Variations in inter-specific and sex-related niche partitioning in pelagic boobies during their annual cycle.

Animals that co-occur in a region (sympatry) may share the same environment (syntopy), and niche differentiation is expected among closely related species competing for resources. The masked booby (Sula dactylatra) and smaller congeneric red-footed booby (Sula sula) share breeding grounds. In addition to the inter-specific size difference, females of both species are also larger than the respective males (reversed sexual size dimorphism). Although both boobies consume similar prey, sometimes in mixed-species flocks, each species and sex may specialize in terms of their diet or foraging habitats. We examined inter- and intra-specific differences in isotopic values (δ13C and δ15N) in these pelagically feeding booby species during the incubation period at Clarion Island, Mexico, to quantify the degrees of inter- and intra-specific niche partitioning throughout the annual cycle. During incubation, both species preyed mainly on flyingfish and squid, but masked boobies had heavier food loads than red-footed boobies. There was no overlap in isotopic niches between masked and red-footed boobies during breeding (determined from whole blood), but there was slight overlap during the non-breeding period (determined from body feathers). Female masked boobies had a higher trophic position than conspecific males during breeding; however, no such pattern was detected in red-footed boobies. These results provide evidence of inter- and intra-specific niche partitioning in these tropical seabird species, particularly during the breeding period and in the more-dimorphic species. Our results suggest that these closely related species use different strategies to cope with the same tropical marine environment.

Micronuclei in embryos of eight seabird species in northwestern Mexico: A biomarker of exposure to coastal pollution?

The micronucleus (MN) test may be used to evaluate genome instability in birds and the potential of different species to function as biomarkers of genotoxicity. However, little is known regarding genome instability in seabird embryos or the instability present among embryonic development stages. Therefore, the present study aimed to describe the frequencies of micronucleated erythrocytes (MNE) and micronucleated polychromatic erythrocytes (MNPCE) in blood samples collected from the embryos of eight seabird species nesting on the coast of Sinaloa, Mexico. An additional description of blood cell maturation along with embryo development during incubation was conducted based on the proportion of polychromatic erythrocytes (PCE), and the potential relationships between metals (Hg and Cd concentrations in egg content) and the MN frequencies in embryo blood were evaluated. The PCE proportion appears to decline as incubation advances (initial stage > intermediate stage > advanced stage), and the values varied between species (Suliformes/Pelecaniformes < Charadriiformes: Laridae), which may be related to differences among incubation periods and reproductive strategies. Interspecific variation in the MNPCE frequency was found in embryos showing advanced development, which could be related to both variations in life-history traits and ecological factors and not Hg or Cd exposure. The genomic instability values in this study are the first to be reported for embryos of seabird species nesting in a subtropical coastal region.

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.

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.

Bioaccumulation of organochlorine pesticides in the Western Sandpiper (Calidris mauri) during the wintering season in Sinaloa, Mexico.

The Western Sandpiper, Calidris mauri, is one of the most abundant migratory shorebirds in the Western Hemisphere. Both Bahia Santa Maria (SM) and Ensenada Pabellones (EP) in Sinaloa, Mexico, are critical wintering sites for this species. We described the presence and concentration of 16 organochlorine pesticides (OCPs) in Western Sandpiper muscle and liver tissues collected from SM and EP during the wintering (December-January) and premigration (March-April) periods of 2010 and 2011, respectively. The individual OCP concentrations varied from 0.003 to 0.127 µg/g dry weight (dw) and were lower than the established thresholds for either acute or chronic effects. Western Sandpipers in SM-Premigration had the highest frequency of OCPs (39.3%), followed by EP-Winter (32.1%) and SM-Winter (28.5%). The frequency of occurrence of all OCPs in the liver presented differences between sites during the wintering period as well as between the wintering and premigration periods in SM. As the primary organ responsible for pollutant detoxification, the liver may bioaccumulate these compounds. No clear trends were observed in muscle tissues or among age-sex groups. Our results showed evidence of OCP bioaccumulation in the Western Sandpiper during the wintering period, which may be related to hyperphagia during the premigration period and to the differential intake of OCP types and quantities between sites due to differences in their availability. However, these conclusions are based on relatively low sample sizes for some groups and require further study with non-pooled samples.

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.

O-hexyl O-2,5-dichlorophenyl phosphoramidate as a substrate for domestic and sea bird serum A-esterases: Hydrolysis levels, Cu2+- and Zn2+-dependence and stereoselectivity.

O-Hexyl O-2,5-dichlorophenyl phosphoramidate (HDCP) induces delayed neuropathy in hens. It has been used as a tool to identify new A-esterase activities in animal tissues. This study shows the EDTA-resistant, Cu2+- and Zn2+-dependent hydrolysis of racemic HDCP in domestic and sea bird serum using UV/Vis spectrophotometry and chiral chromatography. The results clearly show a significant (p ˂ 0.05) Cu2+- and Zn2+-dependent HDCP hydrolysis in the serum of all bird species versus EDTA, except for the Zn2+-dependent HDCPase activity from Yucatecan quail serum. The ratio of Cu2+/Zn2+ hydrolysis varied between 1 and 7 (intraspecies) and 15.6 (interspecies). EDTA affected the Cu2+- and Zn2+-dependent HDCPase activity in the range of 37-95% and 40-50%, respectively. HDCP hydrolysis activated by Cu2+ was significantly (p ˂ 0.05) stereoselective (R-(+)-HDCP ˃ S-(-)-HDCP) in chicken and sea bird serum. Its R-(+)-HDCP/S-(-)-HDCP ratios were 6.8 and 1.6-2.8, respectively. EDTA-resistant and zinc-dependent HDCP hydrolysis were not stereospecific in all bird sera tested. The present ex vivo study reinforces the idea that bird sera have HDCPase activity that is sensitive to divalent metals, resistant to EDTA and possibly associated with the protein albumin.

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.

Lead, cadmium and mercury in the blood of the blue-footed booby (Sula nebouxii) from the coast of Sinaloa, Gulf of California, Mexico.

We used blood samples of the Blue-footed Booby, considering sex (female and male) and age-class (adult and chick) of individuals at different breeding stages during two breeding seasons (2010-2011 and 2011-2012) in Isla El Rancho, Sinaloa, to determine lead, cadmium, and mercury concentrations. Lead and cadmium concentrations were below our detection limit (0.05 and 0.36ppm, respectively). A higher concentration of mercury was found in early stages of breeding, likely related to changes in mercury environmental availability. Mercury concentrations in adults did not relate with their breeding output. Males and adults had higher mercury concentration than females and chicks. We provide information of temporal, sex and age-related variations in the concentrations of mercury in blood of the Blue-footed Booby.

Distribución de aves acuáticas y rapaces en un embalse dulceacuÝcola artificial de Baja California Sur, México / Distribution of aquatic and raptor birds in a freshwater artificial pond of Baja California Sur, Mexico

We determined the taxonomic composition and spatial-temporal distribution of aquatic and raptor birds in a freshwater artificial pond of El Centenario, Baja California Sur, MÚxico, during 24 biweekly censuses (April, 1998 to March, 1999). The pond is particularly attractive for birds because of its variety of food items. A total 25,563 records of 69 species were done, among them the first report of Chlidonias niger and Phalaropus tricolor for the region. Species richness and abundance were determined for the migrant component, mostly Anatidae (16 species and 55.6 of the total abundance) and shorebirds (18 species and 13.3). The greater number of species and individuals was in C the deepest and more heterogeneous section of the pond. The most important species was Oxyura jamaicensis (30 of the total observed individuals), with highest abundance in the peninsula. The artificial pond presented an atypical and distinct ornithological composition because it is located in an arid region, and acts as a resting site for migrant birds. The site included species that usually live in freshwater and coastal areas, a characteristic reflected in their high richness. It contributes noticeably to the local avian biodiversity.