Blue-footed Booby Research Articles

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.

Extrapair offspring of the blue-footed booby show no sign of higher fitness in the first 10 years of life

Extrapair offspring of the blue-footed booby show no sign of higher fitness in the first 10 years of life

Long-term effects of sex-specific sibling interaction on the development of blue-footed boobies

Long-term effects of sex-specific sibling interaction on the development of blue-footed boobies

Nutritional state variations in a tropical seabird throughout its breeding season

Individual body condition is frequently used to explain differences in foraging and breeding ecology in seabirds. However, little is known about the covariations of body mass with the nutritional state of animals as measured through plasma metabolites and how these different measures vary between and within individuals during breeding. Here, we assessed intra-individual variations of plasma metabolites (triglycerides, cholesterol, protein, and ß-hydroxybutyrate concentrations) and in body mass of Blue-footed boobies (Sula nebouxii) throughout their breeding season 2011–2012 in Isla El Rancho, Mexico. We found breeding-stage and sex-specific variations in individuals’ plasma metabolite concentrations, but these did not mirror variations in body mass. Before egg-laying, females had higher triglycerides, cholesterol, and protein concentrations than males. In contrast, males used their nutritional reserves (higher ß-hydroxybutyrate concentrations) more than females during the breeding season (except for early chick-rearing). At the individual level, males gained weight during the breeding season, whereas females lost weight. We also found that between-individual differences in plasma metabolite concentrations and changes in body mass were not consistent throughout the breeding season, while individual body mass was significantly repeatable. This study contributes to a better understanding of seabird breeding ecology and physiology by showing that sex-specific breeding roles might highly influence the nutritional state. Similar patterns might occur in other seabird species, helping to explain why we can find stage- and sex-specific foraging behaviors even in monomorphic species.

Information on forage fish ages from otoliths collected in avian stomach contents

Otolith analysis allows studying multiple aspects of fish biology, including age estimation; however, otoliths collected from avian stomach content have not been used to estimate the age of ingested fish. We evaluated the potential ability to estimate the age of Pacific sardine (Sardinops sagax) from otoliths collected from blue-footed booby (Sula nebouxii) stomach contents sampled in the Galapagos Islands. Blue-footed boobies were selected because they mostly forage close to their colony (<100 m) and were, therefore, more likely to have almost intact otoliths. To estimate age, we employed three previously developed methods for otoliths. We then related these estimates to the fish's standard length and compared these relations statistically using the Akaike Information Criterion (AIC) to determine which method was most parsimonious. We collected 32 otoliths in relatively good condition, of which we aged 31 with the surface-reading method, 26 with the otolith weight method, and 29 with the posterior otolith length method. Average ages obtained with the otolith methods were 5.6 ± 1.7 yr (± standard deviation), 5.7 ± 2.0 yr, and 3.9 ± 1.5 yr, respectively. Estimates obtained with the otolith weight method had the highest correlation with standard length and the lowest AIC values of the three suggesting it was the best method for aging. Our results indicate that aging otoliths extracted from bird stomachs are possible; however, their use depends on the availability of previously developed methods and how digested the fish are when the birds return to the colony.

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 70days 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.

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.

How removal of cats and rats from an island allowed a native predator to threaten a native bird

The question of how to program the removal of two invasive mammals, typically cats and rats, from a marine island without increasing risk to native prey species has received two general answers based on ecological theory: removal of cats must be accompanied by control of their mesopredator prey, and risk is minimized by removing both invaders simultaneously. Nonetheless, a 31-year study showed that in a 82-ha tropical marine bird sanctuary, predation on a native prey, the blue-footed booby, by a native predator, the Atlantic Central American milk snake, apparently diminished after removal of cats then increased 11-fold after the additional removal of black rats. These novel effects are explained in terms of a hypothetical three-link trophic web in which cat removal released rats to increasingly compete with or prey on the snakes that feed on hatchling boobies, and subsequent rat removal released snakes from all remaining predation. The upshot is a disturbing scenario in which approximately 200 milk snakes currently aggregate annually in roughly 1 hectare of booby colony and predate roughly forty percent of the hatchlings. Where the lowest link of an insular trophic web is a native mesopredator that feeds on native prey, the predictions of the classic mesopredator release scenario can be inverted, and removal of invasive mammals may endanger native prey species.

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.

Temporal and sex-based variation in organochlorine pesticide levels in the blue-footed booby in two coastal colonies of Sinaloa, Mexico

The temporal, inter-site, and sex-based variation of 19 organochlorine pesticides (OCPs) in blood plasma samples collected from blue-footed boobies of two islands in Sinaloa, Mexico, was evaluated. The effect of OCPs was evaluated with the heterophil/lymphocyte ratio, micronucleated erythrocyte frequency, and scaled mass index. The OCP-group levels decreased as the breeding season progressed, and interannual (but not inter-colony) differences were detected. Intra-annual variation in OCP levels seemed to reflect run-off inputs, although other environmental processes may better explain the variation between years. Sex-based differences in OCP levels were likely related to ecological and physiological processes linked to breeding (e.g., egg-laying and use of lipid reserves). No correlations between OCP-group levels and biomarkers were detected. Small pelagic fishes are the main prey sources of blue-footed boobies and the targets of regional industrial fisheries, and thus blue-footed booby OCP levels could reflect ecosystem health and indicate potential risks for human consumers.

The curious case of the blue‐footed booby nest

The curious case of the blue‐footed booby nest

Zinc concentrations in Blue-footed booby (Sula nebouxii) eggs, nestlings, and adults

Zinc is essential for animal metabolism, but the variation in Zn concentrations within seabird populations has been seldom explored. We collected Blue-footed booby (Sula nebouxii) eggs during 2012 and 2013 and blood samples from nestlings and adults during 2011 and 2012 in Sinaloa, Mexico, to evaluate differences in Zn concentrations among years, ages, sexes, and breeding stages. Zinc concentrations in eggs ranged between 27.3 and 64.9 ppm (dry weight), whereas Zn levels in the blood of nestlings and adults ranged between 16.1 and 53.1 ppm (dry weight). Egg Zn concentrations did not differ due to developmental stage, although Zn concentrations were significantly higher in 2013 than in 2012. Nestling Zn concentrations differed between years and decreased gradually with age. Chicks had significantly higher Zn concentrations than those of adults. Once nestlings stopped growing, females presented higher Zn concentrations than males. Adult Zn concentrations were higher during the pre-laying period than during the other breeding stages. Our results suggest that growth, sex, and breeding stage affect blood Zn concentrations, which may be due to stage-specific requirements. When compared with those of other seabird species, the Zn concentrations reported here are intermediate, and we did not detect adverse effects on either nestlings or adults.

Mate selection based on labile traits affects short-term fitness in a long-lived seabird.

In long-lived monogamous social species, partner compatibility can play a crucial role in reproductive success. We evaluated assortative mating based on body condition (plasma triglyceride concentration), diet (δ15N), and foraging habitat (δ13C) in the blue-footed booby Sula nebouxii, a long-lived monogamous seabird. We investigated the effects of assortative mating (sum of triglycerides in a pair) and asymmetry within pairs (residuals from regression of female-male triglycerides) on reproductive performance and offspring growth (alkaline phosphatase, ALP). We found that strong assortative mating determined by body condition and diet seemed to be related to a signalling mechanism (nutritional state). This mating pattern had a substantial effect on the breeding parameters and influenced offspring ALP. Within-pair asymmetry did not influence any reproductive parameters, but the ALP of offspring was related to the within-pair relative female condition. Overall, our results indicate that individuals seek the best possible match to maximize their breeding investment and/or individuals are limited in their mate options by their current body condition, which has consequences for offspring fitness in the short term. Our findings show that assortative mating based on body condition produces notable variation in the joint condition of the pair, which determines their breeding success.

Ectoparasite burden of Blue‐footed Booby chicks depends on combined parental ages

The probability of Blue‐footed Booby Sula nebouxii fledglings becoming reproductive adults is maximal when one parent is old and the other young, and minimal when both are old or young. No mechanism has been identified to explain this pattern, but here we showed that nestlings with different‐aged parents are the least infested with ticks. This result constitutes preliminary confirmation of the hypothesis that the effect of combined parental ages on probability of recruitment is mediated by offspring immunocompetence. The contribution of immunocompetence and parental care to these parental age effects needs to be unravelled.

Correction: High quality diet improves lipid metabolic profile and breeding performance in the blue-footed booby, a long-lived seabird.

[This corrects the article DOI: 10.1371/journal.pone.0193136.].

High quality diet improves lipid metabolic profile and breeding performance in the blue-footed booby, a long-lived seabird.

Understanding the role of diet in the physiological condition of adults during reproduction and hence its effect on reproductive performance is fundamental to understand reproductive strategies in long-lived animals. In birds, little is known about the influence of the quality of food consumed at the beginning of the reproductive period and its short-term effects on reproductive performance. To assess the role of diet in the physiological condition of female blue-footed booby, Sula nebouxii (BFBO), during reproduction we evaluated whether individual differences in diet (assessed by using δ13C and δ15N values of whole blood from female birds and muscle tissue of the principal prey species) prior to egg laying and during incubation influenced their lipid metabolic profile (measured as triglyceride levels and C:N ratio) and their reproductive performance (defined by laying date, clutch size and hatching success). Females with higher δ15N values in their blood during the courtship and incubation periods had a higher lipid metabolic profile, earlier laying date, greater clutch size (2–3 eggs) and higher hatching success. Females that laid earlier and more eggs (2–3 eggs) consumed more Pacific anchoveta (Cetengraulis mysticetus) and Pacific thread herring (Opisthonema libertate) than did other females. These two prey species also had high amounts of lipids (C:N ratio) and caloric content (Kcal/g fresh weight). The quality of food consumed by females at the beginning of reproduction affected their physiological condition, as well as their short-term reproductive performance. Our work emphasizes the importance of determining the influence of food quality during reproduction to understand the reproductive decisions and consequences in long-lived animals.

Sula nabouxii in the Anthropocene

Sula, Norse for gannet. Blue-footed Booby, taken for a fool. Type specimens congregate in the online videos, safe in the coo and cuteness of their mating dance, slow-motion cloggers, flex-footed two-step, Charlie Chaplin in a feathered suit. I watched them once in real life, forgetting my seaweed-snarl of first-world failures, the pale paltriness of me. S. nabouxii patient on volcanic headlands, waiting for the colder waters while the planet warms.

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.

Ecomorphology and foraging behaviour of Pacific boobies

Wing size and shape, expressed as wing loading and aspect ratio respectively, together with bill morphology are parameters that can reveal differences related to the foraging ecology of seabirds. Six species of booby (Sulidae) that inhabit the Pacific are the focus of this study: four mainly pelagic species, Masked Booby Sula dactylatra, Nazca Booby Sula granti, Red‐footed Booby Sula sula and Brown Booby Sula leucogaster, and two coastal species, Blue‐footed Booby Sula nebouxii and Peruvian Booby Sula variegata. Pelagic boobies showed segregation among species in body mass and relative bill size, and they differed in wing morphology (wing loading and aspect ratio) from the coastal boobies. The coastal Peruvian and Blue‐footed Boobies are largely allopatric but overlap in northern Peru. In their area of sympatry, they showed evidence of character displacement in body size and in wing and bill morphology, which suggests that competition plays an important role in sympatry. This study improves our understanding of ecological interactions among Pacific boobies and of how selective pressures have shaped their ecomorphology and foraging behaviours.

Age-related parental care in a long-lived bird: implications for offspring development

In long-lived species, behaviour is expected to vary across the lifespan, first improving with maturation and experience and then declining with senescence, but measurement is rare, particularly during old age. Measuring nest defence intensity in 255 known-age blue-footed boobies (Sula nebouxii) of 19 age classes confirmed the inverted-U pattern: intensity of nest defence increased in young males and females until roughly 11–12 years and declined progressively afterwards. We discuss the processes that may generate this distinctive pattern. Regardless of the underlying processes, this study establishes the existence of age-related variation in parental care in a long-lived species. Natural variation in natal conditions has recently been shown to have long-term impacts on development, so this study raises the question whether age-related changes in parental care generate systematic variation in offspring phenotypes. In theory, age-related change in parental care can result in differences among offspring produced at different ages. However, parental behaviour has never been measured over the whole age-span of any long-lived species because of the difficulty of sampling very old animals in the field. We measured intensity of nest defence over the age-span and confirmed that blue-footed boobies exhibit an age-related quadratic pattern in this parental behaviour: defence intensity increases in early life and declines progressively afterwards. Our results imply that similar-shaped patterns may exist in other components of parental care, such as feeding and social interaction, potentially affecting the long-term development of offspring.