Sula Granti Research Articles

Prevalence of Toxoplasma gondii in Galapagos birds: Inference of risk factors associated with diet.

Toxoplasma gondii is a zoonotic intracellular parasite of particular concern in the conservation of wildlife due to its ability to infect all homeotherms and potentially cause acute fatal disease in naive species. In the Galapagos (Ecuador), an archipelago composed of more than a hundred islets and islands, the presence of T. gondii can be attributed to human-introduced domestic cats, but little is known about its transmission in wildlife populations. We compared the prevalence of antibodies against T. gondii in sympatric Galapagos wild bird species that differ in diet and contact with oocyst-contaminated soil to determine the relative importance of trophic habits as an exposure factor. Plasma samples were obtained from 163 land birds inhabiting Santa Cruz, one of the cat-inhabited islands, and from 187 seabirds breeding in cat-free surrounding islands (Daphne Major, North Seymour, and South Plaza). These samples were tested for the presence of T. gondii antibodies using the modified agglutination test (MAT ≥ 1:10). All seven species of land birds and 4/6 species of seabirds presented seropositive results. All great frigatebirds (Fregata minor) (N = 25) and swallow-tailed gulls (Creagrus furcatus) (N = 23) were seronegative. Prevalence ranged from 13% in Nazca boobies (Sula granti) to 100% in Galapagos mockingbirds (Mimus parvulus). It decreased from occasional carnivores (63.43%) to granivores-insectivores (26.22%), and strict piscivores (14.62%). These results indicate that the consumption of tissue cysts poses the highest risk of exposure to T. gondii for Galapagos birds, followed by the ingestion of plants and insects contaminated by oocysts as important transmission pathways.

Circulating corticosterone predicts near-term, while H/L ratio predicts long-term, survival in a long-lived seabird

Assessing stress in wild populations is important in many ecological and conservation contexts because the physiological responses of individuals to stressors can be used to identify at-risk populations and the ability to respond appropriately to stressors is related to individual quality and fitness. Yet, one of the great challenges in ecophysiology is linking physiological measures in wild animal populations with changes in individual fitness. Here, we examined two indices of stress, namely, circulating baseline corticosterone concentration ([Cort]) and the heterophil:lymphocyte (H/L) ratio, in a long-lived seabird, the Nazca booby (Sula granti) and their relationship with current individual state and subsequent survival and residual and lifetime reproductive success. [Cort] was related to sex, age, and current reproductive effort in in that males, older birds, and birds currently engaged in a breeding attempt birds had higher [Cort]. [Cort] was negatively associated with survival to the next breeding season. The H/L ratio was not associated with the current state of birds but predicted cohort-specific long-term survival. Lifespan and reproductive performance are correlated in Nazca boobies; therefore, our results suggest that the H/L ratio may be useful as an indicator of overall fitness, while [Cort] can be used to predict current or near-term fitness in this species. We further propose the H/L [or neutrophil/lymphocyte (N/L)] Ratio-Fitness Hypothesis, which posits that this ratio is repeatable within individuals and are negatively associated with fitness. This hypothesis needs to be tested in Nazca boobies and other species, and when supported by empirical evidence, then these ratios could be a powerful monitoring tool for assessing population health or identifying at-risk populations.

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.

Terrestrial food web of the Malpelo Fauna and Flora Sanctuary, Colombia: An analysis from a topological approach

Malpelo Island is the largest marine protected area (MPA) in the Colombian Pacific; however, the lack of information regarding its ecological dynamics suggests that management and conservation strategies are developed from an individual approach (species or groups of species) and not from an ecosystem one. This study analyzes the terrestrial food web of Malpelo Island, Colombia, based on topological analysis (e.g., centrality). The food web was constructed from 27 nodes representing the main trophogroups, which consist of species or functional groups. Malpelo Island had a food web of four steps with a maximum separation among all trophogroups and trophic pathways, with two steps in average length. Furthermore, the food web was divided into three food web compartments, with a recurrence of connectivity patterns dominated by apparent and exploitative competition, followed by tri-trophic chains and omnivory. Five key trophogroups control the energy flow throughout the food web (detritus, the land crab Johngarthia malpilensis, the lizard Anolis agassizi, the Malpelo dotted galliwasp Diploglossus millepunctatus, and the Nazca booby Sula granti). The high importance of detritus suggests that bottom-up processes act as a control and regulation mechanism of trophic flows. The low number of food web compartments and a high recurrence of specific connectivity patterns in the Malpelo Island terrestrial ecosystem evidence different ecological processes centered on five trophogroups, allowing stability against disturbances. In addition, the simulation of trophogroup removal (randomly or directed) suggests that food web can be vulnerable to structural alterations in their properties, which may have consequences on the resilience of this ecosystem. This study contributes to the knowledge of the trophic dynamics of Malpelo Island, providing a potential tool for management and conservation measures from an ecosystemic approach.

Trophic connectivity between the terrestrial and marine ecosystems of Malpelo Island, Colombia, evaluated through stable isotope analysis

The trophic dynamics of islands with low terrestrial primary productivity often depend on marine allochthonous inputs from nearby donor habitats. For instance, on Malpelo Island, Colombia (4° 00′ 05.63″ N; 81° 36′ 36.41″ W), the Nazca booby Sula granti affects the productivity and trophic dynamics of the terrestrial ecosystem by delivering nutrients, primary in the form guano, chick carcasses, and eggs. This study evaluated the trophic connectivity between the terrestrial and marine ecosystems of Malpelo Island, Colombia based on the isotopic (δ13C and δ15N) assessment of 403 samples (107 terrestrial and 296 marine) collected between 2017 and 2021. Isospaces were estimated based on δ13C and δ15N values, contribution of terrestrial sources in consumer diets (mixing model), 15 N enrichment in C3 plants, and interactions among environments (overlap). δ13C and δ15N values showed a larger terrestrial isospace (134.7‰2) than the marine isospace (117.2‰2). The mixing model indicated that detritusTerrestrial (median: 30.2%) contributed more to the food web than C3 plants (0.2%), reflecting high δ13CMarine content. The high isotopic overlap (> 60%) between terrestrial and marine isospaces suggests a significant trophic connection between environments. These results show the role of the marine ecosystem on the terrestrial ecosystem and the importance of S. granti regarding nutrient transfer between environments. The conservation of this seabird is essential to maintain the balance of this insular ecosystem. Using stable isotopes, this study was able to reveal trophic relationships between ecosystems associated with small oceanic islands that host large seabird colonies but have low primary productivity.

Sex-specific aging in bite force in a wild vertebrate.

The manifold differences between the sexes provide wide scope for sex differences in senescence. However, detecting physiological decline in old age and evaluating any sex difference in aging in a wild population can be challenging. This applies especially to long-lived species that require marking around birth in order to recognize elderly individuals, perhaps decades later. Here, we used bite force of known-age, long-lived Nazca boobies (Sula granti, a seabird) as a functional measure of muscle strength; surprisingly, only a single study has evaluated the possibility of senescent decline in muscle strength in a wild vertebrate. The male-biased adult sex ratio of this population constrains breeding opportunities across the lifespan for males, so we predicted that slower accumulation of reproductive costs would delay senescent decline in bite force in males compared to females, matching observed patterns in some non-muscle traits in this species. Data were collected from 349 adults using a force transducer at the start of the breeding season in November 2017 on Isla Española, Galápagos. Both sexes achieved less bite force in late life. The decline began at a later age in males, providing evidence of sex-specific schedules of decline in muscle function in a wild vertebrate.

First Specimen of the Nazca Booby (Sula granti) for the State of Baja California, Mexico

First Specimen of the Nazca Booby (Sula granti) for the State of Baja California, Mexico

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.

HEALTH STATUS OF NAZCA BOOBIES (SULA GRANTI) ON DAPHNE MAJOR ISLAND IN THE GALÁPAGOS DETERMINED BY HEMATOLOGY, BIOCHEMISTRY, AND PHYSICAL EXAMINATION.

Island species are particularly vulnerable to environmental disturbances and introduced pathogens. Conducting health assessments of wild populations in the Galápagos improves the ability of wildlife managers and veterinarians to detect deteriorations in health status. Seabirds in particular are useful species to monitor due to their colonial breeding and wide migration range. Nazca boobies (Sula granti) in a breeding colony at Daphne Major (n = 30) were given physical examinations, and blood samples were collected for hematology and biochemistry using an iSTAT Portable Clinical Analyzer. Female boobies had longer wing length than males, as well as lower blood urea nitrogen, creatinine, and white blood cell counts. This could be attributed to sexual dimorphism or differences in foraging and mating strategies between the sexes. The time between capture and blood collection had a significant inverse relationship on plasma sodium, potassium, hemoglobin, anion gaps, and lymphocyte counts, suggesting that blood sampling in Nazca boobies should be done in less than 5 m to avoid the impacts of stress on hematological parameters. This is the first health assessment on the breeding colony of Nazca boobies at Daphne Major, and the results can inform future monitoring in this species as well as other sulids.

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.

Molt, Age, and Identification of the Masked and Nazca Boobies in California

Molt, Age, and Identification of the Masked and Nazca Boobies in California

Senescence in nature: New insights from a long-term seabird study.

In Focus: Tompkins, E. M., & Anderson, D. J. (2019). Sex-specific patterns of senescencein Nazca boobies linked to mating system. Journal of Animal Ecology, 88, 986-1000. https://doi.org/10.1111/1365-2656.12944. Sex-specific differences in senescence and environmental impacts on senescence in both sexes remain poorly understood. Tompkins and Anderson (2019) studied senescence in survival (hereafter called actuarial senescence) and in reproduction (hereafter called reproductive senescence) in Nazca boobies using 33years of individual-based capture-recapture data. Senescence patterns (life-history traits, ages at onset, senescence rates) differed between sexes and were affected by environmental conditions (food availability) faced by individuals during their younger ages. Patterns of sex differences in senescence may result from the mating dynamics due to the population's male-biased sex ratio.

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.

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.

Early-life maltreatment predicts adult stress response in a long-lived wild bird.

Persistent phenotypic changes due to early-life stressors are widely acknowledged, but their relevance for wild, free-living animals is poorly understood. We evaluated effects of two natural stressors experienced when young (maltreatment by adults and nutritional stress) on stress physiology in wild Nazca boobies (Sula granti) 6-8 years later, an exceptionally long interval for such studies. Maltreatment as a nestling, but not nutritional stress, was associated years later with depressed baseline corticosterone in females and elevated stress-induced corticosterone concentration [CORT] in males. These results provide rare evidence of long-term hormonal effects of natural early-life stress, which may be adaptive mechanisms for dealing with future stressors.

SERUM CHEMISTRY OF FREE-RANGING NAZCA BOOBIES ( SULA GRANTI).

This study reports body mass and serum chemistry reference values of 121 male and 57 female Nazca boobies (Sulidae: Sula granti) from a colony on Isla Española, Galápagos Islands, Ecuador. Circulating aspartate aminotransferase, creatine kinase, lactate dehydrogenase, total protein, immunoglobulin Y, uric acid, blood urea nitrogen, triglycerides, cholesterol, and creatinine were quantified and analyzed by sex. Sex explained little variance in all examined variables except mass; females were heavier than males, as expected for sulids. Uric acid values had a bimodal distribution, likely reflecting differences in recent foraging success. Aspartate aminotransferase and creatine kinase values were similar to those reported in other sulids. Clinical health reference values are critical for practitioners investigating responses of seabirds to oil spills, coastal restoration efforts, or emerging diseases. These data from a species living in a relatively isolated and pristine area provide a valuable baseline for future health evaluations.

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.

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.

MODEL-BASED GEOMORPHOLOGY OF MALPELO ISLAND AND SPATIAL DISTRIBUTION OF BREEDING SEABIRDS

The spatial distribution of seabird nests present on Malpelo Island, the main characteristics of the islandʼs topography, and the types of substratum available for nesting were addressed using a Digital Elevation Model (DEM). The model is based on data from remote sensors (satellite images, aerial photography and panoramic photography), and from field data processed through a geographical information system. The nests of Sula granti prevail on the surfaces of Malpelo Island and neighboring islets, while those of the remaining species (S. sula, Creagrus furcatus, Anous stolidus, A. minutus and Gygis alba) are spatially restricted to the cliff margins and to crevices or caverns at different heights. The presence of terrestrial predators and predatory birds (Fregata spp.) seems to mainly explain the marginal distribution of other breeding species. The cartographic data presented here differ significantly from past and current representations, especially those concerning the islandʼs emerged surface and other geomorphologic features. This new cartographical information will support future studies on the terrestrial fauna and flora of Malpelo Island and its islets.

ECOLOGÍA TRÓFICA DEL PIQUERO DE NAZCA Sula granti (AVES: SULIDAE) EN LA ISLA MALPELO, COLOMBIA

The trophic ecology of Nazca Booby was evaluated through the analysis of gut contents collected between September 2004 and July 2005 during five field trips. From 110 induced regurgitation samples, the diet was analyzed using the variables number, weight and frequency of occurrence of the different nutritious categories, and using the distribution of the frequencies of sizes of preys at general, intraspecific and temporal levels. Oxyporrhamphus micropterus (halfbeaks fishes, family Hemiramphidae) and fishes of the family Exocoetidae (flying fishes) were the principal components found on the diet, followed by fishes of the families Carangidae and Escombridae. Variations were present in the consumption of the distinct categories at general, intraspecific and temporal levels, with the strongest differences in the consumption of preys of the family Hemiramphidae. The quantity of food taken by S. granti at Malpelo Island showed close relation with its reproductive cycle, and it adjusted to the model of energetic demand proposed for marine birds. Comparisons with other analogue studies showed slight differences between localities, apparently related with the availability of preys. It seems like there is a niche partition between females and males of S. granti at Malpelo Island related with the quantity and sizes of the preys ingested, and in a lesser degree with the composition of the diet. The present work is the first one to evaluate in detail the diet of the Nazca Booby and considerably extends the geographical range of this kind of studies in the Eastern Pacific.