Deep antiquity of seagrasses supporting European eel fisheries in the western Baltic.

Protecting ocean habitats is critical for international efforts to mitigate climate impacts and ensure food security, but the ecological data upon which policy makers base conservation and restoration targets often reflect ecosystems that have already been deeply impacted by anthropogenic change. The archaeological record is a biomolecular archive offering a temporal scope that cannot be gathered from historical records or contemporary fieldwork. Insights from biogeochemical and osteometric analyses of fish bones, combined with context from contemporary field studies, show how prehistoric fisheries in the western Baltic relied on seagrass meadows. European eels (Anguilla anguilla) harvested by Mesolithic and Neolithic peoples over millennia showed a strong fidelity for eelgrass foraging habitats, an ecological relationship that remains largely overlooked today, demonstrating the value of protecting these habitats. These data open new windows onto ecosystem- and species-level behaviours, highlighting the need for wider incorporation of archaeological data in strategies for protecting our oceans.

Seaweed-eating sheep show that δ34 S evidence for marine diets can be fully masked by sea spray effects.

RATIONALE: Stable sulfur isotope compositions (δ34 S values) are a useful marker of terrestrial (lower δ34 S) versus marine (higher δ34 S) diets. In coastal areas, 34 S-enriched sea spray can obscure these marine/terrestrial differences. We sought to establish whether δ34 S values of sea spray-affected terrestrial fauna can be distinguished from those of marine-feeding terrestrial fauna. METHODS: We measured bone and dentine collagen δ34 S values, as well as stable carbon (δ13 C) and nitrogen (δ15 N) isotope compositions via continuous flow elemental analysis/isotope ratio mass spectrometry of 21 sheep (Ovis aries) raised on an island (North Ronaldsay, UK) of <7 km2 that had widely divergent access to marine (seaweed) and heavily sea spray-affected terrestrial (grass) food sources. We also analyzed the bone collagen of marine and terrestrial fauna from this island. RESULTS: Sheep bone collagen showed well-defined trends with highly significant correlations between δ13 C and δ15 N values indicative of feeding along a continuum of fully terrestrial to fully marine diets, consistent with other modern baseline data from marine and terrestrial animals in the same area. In contrast, δ34 S values were generally elevated for all sheep and were not significantly correlated with either δ13 C or δ15 N values. CONCLUSIONS: Our findings demonstrate that δ34 S values are poorly suited for differentiating marine and terrestrial diets in terrestrial animals in areas with pronounced sea spray effects. Care must be taken to characterize the isotopic compositions of potential food items before δ34 S values are used as a marker for reliance on marine protein in modern and ancient contexts.

Effects of lipid extraction and ultrafiltration on stable carbon and nitrogen isotopic compositions of fish bone collagen.

RATIONALE: Fish bone collagen isotopic measurements are increasingly important in palaeodietary and paleoenvironmental studies yet differences in the chemical and physical properties of fish relative to other vertebrate bones are rarely considered. Lipid content in fish bone, which can exceed 50%, may underlie the poor collagen integrity criteria typically observed in archaeological studies. METHODS: We compare stable carbon and nitrogen isotopic and elemental compositions of bone collagen prepared using four different methods from a wide range of modern fish species to: (1) assess the extent to which lipid content influences bone collagen δ(13) C and δ(15) N values, and (2) evaluate the relative efficacy of chemical (2:1 chloroform/methanol) and physical (30 kDa ultrafilters) methods for removing lipids from bones. RESULTS: Lower δ(13) C values were observed when the lipid content exceeded 5% of the initial bone mass. The lipid content did not influence the δ(15) N values. 30 kDa ultrafiltration, a common pretreatment for purifying archaeological collagen, removed fewer lipids and was associated with reduced collagen yields (37% loss) as well as altered amino acid compositions. In contrast, collagen prepared using a 2:1 chloroform/methanol lipid extraction step resulted in significantly improved collagen yields, elemental compositions, and isotopic measurements relative to a control treatment. CONCLUSIONS: The chemical lipid extraction method (2:1 chloroform/methanol) performed significantly better than the physical lipid extraction method (30 kDa ultrafilters). Given the high quantities of lipids in fish bones we recommend the inclusion of a chemical lipid extraction step when isolating collagen from modern and archaeological fish bones. Copyright © 2016 John Wiley & Sons, Ltd.

Archaeological evidence for long-term human impacts on sea turtle foraging behaviour.

Early conservation efforts to prevent the loss of green sea turtles (Chelonia mydas) from the Caribbean Sea jumpstarted marine habitat and biodiversity protection. However, even there, limitations on historical observations of turtle ecology have hampered efforts to contextualize foraging behaviours for conservation management. We integrate isotopic and zooarchaeological evidence from green sea turtles harvested at the Miskito Cays (Nicaragua) to assess foraging behaviour before and after a step change in harvesting intensity. Highly structured isotopic evidence shows greater foraging adaptability in earlier populations. This provides a counterpoint to recent synthesis, suggesting the ecological non-exchangeability of sea turtles, which complicates conservation planning focused on genetic-stock-based repopulation. In contrast, our results suggest future populations would have a capacity for higher degrees of ecological exchangeability than current perspectives allow. This highlights a need to consider the kinds of longer term perspectives, such as those offered by archaeological materials, when planning for future sea turtle recovery.

The ratting of North America: A 350-year retrospective on Rattus species compositions and competition.

While the impacts of black (Rattus rattus) and brown (Rattus norvegicus) rats on human society are well documented-including the spread of disease, broad-scale environmental destruction, and billions spent annually on animal control-little is known about their ecology and behavior in urban areas due to the challenges of studying animals in city environments. We use isotopic and ZooMS analysis of archaeological (1550s-1900 CE) rat remains from eastern North America to provide a large-scale framework for species arrival, interspecific competition, and dietary ecology. Brown rats arrived earlier than expected and rapidly outcompeted black rats in coastal urban areas. This replacement happened despite evidence that the two species occupy different trophic positions. Findings include the earliest molecularly confirmed brown rat in the Americas and show a deep ecological structure to how rats exploit human-structured areas, with implications for understanding urban zoonosis, rat management, and ecosystem planning as well as broader themes of rat dispersal, phylogeny, evolutionary ecology, and climate impacts.

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

Theory and field studies suggest that long-term individual foraging site fidelity (IFSF) may be an important adaptation to competition from increasing population. However, the driving mechanisms and extent of long-term IFSF in wild populations of long-lived, migratory animals has been logistically difficult to study, with only a few confirmed instances. Temporal isotopic datasets can reveal long-term patterns in geographical foraging behaviour. We investigate the isotopic compositions of endangered short-tailed albatross (Phoebastria albatrus) over four millennia leading up to their near-extinction. Although not exhibited by short-tailed albatross today, we show past sub-populations displayed a high-degree of long-term IFSF, focusing on the same locations for hundreds of generations. This is the first large-scale evidence for the deep antiquity of long-term IFSF and suggests that it's density-driven. Globally, as populations of species like short-tailed albatross continue to recover from overexploitation, potential for resurgence of geographic specialization may increase exposure to localized hazards, requiring closer conservation monitoring.

Documenting the short-tailed albatross (Phoebastria albatrus) clades historically present in British Columbia, Canada, through ancient DNA analysis of archaeological specimens.

The short-tailed albatross (Phoebastria albatrus) is a threatened seabird whose present-day range encompasses much of the North Pacific. Within this species, there are two genetic clades (Clades 1 and 2) that have distinctive morphologies and foraging ecologies. Due to a global population collapse in the late 19th and early 20th centuries, the frequency of these clades among the short-tailed albatross population that historically foraged off British Columbia, Canada, is unclear. To document the species' historical genetic structure in British Columbia, we applied ancient DNA (aDNA) analysis to 51 archaeological short-tailed albatross specimens from the Yuquot site (Borden site number: DjSp-1) that span the past four millennia. We obtained a 141 bp cytochrome b sequence from 43 of the 51 (84.3%) analyzed specimens. Analyses of these sequences indicate 40 of the specimens belong to Clade 1, while 2 belong to Clade 2. We also identified a single specimen with a novel cytochrome b haplotype. Our results indicate that during the past four millennia most of the short-tailed albatrosses foraging near Yuquot belonged to Clade 1, while individuals from other lineages made more limited use of the area. Comparisons with the results of previous aDNA analyses of archaeological albatrosses from Japanese sites suggest the distribution of Clades 1 and 2 differed. While both albatross clades foraged extensively in the Northwest Pacific, Clade 1 albatrosses appear to have foraged along the west coast of Vancouver Island to a greater extent. Due to their differing distributions, these clades may be exposed to different threats.

The evolution of dog diet and foraging: Insights from archaeological canids in Siberia.

Research on the evolution of dog foraging and diet has largely focused on scavenging during their initial domestication and genetic adaptations to starch-rich food environments following the advent of agriculture. The Siberian archaeological record evidences other critical shifts in dog foraging and diet that likely characterize Holocene dogs globally. By the Middle Holocene, body size reconstruction for Siberia dogs indicates that most were far smaller than Pleistocene wolves. This contributed to dogs' tendencies to scavenge, feed on small prey, and reduce social foraging. Stable carbon and nitrogen isotope analysis of Siberian dogs reveals that their diets were more diverse than those of Pleistocene wolves. This included habitual consumption of marine and freshwater foods by the Middle Holocene and reliance on C4 foods by the Late Holocene. Feeding on such foods and anthropogenic waste increased dogs' exposure to microbes, affected their gut microbiomes, and shaped long-term dog population history.

Early evidence for historical overfishing in the Gulf of Mexico.

Fisheries encompass complex interplays between social, economic, and environmental factors, but limitations on historical fisheries data can hamper efforts to identify and contextualize the long-term spatiotemporal patterns that shape them. We integrate 2500 years of stable isotope (δ34S, δ13C, and δ15N) and zooarchaeological evidence from Gulf of Mexico fisheries to assess cultural, demographic, and technological changes affecting sheepshead (Archosargus probatocephalus) populations and fishing practices in Louisiana, USA. Concurrent with human population growth, average sizes of sheepshead caught decreased from the 1720s to 1830s. The size of fish caught after the 1830s increased to pre-1720 levels at the same time that isotopic compositions of fish bone collagen show that fish were being caught from a more diverse range of ecosystems, including distant seagrass beds. Our findings provide the first evidence for large-scale depressions of historical sheepshead populations and the processes driving them, including rapid human population growth and sustained harvesting pressure.

Integrating fish scale and bone isotopic compositions for 'deep time' retrospective studies.

Isotopic studies of archived fish scales have tremendous potential to develop long-term retrospectives that provide important insights into how humans have altered aquatic ecosystems. However, fish specimens in museum archives and other repositories typically date to time periods when the impacts of industrial societies may have already caused profound environmental changes. Archaeological fish bones offer an opportunity to bridge this key temporal gap by providing samples spanning from the recent past to as far back as the Pleistocene. Collagen is the primary protein component of both fish scale and bone, but the comparability of isotopic compositions from these tissues has not been established experimentally. To lay the framework for integrating isotopic datasets from these tissues, we compare δ13C and δ15N of bone and scale collagen, as well as other tissues, from fish with life-time controlled diets. Results show that while there is no difference in δ13C between scale and bone collagen, there may be a very slight but meaningful inter-tissue offset in δ15N (<0.3‰). We discuss potential sources of δ15N variation in scale and bone collagen measurements. Because there is no difference in scale and bone δ13C, and the observed offset in δ15N is very small (less than analytical uncertainty in many studies), our findings demonstrate that collagen isotopic compositions from these tissues should be directly comparable when integrating datasets from modern and ancient samples to build more powerful, millennium-scale isotopic times series. In linking isotopic compositions of collagen from modern, historical (scales), and archaeological (bones) fish, our findings open the way for more nuanced contextualization of how ecosystems functioned prior to large-scale exploitation and how they have responded to mounting anthropogenic pressures in the intervening centuries.

Storing fish?: a dog's isotopic biography provides insight into Iron Age food preservation strategies in the Russian Arctic.

Analysis of individual animal bodies can provide numerous useful insights in archeology, including how humans provisioned such animals, which in turn informs on a variety of other past behaviors such as human dietary patterns. In this study, we conducted stable carbon (δ 13C) and nitrogen (δ 15N) isotope analysis of collagen and keratin from four types of tissues from a dog burial at the Ust'-Polui site in the Iamal region of Arctic Russia. Ust'-Polui is an Iron Age site located on the Lower Ob River, a major northern fishery characterized by extreme seasonal shifts in fish presence. During a 6-month period stretching over the coldest months of the year, fish are nearly entirely absent in the Lower Ob River. Despite this, the stable isotope compositions of the dog's bone and dentine collagen and hair and nail keratin all indicate a monotonous diet focusing on local fish. This pattern indicates the dog was provisioned year-round with fish. This was likely accomplished by mass harvesting of fish using nets or traps. Such fish were then processed and frozen for consumption during the non-fishing season. These findings suggest that people in the Ust'-Polui region also relied to some extent on fish throughout the year. Stored fish likely provided a dietary buffer for uneven returns from reindeer and bird hunting, both of which also are well-evidenced at the site.

Ancient dog diets on the Pacific Northwest Coast: zooarchaeological and stable isotope modelling evidence from Tseshaht territory and beyond.

Domestic dogs are frequently encountered in Indigenous archaeological sites on the Northwest Coast of North America. Although dogs depended on human communities for care and provisioning, archaeologists lack information about the specific foods dogs consumed. Previous research has used stable isotope analysis of dog diets for insight into human subsistence ('canine surrogacy' model) and identified considerable use of marine resources. Here, we use zooarchaeological data to develop and apply a Bayesian mixing model (MixSIAR) to estimate dietary composition from 14 domestic dogs and 13 potential prey taxa from four archaeological sites (2,900-300 BP) in Tseshaht First Nation territory on western Vancouver Island, British Columbia, Canada. Two candidate models that best match zooarchaeological data indicate dogs predominantly consumed salmon and forage fish (35-65%), followed by nearshore fish (4-40%), and marine mammals (2-30%). We compared these isotopic data to dogs across the Northwest Coast, which indicated a pronounced marine diet for Tseshaht dogs and, presumably, their human providers. These results are broadly consistent with the canine surrogacy model as well as help illuminate human participation in pre-industrial marine food webs and the long-term role of fisheries in Indigenous economies and lifeways.

Differentiating salmonid migratory ecotypes through stable isotope analysis of collagen: Archaeological and ecological applications.

The ability to distinguish between different migratory behaviours (e.g., anadromy and potamodromy) in fish can provide important insights into the ecology, evolution, and conservation of many aquatic species. We present a simple stable carbon isotope (δ13C) approach for distinguishing between sockeye (anadromous ocean migrants) and kokanee (potamodromous freshwater residents), two migratory ecotypes of Oncorhynchus nerka (Salmonidae) that is applicable throughout most of their range across coastal regions of the North Pacific Ocean. Analyses of kokanee (n = 239) and sockeye (n = 417) from 87 sites spanning the North Pacific (Russia to California) show that anadromous and potamodromous ecotypes are broadly distinguishable on the basis of the δ13C values of their scale and bone collagen. We present three case studies demonstrating how this approach can address questions in archaeology, archival, and conservation research. Relative to conventional methods for determining migratory status, which typically apply chemical analyses to otoliths or involve genetic analyses of tissues, the δ13C approach outlined here has the benefit of being non-lethal (when applied to scales), cost-effective, widely available commercially, and should be much more broadly accessible for addressing archaeological questions since the recovery of otoliths at archaeological sites is rare.

Anthropogenic changes to the Holocene nitrogen cycle in Ireland.

Humans have always affected their ecosystems, but finding evidence for significant and lasting changes to preindustrial landscapes is rare. We report on human-caused changes to the nitrogen cycle in Ireland in the Bronze Age, associated with intensification of agriculture and animal husbandry that resulted in long-term changes to the nitrogen isotope values of animals (wild and domesticates) during the Holocene. Major changes to inputs and cycling of soil nitrogen occurred through deforestation, land clearance and management, and more intensive animal husbandry and cereal crop cultivation in the later Bronze Age; after this time, the Irish landscape took on its current form. Within the debate concerning the onset of the Anthropocene, our data suggest that human activity in Ireland was significant enough in the Bronze Age to have long-term impact, thereby marking a profound shift in the relationship between humans and their environment.

The evolutionary history of dogs in the Americas.

Dogs were present in the Americas before the arrival of European colonists, but the origin and fate of these precontact dogs are largely unknown. We sequenced 71 mitochondrial and 7 nuclear genomes from ancient North American and Siberian dogs from time frames spanning ~9000 years. Our analysis indicates that American dogs were not derived from North American wolves. Instead, American dogs form a monophyletic lineage that likely originated in Siberia and dispersed into the Americas alongside people. After the arrival of Europeans, native American dogs almost completely disappeared, leaving a minimal genetic legacy in modern dog populations. The closest detectable extant lineage to precontact American dogs is the canine transmissible venereal tumor, a contagious cancer clone derived from an individual dog that lived up to 8000 years ago.

Lake Ontario salmon (Salmo salar) were not migratory: A long-standing historical debate solved through stable isotope analysis.

Lake Ontario once supported a large complex of Atlantic Salmon (Salmo salar) populations that became extinct prior to scientific study. Since the 1860s, research efforts to conserve and reintroduce a sustainable population of Atlantic Salmon have focused on determining whether Lake Ontario's original salmon populations had migrated to the Atlantic Ocean as part of their lifecycle (anadromy), stayed in the lake year-round (potamodromy), or both. We used stable carbon, nitrogen, and sulfur isotope analyses of archaeological bones and historical museum-archived salmon scales to show that the original salmon populations from Lake Ontario completed their entire lifecycle without migrating to the Atlantic Ocean. With a time depth of more than 500 years, our findings provide a unique baseline with significant potential for informing modern restocking and conservation efforts.