Four millennia of long-term individual foraging site fidelity in a highly migratory marine predator

Understanding foraging mobility is crucial for conserving migratory species recovering from overexploitation. The short-tailed albatross (Phoebastria albatrus), once abundant, was nearly driven to extinction but is now recovering. Current conservation efforts focus on monitoring breeding colonies and foraging ranges, but the species remains at less than 1% of its pre-collapse population. Anticipating shifts in foraging behavior in response to population growth and potential threats like fisheries bycatch is vital. Short-tailed albatrosses forage in neritic and oceanic habitats, concentrating in hotspots associated with bathymetry and climate. Juveniles explore more widely than adults. Currently, bycatch mitigation focuses on known hotspots, but understanding the factors governing foraging area selection and time allocation is crucial for effective conservation. Individual foraging site fidelity (ISF), where birds forage primarily in a subset of the population's range, is another important element. Long-term ISF (repeated over multiple annual cycles) increases vulnerability to localized hazards. While recognized in some seabird populations, its prevalence among short-tailed albatrosses is unknown. Modern observations suggest some juvenile ISF, but most individuals show low spatial fidelity. Low population sizes mean that behavior may change as the species recovers. Archaeological and historical data can provide insight into past distributions and abundance, but not individual or population-level foraging fidelity. This study uses isotopic analysis of archaeological specimens to explore long-term patterns in foraging characteristics.

Previous research suggests that long-term individual foraging site fidelity (IFSF) is an important adaptation to competition from increasing population density in many species. However, studying this in wild populations of long-lived, migratory animals is logistically challenging, and confirmed instances are rare. Stable isotope analysis of animal tissues, particularly bone collagen (which reflects long-term dietary patterns), can reveal geographical foraging behavior. Previous isotopic analyses of short-tailed albatross bone collagen from various North Pacific locations have shown varying degrees of isotopic niche breadth, indicating differences in foraging strategies and habitat use across their range. These studies however, did not address the question of long-term individual foraging site fidelity in this species.

This study analyzed the stable carbon (δ13C) and nitrogen (δ15N) isotope compositions of bone collagen from 95 archaeological short-tailed albatross specimens collected from the Yuquot site on Vancouver Island, spanning a 450-year period (1520-1970 CE). Two nineteenth-century feather samples from the nearby Juan de Fuca Strait were also included. The large sample size, temporal span, restricted geographical area, and the site's location at the edge of the species' foraging range provided an ideal context to study variation in foraging fidelity. Archaeological specimens were selected using established protocols to minimize bias. Samples underwent rigorous cleaning and pretreatment to remove contaminants. Isotope analysis was conducted using established methods. Statistical analyses, including Pearson's correlation, Shapiro-Wilk tests, Levene's tests, and Welch's t-test, were performed to assess isotopic variation among different temporal groups. A bootstrapping simulation was used to assess the probability of observing the observed isotopic patterns under random conditions. The results were compared to previously published isotopic data from other North Pacific sites. Data on elemental concentrations, isotopic ratios, and other analytical parameters were collected and subjected to rigorous quality control measures to assure that the isotopic signatures were not altered by contamination or degradation. Internal and external standards were used for calibration and quality assurance.

Ninety-three bone collagen samples passed quality control. Mean δ13C and δ15N values were -14.6 ± 0.4‰ and +18.0 ± 0.7‰, respectively. There were no statistically significant differences in mean δ13C and δ15N between sequential time periods. The isotopic niche of the Yuquot site sample was much smaller than samples from other regions of the species' range. This suggests that individuals from the Yuquot site shared a more narrowly defined and geographically similar foraging area compared to birds from other locations. Furthermore, the consistent isotopic values across time periods suggest that foraging habitats used near the Yuquot site were stable over the 4250-year study period. Isotopic compositions from two 19th-century feather samples closely matched those from bone collagen, indicating that foraging behaviors remained similar until at least the late 1880s. The smaller isotopic niche at Yuquot compared to other regions suggests either that birds from this area fed in equal proportions across various prey types and habitats, or, more plausibly, that they exhibited high long-term individual foraging site fidelity (IFSF), focusing on a smaller number of hotspots near the west coast of Vancouver Island. Historical records indicate that the area may have once contained significant foraging hotspots that are now less important. The absence of long-term IFSF in modern populations may be linked to low population density and the resulting low competition. This study did not assess age differences of the specimens, but the findings were consistent for both juvenile and adult foraging behaviors.

The narrow isotopic niche at the Yuquot site strongly supports the hypothesis of long-term IFSF in short-tailed albatrosses in this region. This contrasts with the wider isotopic niches observed in other regions, suggesting that individuals at the Yuquot site displayed a stronger geographic affinity to specific foraging areas. The consistency of isotopic values across millennia suggests that these foraging areas remained stable over thousands of years. The absence of modern long-term IFSF could be a consequence of low population density and reduced interspecific/intraspecific competition. As the population grows, there is a chance that long-term IFSM could re-emerge, making some birds more susceptible to localized hazards. The study highlights a need for further multi-year tracking studies and genetic analyses to fully understand the drivers and implications of this behavior.

This study provides the first large-scale evidence for the deep antiquity of long-term IFSF in a highly migratory marine predator. The findings suggest that density-dependent competition may be a driving force behind this behavior. As short-tailed albatross populations recover, the potential resurgence of geographic specialization may increase exposure to localized hazards, necessitating continued monitoring and adaptation of conservation strategies. Future research should focus on integrating genetic analyses with longer-term tracking studies to fully elucidate the mechanisms governing IFSF and its conservation implications.

The study could not determine the biological ages of the specimens, preventing a direct assessment of age-related variation in foraging behavior. The interpretation of isotopic data relies on assumptions about the relationship between isotopic values and foraging area, and other factors could have influenced isotopic variation. While the findings strongly suggest long-term IFSF, the study cannot definitively rule out other possible explanations, and the exact geographical locations of the foraging hotspots remain uncertain.