Anne E. Wiley

Millennial-scale isotope records from a wide-ranging predator show evidence of recent human impact to oceanic food webs

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 δ15N 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.

Population divergence and gene flow in an endangered and highly mobile seabird

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.

Isotopic characterization of flight feathers in two pelagic seabirds: Sampling strategies for ecological studies

Abstract. We wish to use stable-isotope analysis of flight feathers to understand the feeding behavior of pelagic seabirds, such as the Hawaiian Petrel (Pterodroma sandwichensis) and Newells Shearwater (Puffinus auricularis newelli). Analysis of remiges is particularly informative because the sequence and timing of remex molt are often known. The initial step, reported here, is to obtain accurate isotope values from whole remiges by means of a minimally invasive protocol appropriate for live birds or museum specimens. The high variability observed in &dgr;13C and &dgr;15N values within a feather precludes the use of a small section of vane. We found the average range within 42 Hawaiian Petrel remiges to be 1.3‰ for both &dgr;13C and &dgr;15N and that within 10 Newells Shearwater remiges to be 1.3‰ and 0.7‰ for &dgr;13C and &dgr;15N, respectively. The &dgr;13C of all 52 feathers increased from tip to base, and the majority of Hawaiian Petrel feathers showed an analogous trend in &dgr;15N. Although the average range of &dgr;D in 21 Hawaiian Petrel remiges was 11‰, we found no longitudinal trend. We discuss influences of trophic level, foraging location, metabolism, and pigmentation on isotope values and compare three methods of obtaining isotope averages of whole feathers. Our novel barb-sampling protocol requires only 1.0 mg of feather and minimal preparation time. Because it leaves the feather nearly intact, this protocol will likely facilitate obtaining isotope values from remiges of live birds and museum specimens. As a consequence, it will help expand the understanding of historical trends in foraging behavior.

Ancient DNA Reveals Genetic Stability Despite Demographic Decline: 3,000 Years of Population History in the Endemic Hawaiian Petrel

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.

Broad-scale trophic shift in the pelagic North Pacific revealed by an oceanic seabird

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 δ15N chronologies for Hawaiian deep-sea corals and bulk δ15N 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.

Influence of Feather Selection and Sampling Protocol on Interpretations of Hawaiian Petrel (Pterodroma sandwichensis) Nonbreeding Season Foraging Habits from Stable Isotope Analysis

Abstract. 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 δ13C increased longitudinally, no δ15N longitudinal trends emerged, yet inter-individual δ15N variability was high. P6 δ13C data suggest that Hawaiian Petrels molt at low latitudes. Among colonies, all of which are located in the Hawaiian Islands, USA, low P6 δ15N values for Maui birds relative to Hawaii and Lanai birds reflect foraging segregation and differential utilization of 15N-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 skin ornaments reflect foraging propensity in a seabird, Sula leucogaster.

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.