Hydrogen isotope ratios (δ2H) are widely used to study animal movement and food web energetics. However, unexplained, non-geographically derived δ2H variation can limit the accuracy and resolution of δ2H-based interpretations. We examined potential causes of δ2H variation–including age, body size, and amino acid (AA) factors–in a non-migratory Cocos booby (Sula brewsteri) colony around Islas Marietas, Mexico (20°41′N, 105°36′W) in 2016–2018. We also explored the applicability of novel AA δ2H data as high-resolution tracers for biosynthesis and food web dynamics in the marine realm. Among the 87 birds in our study, the δ2H values of plasma from chicks (< 45 days old) and feathers from juveniles (grown from 40–70 days old) both increased with age by > 25‰, and plasma δ2H correlated with body size in both chicks and adults. Proline δ2H values exhibited a striking range (over several hundred per mille), were the predominant AA driver of patterns in bulk plasma δ2H values (r2> 0.6 for chicks, > 0.8 for adults), and correlated with body size and chick age. Based on our dataset, we predict that Threonine δ2H values may indicate marine versus terrestrial resource use, Alanine δ2H values may reliably reflect environmental water, and Serine δ2H values may retain a marine basal food signal in carnivores. We suggest future studies carefully consider the influence of body size and age while interpreting δ2H datasets. Furthermore, we contend that AA δ2H data hold an untapped cache of ecological and physiological information that should be exploited to better understand δ2H propagation through food webs and refine the utility of this isotopic tool.

ABSTRACTForaging during breeding is a demanding activity linked to breeding investment and possibly constrained by individual quality. Telomere length, the protective nucleoproteins located at the ends of the chromosomes, is considered a trait reflecting somatic maintenance and individual quality. Therefore, foraging effort and parental investment may be positively related to telomere length, if individuals with longer telomeres are of better quality and thus able to maintain better body condition and allocate more resources to parental activities. In the brown booby (Sula leucogaster), we investigated if telomere length is related to body mass (a proxy of condition) and whether variation in foraging behavior and provisioning effort is related to telomere length or body mass. Then, we explored whether variation in foraging and provisioning influences the chick mass growth rate. In 34 pairs nesting in Isla de San Jorge, in the Gulf of California, México, we sampled their blood to estimate telomere length, measured their body mass, and for 10 days, recorded their foraging behavior via global positioning system (GPS) loggers and their chick provisioning rate and chicks' mass growth rate. We found a positive relationship between parents' body mass and telomere length. Body mass did not affect foraging behavior. Females with longer telomeres were more prone to travel longer distances toward offshore and deeper waters than females with shorter telomeres. In contrast, males with longer telomere lengths performed more nearshore foraging trips than males with shorter telomeres. The chick provisioning rate was unrelated to telomere length or body mass, but females fed the chick at a rate 2.4 times greater than males. Females' offshore foraging, but not males', was positively related to chick mass growth rate. Our results suggest that individual quality, indicated by telomere length, is an important driver of sex‐specific, between‐individual variation in foraging behavior, indirectly affecting offspring condition.

Carotenoid-dependent ornaments can reflect animals’ diet and foraging behaviors. However, this association should be spatially flexible and variable among populations to account for geographic variation in optimal foraging behaviors. We tested this hypothesis using populations of a marine predator (the brown booby, Sula leucogaster) that forage across a gradient in ocean depth in and near the Gulf of California. Specifically, we quantified green chroma for two skin traits (foot and gular color) and their relationship to foraging location and diet of males, as measured via global positioning system tracking and stable carbon isotope analysis of blood plasma. Our three focal colonies varied in which foraging attributes were linked to carotenoid-rich ornaments. For gular skin, our data showed a shift from a benthic prey-green skin association in the shallow waters in the north to a pelagic prey-green skin association in the deepest waters to the south. Mean foraging trip duration and distance of foraging site from coast also predicted skin coloration in some colonies. Finally, brown booby colonies varied in which trait (foot versus gular skin color) was associated with foraging metrics. Overall, our results indicate that male ornaments reflect quality of diet and foraging–information that may help females select mates who are adapted to local foraging conditions and therefore, are likely to provide better parental care. More broadly, our results stress that diet-dependent ornaments are closely linked to animals’ environments and that we cannot assume ornaments or ornament signal content are ubiquitous within species, even when ornaments appear similar among populations.

Stable isotope analyses of archival specimens have revealed trophic declines over the past 150 yr in a growing number of predatory pelagic seabirds that breed in the Hawaiian Islands. However, they have not examined whether isotopic shifts occurred primarily during a specific phase of the annual cycle, which could allow us to better identify the causes of trophic declines and potential consequences for affected populations. We evaluated seasonal (breeding versus nonbreeding season) foraging habits of 2 ecologically distinct species, Newell’s shearwater Puffinus newelli and Laysan albatross Phoebastria immutabilis, and extended this analysis back 50 and 100 yr, respectively. Our assessment relied on amino acid δ15N proxies for nutrient regime use (δ15NPhe) and trophic position (Δδ15NGlu-Phe) from 2 tissues (feather and bone collagen) reflecting different time scales. Both study species exhibited season-specific isotopic shifts resulting in more pronounced seasonality in modern populations. We also identified inter-species differences in nutrient regime use, regardless of season. Laysan albatross experienced a trophic decline exclusive to the breeding season, while their nonbreeding season foraging ecology has remained constant over the past century. In contrast, the nutrient regime at the base of the food chain for Newell’s shearwaters during the nonbreeding season underwent a shift within the last 50 yr, and the trophic decline they experienced was heavily weighted toward the nonbreeding season. Efforts to mitigate potential fitness consequences of future trophic declines might benefit from focusing on fisheries management near the Hawaiian Islands, where susceptible seabirds forage during winter/spring, rather than the entire North Pacific.

We investigated how foraging habits vary among three ecologically distinct wide-ranging seabirds. Using amino acid δ15N proxies for nutrient regime (δ15NPhe) and trophic position (Δδ15NGlu-Phe), we compared Newell’s shearwater (Puffinus newelli) and Laysan albatross (Phoebastria immutabilis) foraging habits over the past 50–100 years, respectively, to published records for the Hawaiian petrel (Pterodroma sandwichensis). Standard ellipses constructed from the isotope proxies show that inter-population and interspecific foraging segregation have persisted for several decades. We found no evidence of a shift in nutrient regime at the base of the food web for the three species. However, our data identify a trophic decline during the past century for Newell’s shearwater and Laysan albatross (probability ≥ 0.97), echoing a similar decline observed in the Hawaiian petrel. During this time, Newell’s shearwaters and Hawaiian petrels have experienced population declines and Laysan albatross has experienced range extension and apparent population stability. Counting other recent studies, a pattern of trophic decline over the past century has now been identified in eight species of pelagic seabirds that breed in the Hawaiian Islands. Because our study species forage broadly across the North Pacific Ocean and differ in morphological and behavioral traits and feeding methods, the identified trophic declines suggest a pervasive shift in food web architecture within the past century.

Quantifying individual specialization and other forms of intraspecific ecological diversity can reveal variation that is critical for evolutionary or behavioral adaption of a species to changing environments. Here, the isotopic niche and degree of individual foraging specialization were quantified for an endangered seabird, the Hawaiian petrel (Pterodroma sandwichensis), nesting on Lānaʻi (20°48′N, 156°52′W) and 72 km away on Haleakalā, Maui (20°42′N, 156°15′W; 20° 43′N, 156°14′W) between 2006 and 2011. Stable isotope values (δ13C and δ15N) from sequentially grown flight feathers provided time-series data that reflect the foraging habitat (relative latitude, nutrient regime of foraging location) and diet (trophic level) of individual birds across the period of molt. The two colonies differed in mean δ15N and δ13C throughout the period of molt, total nitrogen isotopic niche width, and extent of individual specialization with regard to δ15N. It is likely that petrels from Lānaʻi and Haleakalā use different feeding locations during the non-breeding season, when they are no longer tied to closely spaced breeding colonies. The loss of either colony could result in a substantial, long-term reduction in ecological diversity of the species (and perhaps, in adaptability). In contrast, comparisons of measured versus null specialization indices strongly suggest that both Lānaʻi and Haleakalā populations consist of individual generalists. Individual generalization with regard to foraging habitat and diet is here predicted to be common among tropical and subtropical oceanic seabirds. Such generalization could facilitate rapid, population-level responses of seabird species to marine environmental change via individual plasticity.

Isotope data from Hawaiian Petrel (Pterodroma sandwichensis) primaries P1 and P6 were compared to determine whether foraging habits change between the beginning and middle of the nonbreeding season. P6 data did not differ between samples derived from a longitudinal and a minimally invasive protocol and point samples taken from the feather bases. While P6 delta C-13 increased longitudinally, no delta N-15 longitudinal trends emerged, yet inter-individual delta N-15 variability was high. P6 delta C-13 data suggest that Hawaiian Petrels molt at low latitudes. Among colonies, all of which are located in the Hawaiian Islands, USA, low P6 delta N-15 values for Maui birds relative to Hawaii and Lanai birds reflect foraging segregation and differential utilization of N-15-enriched oceanic regions. For the Hawaiian Petrel, the isotopic similarity between P1 and P6 indicates that analogous ecological interpretations can be drawn from these feathers, and similar foraging habits persist from the beginning to middle of the nonbreeding season. Prolonged inter-colony foraging segregation may facilitate coexistence of colonies and, together with high intra-colony foraging diversity, may reduce extinction risk for the endangered Hawaiian Petrel.

Carotenoid-based ornaments are common signalling features in animals. It has long been proposed that such ornaments communicate information about foraging abilities to potential mates. However, evidence linking foraging with ornamentation is largely missing from unmanipulated, free-ranging populations. To investigate this relationship, we studied a coastal population of brown booby (Sula leucogaster brewsteri), a seabird with a carotenoid-based gular skin ornament. δ13C values from both feathers and blood plasma were negatively correlated with male gular colour, indicating birds that consumed more pelagic prey in offshore locations had more ornamented skin than those that fed on nearshore, benthic prey. This relationship was supported by our GPS tracking results, which revealed longer, more offshore foraging trips among highly ornamented males. Our data show that brown booby ornaments are honest indicators of foraging propensity; a link consistent with the rarity hypothesis and potentially driven by the concentration of carotenoids found in phytoplankton versus benthic algae. Carotenoid-based ornaments may reflect foraging tendencies in animals such as coastal predators that use food webs with distinct carotenoid profiles.

Stable isotope analysis has expanded the usefulness of avian specimen collections in ways that were generally unanticipated by the original collectors. This technique enables aspects of avian ecology to be studied using very small samples of feather or other tissue taken from specimens. Stable isotope values can be informative about diet, trophic ecology, spatial habitat use, and the migratory connectivity of breeding and nonbreeding populations. They can also provide access to understudied time periods in a bird's annual cycle, particularly periods of molt. Use of museum specimens offers advantages for these studies: museum collections generally span longer time periods than field samples and represent broad geographic ranges. In this chapter, we review established and emerging isotopic techniques and their applications in avian ecology, with an aim to inspire and inform research using museum collections. We focus on analyses of bulk tissues and proteins, and we discuss ways in which sampling strategies for museum specimens can be adjusted to suit the research question, including considerations such as the timing of feather molt and the length of time during the life of a bird that is reflected by a sample. We also discuss general caveats for interpreting isotope data, the variance of which is usually influenced by multiple factors. In greater detail, we present recommendations for sampling museum specimens, such as avoiding a potential confounding influence of melanin concentration on carbon isotope values in feather, and minimizing damage to museum specimens when sampling. Stable isotope data from museum specimens have great potential to inform ornithologists about the trophic and spatial ecology of birds, and to provide long-term baseline data for studying how these attributes may be changing in the Anthropocene.

Human-induced ecological change in the open oceans appears to be accelerating. Fisheries, climate change and elevated nutrient inputs are variously blamed, at least in part, for altering oceanic ecosystems. Yet it is challenging to assess the extent of anthropogenic change in the open oceans, where historical records of ecological conditions are sparse, and the geographical scale is immense. We developed millennial-scale amino acid nitrogen isotope records preserved in ancient animal remains to understand changes in food web structure and nutrient regimes in the oceanic realm of the North Pacific Ocean (NPO). Our millennial-scale isotope records of amino acids in bone collagen in a wide-ranging oceanic seabird, the Hawaiian petrel ( Pterodroma sandwichensis ), showed that trophic level declined over time. The amino acid records do not support a broad-scale increase in nitrogen fixation in the North Pacific subtropical gyre, rejecting an earlier interpretation based on bulk and amino acid specific δ 15 N chronologies for Hawaiian deep-sea corals and bulk δ 15 N chronologies for the Hawaiian petrel. Rather, our work suggests that the food web structure in the NPO has shifted at a broad geographical scale, a phenomenon potentially related to industrial fishing.

* Wiley, A. E., H. F. James, and P. H. Ostrom. 2017. Emerging techniques for isotope studies of avian ecology. Pp. 89–109 in M. S. Webster (editor), The Extended Specimen: Emerging Frontiers in Collections-based Ornithological Research. Studies in Avian Biology (no. 50), CRC Press, Boca Raton, FL. Abstract. Stable isotope analysis has expanded the usefulness of avian specimen collections in ways that were generally unanticipated by the original collectors. This technique enables aspects of avian ecology to be studied using very small samples of feather or other tissue taken from specimens. Stable isotope values can be informative about diet, trophic ecology, spatial habitat use, and the migratory connectivity of breeding and nonbreeding populations. They can also provide access to understudied time periods in a bird’s annual cycle, particularly periods of molt. Use of museum specimens offers advantages for these studies: museum collections generally span longer time periods than field samples and represent broad geographic ranges. In this chapter, we review established and emerging isotopic techniques and their applications in avian ecology, with an aim to inspire and inform research using museum collections. We focus on analyses of bulk tissues and proteins, and we discuss ways in which sampling strategies for museum specimens can be adjusted to suit the research question, including considerations such as the timing of feather molt and the length of time during the life of a bird that is reflected by a sample. We also discuss general caveats for interpreting isotope data, the variance of which is usually influenced by multiple factors. In greater detail, we present recommendations for sampling museum specimens, such as avoiding a potential confounding influence of melanin concentration on carbon isotope values in feather, and minimizing damage to museum specimens when sampling. Stable isotope data from museum specimens have great potential to inform ornithologists about the trophic and spatial ecology of birds, and to provide long-term baseline data for studying how these attributes may be changing in the Anthropocene.

Citation for published item: Wiley, A.E. and Ostrom, P.H. and Welch, A.J. and Fleischer, R.C. and Gandhi, H. and Southon, J.R. and Sta ord, T.W. and Penniman, J.F. and Hu, D. and Duvall, F.P. and James, H.F. (2013) 'Millennial-scale isotope records from a wide-ranging predator show evidence of recent human impact to oceanic food webs.', Proceedings of the National Academy of Sciences of the United States of America., 110 (22). pp. 8972-8977.

Hydrogen isotopes have significantly enhanced our understanding of the biogeography of migratory animals. The basis for this methodology lies in predictable, continental patterns of precipitation δD values that are often reflected in an organism's tissues. δD variation is not expected for oceanic pelagic organisms whose dietary hydrogen (water and organic hydrogen in prey) is transferred up the food web from an isotopically homogeneous water source. We report a 142‰ range in the δD values of flight feathers from the Hawaiian petrel (Pterodroma sandwichensis), an oceanic pelagic North Pacific species, and inquire about the source of that variation. We show δD variation between and within four other oceanic pelagic species: Newell's shearwater (Puffinus auricularis newellii), Black-footed albatross (Phoebastria nigripes), Laysan albatross (Phoebastria immutabilis) and Buller's shearwater (Puffinus bulleri). The similarity between muscle δD values of hatch-year Hawaiian petrels and their prey suggests that trophic fractionation does not influence δD values of muscle. We hypothesize that isotopic discrimination is associated with water loss during salt excretion through salt glands. Salt load differs between seabirds that consume isosmotic squid and crustaceans and those that feed on hyposmotic teleost fish. In support of the salt gland hypothesis, we show an inverse relationship between δD and percent teleost fish in diet for three seabird species. Our results demonstrate the utility of δD in the study of oceanic consumers, while also contributing to a better understanding of δD systematics, the basis for one of the most commonly utilized isotope tools in avian ecology.

Human exploitation of marine ecosystems is more recent in oceanic than near shore regions, yet our understanding of human impacts on oceanic food webs is comparatively poor. Few records of species that live beyond the continental shelves date back more than 60 y, and the sheer size of oceanic regions makes their food webs difficult to study, even in modern times. Here, we use stable carbon and nitrogen isotopes to study the foraging history of a generalist, oceanic predator, the Hawaiian petrel (Pterodroma sandwichensis), which ranges broadly in the Pacific from the equator to near the Aleutian Islands. Our isotope records from modern and ancient, radiocarbon-dated bones provide evidence of over 3,000 y of dietary stasis followed by a decline of ca. 1.8‰ in δ(15)N over the past 100 y. Fishery-induced trophic decline is the most likely explanation for this sudden shift, which occurs in genetically distinct populations with disparate foraging locations. Our isotope records also show that coincident with the apparent decline in trophic level, foraging segregation among petrel populations decreased markedly. Because variation in the diet of generalist predators can reflect changing availability of their prey, a foraging shift in wide-ranging Hawaiian petrel populations suggests a relatively rapid change in the composition of oceanic food webs in the Northeast Pacific. Understanding and mitigating widespread shifts in prey availability may be a critical step in the conservation of endangered marine predators such as the Hawaiian petrel.

Seabirds are highly vagile and can disperse up to thousands of kilometers, making it difficult to identify the factors that promote isolation between populations. The endemic Hawaiian petrel (Pterodroma sandwichensis) is one such species. Today it is endangered, and known to breed only on the islands of Hawaii, Maui, Lanai and Kauai. Historical records indicate that a large population formerly bred on Molokai as well, but this population has recently been extirpated. Given the great dispersal potential of these petrels, it remains unclear if populations are genetically distinct and which factors may contribute to isolation between them. We sampled petrels from across their range, including individuals from the presumably extirpated Molokai population. We sequenced 524 bp of mitochondrial DNA, 741 bp from three nuclear introns, and genotyped 18 microsatellite loci in order to examine the patterns of divergence in this species and to investigate the potential underlying mechanisms. Both mitochondrial and nuclear data sets indicated significant genetic differentiation among all modern populations, but no differentiation was found between historic samples from Molokai and modern birds from Lanai. Population-specific nonbreeding distribution and strong natal philopatry may reduce gene flow between populations. However, the lack of population structure between extirpated Molokai birds and modern birds on Lanai indicates that there was substantial gene flow between these populations and that petrels may be able to overcome barriers to dispersal prior to complete extirpation. Hawaiian petrel populations could be considered distinct management units, however, the dwindling population on Hawaii may require translocation to prevent extirpation in the near future.

In the Hawaiian Islands, human colonization, which began approximately 1,200 to 800 years ago, marks the beginning of a period in which nearly 75% of the endemic avifauna became extinct and the population size and range of many additional species declined. It remains unclear why some species persisted whereas others did not. The endemic Hawaiian petrel (Pterodroma sandwichensis) has escaped extinction, but colonies on two islands have been extirpated and populations on remaining islands have contracted. We obtained mitochondrial DNA sequences from 100 subfossil bones, 28 museum specimens, and 289 modern samples to investigate patterns of gene flow and temporal changes in the genetic diversity of this endangered species over the last 3,000 years, as Polynesians and then Europeans colonized the Hawaiian Islands. Genetic differentiation was found to be high between both modern and ancient petrel populations. However, gene flow was substantial between the extirpated colonies on Oahu and Molokai and modern birds from the island of Lanai. No significant reductions in genetic diversity occurred over this period, despite fears in the mid-1900s that this species may have been extinct. Simulations show that even a decline to a stable effective population size of 100 individuals would result in the loss of only 5% of the expected heterozygosity. Simulations also show that high levels of genetic diversity may be retained due to the long generation time of this species. Such decoupling between population size and genetic diversity in long-lived species can have important conservation implications. It appears that a pattern of dispersal from declining colonies, in addition to long generation time, may have allowed the Hawaiian petrel to escape a severe genetic bottleneck, and the associated extinction vortex, and persist despite a large population decline after human colonization.

Foraging segregation may play an important role in the maintenance of animal diversity, and is a proposed mechanism for promoting genetic divergence within seabird species. However, little information exists regarding its presence among seabird populations. We investigated genetic and foraging divergence between two colonies of endangered Hawaiian petrels (Pterodroma sandwichensis) nesting on the islands of Hawaii and Kauai using the mitochondrial Cytochrome b gene and carbon, nitrogen and hydrogen isotope values (δ13C, δ15N and δD, respectively) of feathers. Genetic analyses revealed strong differentiation between colonies on Hawaii and Kauai, with ΦST = 0.50 (p < 0.0001). Coalescent-based analyses gave estimates of <1 migration event per 1,000 generations. Hatch-year birds from Kauai had significantly lower δ13C and δ15N values than those from Hawaii. This is consistent with Kauai birds provisioning chicks with prey derived from near or north of the Hawaiian Islands, and Hawaii birds provisioning young with prey from regions of the equatorial Pacific characterized by elevated δ15N values at the food web base. δ15N values of Kauai and Hawaii adults differed significantly, indicating additional foraging segregation during molt. Feather δD varied from −69 to 53‰. This variation cannot be related solely to an isotopically homogeneous ocean water source or evaporative water loss. Instead, we propose the involvement of salt gland excretion. Our data demonstrate the presence of foraging segregation between proximately nesting seabird populations, despite high species mobility. This ecological diversity may facilitate population coexistence, and its preservation should be a focus of conservation strategies.