay of 7 days. 3. ENSO conditions also produced declines in breeding participation, clutch size, brood size, hatching success and fledging success, especially when surface waters surrounding the colony were warmer during winter and spring. Each additional degree (°C) of water temperature produced a reduction of 0.45 fledglings per nest. Different breeding parameters were sensitive to ENSO indices in different blocks of months. 4. Warming of local waters during the winter was associated with decline in ocean productivity in the current year and the following year, consistent with ENSO impacts on breeding parameters being mediated by effects on local productivity and prey availability. However, there was no evidence of lagged effects of ENSO on any breeding parameter. 5. Comparison of 5 years revealed that when local surface waters were warm, chicks grew more slowly, but no effects of ENSO on weight and size of eggs were evident in data of 9 and 7 years, respectively. 6. Our findings extend evidence of impacts of ENSO on seabird reproduction to the eastern tropical Pacific and indicate that several breeding parameters of blue-footed boobies (but not egg size) are affected in the short term by ENSO conditions, particularly by local anomalies in sea surface temperature associated with decline in ocean productivity.

Sibling bullying during infancy does not make wimpy adults.

Despite frequent suggestions that dominance-subordination relationships in infancy can affect subsequent agonistic potential during adult life, to our knowledge no explicit test has been made. Experiments have shown that adverse conditions during early development can have long-term effects on a variety of traits ranging from growth to competitive behaviour. In many vertebrate species, the main social setting in which the infant develops is a sibling group where competition is often mediated by a dominance hierarchy. Here, we show in a long-lived marine bird that subordination to an aggressive sibling throughout infancy does not compromise aggressiveness years later during adult life. Former junior and senior chicks of the blue-footed booby, whose typical brood of two chicks exhibits a consistent dominance-subordination relationship with strong 'trained winner' and 'trained loser' conditioning effects, did not differ in their aggressiveness while defending their nest against a conspecific intruder stimulus. Our results suggest that aggressive subordination and associated food deprivation, poor growth and elevated stress hormone during infancy do not prejudice aggressiveness of adult boobies during at least the first 13 years of life. Development of important traits such as aggressive tendencies may be buffered against the normal and predictable challenges of infancy.

Effects of recruiting age on senescence, lifespan and lifetime reproductive success in a long-lived seabird.

Theories of ageing predict that early reproduction should be associated with accelerated reproductive senescence and reduced longevity. Here, the influence of age of first reproduction on reproductive senescence and lifespan, and consequences for lifetime reproductive success (LRS), were examined using longitudinal reproductive records of male and female blue-footed boobies (Sula nebouxii) from two cohorts (1989 and 1991). The two sexes showed different relationships between age of first reproduction and rate of senescent decline: the earlier males recruited, the faster they experienced senescence in brood size and breeding success, whereas in females, recruiting age was unrelated to age-specific patterns of reproductive performance. Effects of recruiting age on lifespan, number of reproductive events and LRS were cohort- and/or sex-specific. Late-recruiting males of the 1989 cohort lived longer but performed as well over the lifetime as early recruits, suggesting the existence of a trade-off between early recruitment and long lifespan. In males of the 1991 cohort and females of both cohorts, recruiting age was apparently unrelated to lifespan, but early recruits reproduced more frequently and fledged more chicks over their lifetime than late recruits. Male boobies may be more likely than females to incur long-term costs of early reproduction, such as early reproductive senescence and diminished lifespan, because they probably invest more heavily than females. In the 1991 cohort, which faced the severe environmental challenge of an El Niño event in the first year of life, life-history trade-offs of males may have been masked by effects of individual quality.

Telomere lengths correlate with fitness but assortative mating by telomeres confers no benefit to fledgling recruitment.

Assortative mating by telomere lengths has been observed in several bird species, and in some cases may increase fitness of individuals. Here we examined the relationship between telomere lengths of Blue-footed Booby (Sula nebouxii) mates, long-lived colonial seabirds with high annual divorce rates. We tested the hypothesis that interactions between maternal and paternal telomere lengths affect offspring and parental survival. We found that relative telomere lengths (RTL) were strongly positively correlated between members of a breeding pair. In addition, RTL of both parents interacted to predict fledgling recruitment, although fledglings with two very long-RTL parents performed only averagely. Telomere lengths also predicted adult survival: birds with long telomeres were more likely to survive, but birds whose mate had long telomeres were less likely to survive. Thus, having long telomeres benefits survival, while choosing a mate with long telomeres benefits reproductive output while penalizing survival. These patterns demonstrate that while a breeder's RTL predicts offspring quality, assortative mating by RTL does not enhance fitness, and a trade-off between different components of fitness may govern patterns of assortative mating by telomere length. They also illustrate how testing the adaptive value of only one parent's telomere length on either survival or reproductive success alone may provide equivocal results.

Senescence of maternal effects: aging influences egg quality and rearing capacities of a long-lived bird.

Senescence could depress prenatal and postnatal capacities of mothers to invest in offspring. Longitudinal observations on the blue-footed booby (Sula nebouxii) revealed a quadratic effect of female age on fledgling production and cohort differences in rate of reproductive decline. By swapping clutches between females of different ages, we tested whether reproductive senescence is due to decline in egg quality or capacity to care. As laying mothers aged, egg size, ulna length of 5-day-old chicks, and ulna growth of second chicks up to age 30 days declined, and as rearing mothers aged, ulna growth and cellular mediated immune response of second chicks diminished. Oddly, senescent females (>11 years) produced more fledglings when rearing offspring of middle-aged females (8-11 years) than when rearing offspring of senescent or young females. Thus, senescence reduced egg quality and rearing capacities, and reproductive success of senescent mothers depended on prenatal effects associated with the age of the laying mother. Reproductive senescence of boobies may involve constraints on resources allocated to reproduction as well as adaptive adjustment of provision and care according to offspring value, implying that negative effects of senescence on offspring survival can be ameliorated by plasticity in postlaying or postnatal care.

Climatic influence on demographic parameters of a tropical seabird varies with age and sex.

In marine ecosystems climatic fluctuation and other physical variables greatly influence population dynamics, but differential effects of physical variables on the demographic parameters of the two sexes and different age classes are largely unexplored. We analyzed the effects of climate on the survival and recruitment of both sexes and several age classes of a long-lived tropical seabird, the Blue-footed Booby (Sula nebouxii), using long-term observations on marked individuals. Results demonstrated a complex interaction between yearly fluctuations in climate (both local and global indexes, during both winter and breeding season) and the sex and age of individuals. Youngest birds' survival and recruitment were commonly affected by local climate, whereas oldest birds' parameters tended to be constant and less influenced by environmental variables. These results confirm the theoretical prediction that sex- and age-related variation in life-history demographic traits is greater under poor environmental conditions, and they highlight the importance of including variability in fitness components in demographic and evolutionary models. Males and females showed similar variation in survival but different recruitment patterns, in relation to both age and the spatial scale of climatic influence (local or global). Results indicate different life-history tactics for each sex and different ages, with birds likely trying to maximize their fitness by responding to the environmental contingencies of each year.

Senescing sexual ornaments recover after a sabbatical.

Somatic deterioration in ageing animals may arise from allocation of resources to reproduction at the expense of repair and maintenance. Thus, accumulated reproductive effort is likely to progressively limit the expression of sexual ornaments at older ages. We analysed the effect of age and reproductive effort on the sexual attractiveness (foot colour) of male blue-footed boobies. Using a long-term dataset, we found that, as animals age and accumulate reproductive events, the expression of foot colour deteriorates. In addition, after non-breeding events males displayed more colourful feet compared with males that reproduced the year before, suggesting that sabbatical years facilitate recovery. Our results indirectly support the idea that allocation of resources to reproduction limits sexual attractiveness and that animals could cope with the negative effects of senescence on sexual ornaments by skipping some breeding events.

Congenital feeding response to a novel prey in a Mexican gartersnake.

In this study, we explored chemosensory, ingestive and prey-catching responses of neonate Mexican Black-bellied Gartersnakes (Thamnophis melanogaster) to crayfish (Cambarellus montezumae). By comparing snakes from a recently discovered crayfish-eating population and a typical non-crayfish-eating population, we asked which behavioral components change as a species enlarges its feeding niche. In the crayfish-eating population chemosensory responsiveness to crayfish was not enhanced but its heritability was higher. Neonates of both populations showed similar preference for freshly-molted versus unmolted crayfish, and whereas the tendency to ingest both crayfish stages remained stable between ages 15 and 90 days in the non-crayfish-eating population, in the crayfish-eating population it actually decreased. Techniques to catch and manipulate molted crayfish were similar in the two populations. We discuss the possibility that there is no increase in the behavioral response to eat crayfish by the neonates of the crayfish-eating populations, possibly due to the absence of ecological and spatial isolation between the two T. melanogaster populations. The crayfish ingestion in some population of T. melanogaster can be explained by environmental differences between populations, or by recent origin of crayfish ingestion in T. melanogaster.

Simultaneous positive and negative density-dependent dispersal in a colonial bird species.

Contradictory patterns of density-dependent animal dispersal can potentially be reconciled by integrating the conspecific attraction hypothesis with the traditional competition hypothesis. We propose a hypothesis that predicts a U-shaped relationship between density and both natal and breeding dispersal distance. Using 10 years of observations on a breeding colony of the Blue-footed Booby (Sula nebouxii), the hypothesis was confirmed by documenting simultaneous positive and negative density-dependent dispersal distances in natal and breeding dispersal of males and breeding dispersal of females within the colony. Point-pattern analyses demonstrated that the breeding sites of Blue-footed Boobies were highly aggregated in all years within a large study area, and aggregation presumably resulted in heterogeneity in patch density throughout the colony. As predicted, at moderate to high densities, dispersal distances showed positive density dependence, with individuals moving to lower density patches. In contrast, at low to moderate densities, dispersal distances showed negative density dependence, with individuals moving to higher density patches. In both sexes of the 1994 cohort, the higher the mean density in patches used by an individual over the long term (up to age 11 years), the fewer fledglings it produced. A positive effect of density on long-term reproductive success was not detected, possibly because birds that failed during pair formation or incubation were not sampled. Density of conspecifics may be an important influence on habitat selection of breeders, and dispersal may tend to carry individuals to patches where pair formation opportunities are better and negative effects of competition on reproductive success are reduced.

Experiencing El Niño conditions during early life reduces recruiting probabilities but not adult survival.

In wild long-lived animals, analysis of impacts of stressful natal conditions on adult performance has rarely embraced the entire age span, and the possibility that costs are expressed late in life has seldom been examined. Using 26 years of data from 8541 fledglings and 1310 adults of the blue-footed booby (Sula nebouxii), a marine bird that can live up to 23 years, we tested whether experiencing the warm waters and food scarcity associated with El Niño in the natal year reduces recruitment or survival over the adult lifetime. Warm water in the natal year reduced the probability of recruiting; each additional degree (°C) of water temperature meant a reduction of roughly 50% in fledglings' probability of returning to the natal colony as breeders. Warm water in the current year impacted adult survival, with greater effect at the oldest ages than during early adulthood. However, warm water in the natal year did not affect survival at any age over the adult lifespan. A previous study showed that early recruitment and widely spaced breeding allow boobies that experience warm waters in the natal year to achieve normal fledgling production over the first 10 years; our results now show that this reproductive effort incurs no survival penalty, not even late in life. This pattern is additional evidence of buffering against stressful natal conditions via life-history adjustments.

Why do some siblings attack each other? Comparative analysis of aggression in avian broods.

In many parentally fed species, siblings compete for food not only by begging and scrambling, but also by violently attacking each other. This aggressive competition has mostly been studied in birds, where it is often combined with dominance subordination, aggressive intimidation, and siblicide. Previous experimental and theoretical studies proposed several life-history, morphological, and behavioral variables that may facilitate the evolution of broodmate aggression, and explain its taxonomic distribution. Here we apply phylogenetic comparative analyses for the first time to test the influence of five hypothesized facilitators of the evolution of broodmate aggression, analyzing 69 species in seven avian families using two quantitative measures of aggression: incidence and intensity. We show that incidence and intensity of aggression increase with long nestling periods and indirect feeding, and small brood size is associated with intense aggression. Large food parcels were not correlated with either the incidence or intensity of aggression. Our study suggests that indirect feeding, long nestling periods, and small broods, possibly in combination with other factors, have tended to favor the evolution of aggressive broodmate competition.