Ancient Food Webs Research Articles

Sedimentary ancient DNA sequences reveal marine ecosystem shifts and indicator taxa for glacial-interglacial sea ice conditions

Sedimentary ancient DNA (sedaDNA) analysis is a promising new approach for reconstructing the impact of past climate and environmental changes on marine paleobiodiversity. By recovering, amplifying, and sequencing taxonomically informative sedaDNA fragments preserved in sediments, it is possible to assess the response of a broad range of eukaryote taxa, including non-fossilizing lineages, to past climate change. Here we present a unique marine derived sedaDNA metabarcoding record, spanning the penultimate glacial-interglacial transition across Marine Isotope Stages 6 to 5d (>135–107 ka) from an Eirik Drift core-site in the Labrador Sea. We identified a range of marine groups including dinoflagellates, diatoms, coccolithophores, chlorophytes, and copepods. There were representatives of primary/secondary producers, grazers, and parasites, which may represent remnants of complex ecosystems and ancient food webs. There were significant biodiversity shifts following the penultimate deglaciation and changing sea ice conditions throughout the Last Interglacial. These shifts reflected the striking increase in community richness during periods of seasonal sea ice and reduction under extensive perennial sea ice cover and open ocean. We identify two potential sedaDNA indicator taxa sequences associated with past seasonal sea ice which are most likely pico-eukaryote representatives of Micromonas and Pyramimonas, both green algae with known sea ice associations in modern ecosystems. Our work demonstrates the importance of high resolution marine sedaDNA metabarcoding for unravelling climate-ecosystem linkages and strengthens the potential of sedaDNA signals for past sea ice reconstructions through indicator sequences.

Sea Otters, Mercury, and Monitoring Climate Change

An increase in mobility of heavy metals, like mercury (Hg), has the potential to be one of the climate change related impacts on Arctic and sub-Arctic ecosystems. Sea level rise and flooding events in high latitude coastal ecosystems could increase the bioavailability of contaminants such as mercury. Mercury concentrations have been used as an indicator of past exposure to heavy metals in ancient Pacific cod and here we report on concentrations in archeologically recovered sea otter bones (Enhydra lutris). Methods utilizing stable isotope ratios can be used to reconstruct ancient food webs and help identify prey which may have bioaccumulated high concentrations of mercury. Modern sea otters have δ13C, δ15N, and mercury values corresponding largely to a benthic diet. Conversely, if higher δ15N and mercury levels were found in ancient sea otter bones located in a coastal ecosystem, these increases may be associated with rising sea level following the last glacial maximum. These data place present day and projected climate change related perturbations, like sea level rise, in a historical context.

Disentangling ecological and taphonomic signals in ancient food webs

AbstractAnalyses of ancient food webs reveal important paleoecological processes and responses to a range of perturbations throughout Earth's history, such as climate change. These responses can inform our forecasts of future biotic responses to similar perturbations. However, previous analyses of ancient food webs rarely accounted for key differences between modern and ancient community data, particularly selective loss of soft-bodied taxa during fossilization. To consider how fossilization impacts inferences of ancient community structure, we (1) analyzed node-level attributes to identify correlations between ecological roles and fossilization potential and (2) applied selective information loss procedures to food web data for extant systems. We found that selective loss of soft-bodied organisms has predictable effects on the trophic structure of “artificially fossilized” food webs because these organisms occupy unique, consistent food web positions. Fossilized food webs misleadingly appear less stable (i.e., more prone to trophic cascades), with less predation and an overrepresentation of generalist consumers. We also found that ecological differences between soft- and hard-bodied taxa—indicated by distinct positions in modern food webs—are recorded in an early Eocene web, but not in Cambrian webs. This suggests that ecological differences between the groups have existed for ≥48 Myr. Our results indicate that accounting for soft-bodied taxa is vital for accurate depictions of ancient food webs. However, the consistency of information loss trends across the analyzed food webs means it is possible to predict how the selective loss of soft-bodied taxa affects food web metrics, which can permit better modeling of ancient communities.

A Geometric Morphometric Evaluation of Equid Tooth Shape at Natural Trap Cave, Wyoming

Natural Trap Cave is a sinkhole cave located in Big Horn County in northern Wyoming. The cave preserves many Quaternary taxa, including pollen and large carnivorous and herbivorous mammals such as various felids and ungulates. Many of these taxa went extinct in North America following the late Pleistocene megafaunal extinction. The cave was first excavated in the 1970s and 80s by teams from the University of Kansas and the University of Missouri, and more recently by teams from Des Moines University, The University of Adelaide, and The University of Rochester, along with a wide variety of volunteers. Specimens from this cave have been used to elucidate floral change in the area, disentangle ancient food webs, and extend the hypothesized range for Beringian wolves.Horses are the most common megafaunal group from this site, encompassing two genera: Equus and Haringtonhippus, the “New World stilt‐legged” horse, based on post‐cranial elements and mitochondrial DNA. Some recent studies have shown that horse taxa can be identified by tooth occlusal surface morphology. This study aims to test if isolated equid cheek teeth from Natural Trap Cave can be identified to the genus level, between Equus and Haringtonhippus using geometric morphometrics. 2D landmarks and sliding semi‐landmarks were taken around the periphery of a set of upper cheek teeth, including the areas of greatest curvature at the metastyle, mesostyle, parastyle, and around the protocone and post protoconal valley. Principal component analyses on known specimens do in fact separate Equus and Haringtonhippus, and this difference is statistically sigificant, with the primary difference being the width of the protocone. Additionally, molars and premolars also occupied significantly different areas of morphospace, opening up the possibility of identifying tooth position on unknown specimens as well. With the abundance of isolated horse teeth (either Equus or Haringtonhippus) from Natural Trap Cave, having a reliable means to distinguish between genera will allow us to better study the ecological differences between them and better understand the environment and faunal interactions in late Pleistocene Wyoming.Support or Funding InformationNSF EAR/SGP 1425059 (Natural Trap Cave Revisited: Ancient DNA, Climate and the Megafaunal Extinction) Julie Meachen, PI

A new actinomycete from a Guadalupian vertebrate coprolite from Brazil

Coprolites (fossil feces) are important sources of evidence of ancient food webs and ecosystems. Actinomycetes are a fundamental component in the decay of organic matter, and serve as catalysts for nutrient cycles. Recently, gas vesicles filled with numerous verrucose colonies of substrate mycelium of an actinomycete were discovered inside a fossilized spiral amphipolar fish coprolite recovered from mid–Permian deposits of Brazil. These colonies are composed of masses of substrate hyphae, some of which are undergoing segmentation. Arising from the colonies are chains of spores separated by narrow, elongate connectives. The fossil actinomycete is described below as Palaeostromatus diairetus gen. et sp. nov. and represents the oldest known actinomycete associated with vertebrate deposits. Since the colonies occur only inside the coprolite, either Palaeostromatus diairetus gen. et sp. nov. was part of the gut flora or it was acquired from a food source. The only other remains in the coprolite are eighteen paleoniscoid fish scales, which suggests that the producer was a carnivorous/omnivorous fish. This is the oldest record of a direct interaction between vertebrates and actinomycetes.

Microbiota and food residues including possible evidence of pre-mammalian hair in Upper Permian coprolites from Russia

Coprolites (fossil faeces) provide direct evidence on the diet of its producer and unique insights on ancient food webs and ecosystems. We describe the contents of seven coprolites, collected from the Late Permian Vyazniki site of the European part of Russia. Two coprolite morphotypes (A, B) contain remains of putative bacteria, cyanobacteria, fungi, protists, invertebrate eggs, arthropod elements, undigested bone and tooth fragments, fish scales and elongated hair-like structures with hollow interiors. Content, size and shape of the coprolites together with the associated body fossil record suggest that the most probable scat-producers were carnivorous tetrapods; the bone-rich morphotype A reveals short food retention time and a fast metabolism and is therefore assigned to therapsid carnivores whereas morphotype B with rarer and degraded bones are assigned to archosauromorphs or other non-therapsid carnivores. The general coprolite matrix contains abundant micron-sized spheres and thin-walled vesicles which are interpreted as oxide and phosphatic pseudomorphs after microbial cells. From analyses of the undigested bones, we infer that they represent remains of actinopterygian fish, a therapsid and unrecognizable parts of amphibians and/or reptiles. Additionally, hair-like structures found in one coprolite specimen occur as diagenetically altered (oxide-replaced) structures and moulds (or partly as pseudomorphs) in a microcrystalline carbonate-fluoride-bearing calcium phosphate. This suggests that the latest Permian therapsids probably were equipped with hair-like integument or hairsuit. If true, this is by far the oldest evidence of this mammalian character in the stem group of mammals.

Dietary reconstruction, mobility, and the analysis of ancient skeletal tissues: Expanding the prospects of stable isotope research in archaeology

The use of stable isotope ratio analysis in archaeology has exploded over the past few decades to the point where it is now an established tool that is routinely used to investigate questions relating to diet and mobility. Early applications focused mostly on the analysis of human skeletal tissues as a way to reconstruct major shifts in human diet, but current stable isotopic approaches have expanded to include high resolution analyses of human, animal, and plant remains, which are helping to better define the resource exploitation and management strategies that underscore changes in the human diet. In addition, stable isotopic data sets are now regularly filtered through interpretive archaeological theoretical frameworks to explore socially mediated food acquisition and consumption choices, mortuary practices, and social identity. Much work remains to be done in documenting the biological and ecological variation in the distribution of stable isotopes in ancient food webs and the mechanisms responsible for the isotopic signals observed in archaeological plant and animal tissues. Here, we identify several areas in stable isotope analysis where additional ‘first principles’ driven research would help to improve existing isotopic methods, or develop new ones, and consequently improve our ability to answer questions of archaeological significance. We consider the strengths and limitations of the application of stable isotope analysis to ancient skeletal material obtained from archaeological contexts. We also pay particular attention to nitrogen isotopic variation in ancient ecosystems, organic oxygen and hydrogen isotopes to;mixing models as a means of estimating source contributions in human diet, mobility, and isoscapes; and to how compound specific analyses may help detangle dietary routing. We conclude with a plea for greater scientific rigour and more informed use of stable isotope analyses and call for a closer integration of stable isotope analysis with other aspects of archaeological research programmes, in order to optimise the information that isotopes can provide.

Modern Lessons from Ancient Food Webs

Modern Lessons from Ancient Food Webs

The impact of 850,000 years of climate changes on the structure and dynamics of mammal food webs.

Most evidence of climate change impacts on food webs comes from modern studies and little is known about how ancient food webs have responded to climate changes in the past. Here, we integrate fossil evidence from 71 fossil sites, body-size relationships and actualism to reconstruct food webs for six large mammal communities that inhabited the Iberian Peninsula at different times during the Quaternary. We quantify the long-term dynamics of these food webs and study how their structure changed across the Quaternary, a period for which fossil data and climate changes are well known. Extinction, immigration and turnover rates were correlated with climate changes in the last 850 kyr. Yet, we find differences in the dynamics and structural properties of Pleistocene versus Holocene mammal communities that are not associated with glacial-interglacial cycles. Although all Quaternary mammal food webs were highly nested and robust to secondary extinctions, general food web properties changed in the Holocene. These results highlight the ability of communities to re-organize with the arrival of phylogenetically similar species without major structural changes, and the impact of climate change and super-generalist species (humans) on Iberian Holocene mammal communities.

Longer and Less Overlapping Food Webs in Anthropogenically Disturbed Marine Ecosystems: Confirmations from the Past

The human exploitation of marine resources is characterised by the preferential removal of the largest species. Although this is expected to modify the structure of food webs, we have a relatively poor understanding of the potential consequences of such alteration. Here, we take advantage of a collection of ancient consumer tissues, using stable isotope analysis and SIBER to assess changes in the structure of coastal marine food webs in the South-western Atlantic through the second half of the Holocene as a result of the sequential exploitation of marine resources by hunter-gatherers, western sealers and modern fishermen. Samples were collected from shell middens and museums. Shells of both modern and archaeological intertidal herbivorous molluscs were used to reconstruct changes in the stable isotopic baseline, while modern and archaeological bones of the South American sea lion Otaria flavescens, South American fur seal Arctocephalus australis and Magellanic penguin Spheniscus magellanicus were used to analyse changes in the structure of the community of top predators. We found that ancient food webs were shorter, more redundant and more overlapping than current ones, both in northern-central Patagonia and southern Patagonia. These surprising results may be best explained by the huge impact of western sealing on pinnipeds during the fur trade period, rather than the impact of fishing on fish populations. As a consequence, the populations of pinnipeds at the end of the sealing period were likely well below the ecosystem's carrying capacity, which resulted in a release of intraspecific competition and a shift towards larger and higher trophic level prey. This in turn led to longer and less overlapping food webs.

Understanding specifics in generalist diets of carnivorans by analyzing stable carbon isotope values in Pleistocene mammals of Florida

Within ancient ecosystems, it is generally difficult to determine the specific diets of species from higher trophic levels, which in turn hinders our understanding of trophic relationships and energy flow through these systems. To better understand the ecology of taxa at higher trophic levels, we used analysis of tooth enamel stable carbon isotope values to infer the dietary preferences ofCanis edwardiiandSmilodon gracilisfrom the Leisey Shell Pit 1A (LSP 1A) and Inglis 1A, two Pleistocene localities in Florida. The goals of the analyses were to (1) determine whether these carnivorans specialized in particular prey types or maintained a generalist diet; (2) ascertain whether carbon isotope values support what was previously suggested about the ecology of these species; and (3) establish what ecological details of ancient food webs can be discovered by carbon isotope analyses at higher trophic levels. Results show that the sampled carnivoran carbon isotope values are distributed among suspected prey isotope values, suggesting that varied prey were taken at the study localities. Prey compositions were modeled for each carnivoran species by using Stable Isotope Analysis in R (SIAR). The modeled diets indicate that each studied carnivoran had a generalist diet; however, there are differences in how these taxa achieved dietary generalization. At the glacial Inglis 1A locality, sampled individuals ofC. edwardiiandS. gracilisshow similar isotope values and modeled dietary prey proportions, although both carnivorans do show a preference for grazing prey species. The similar isotopic values, and calculated prey proportions, observed between these species may imply greater interspecific competition for food. At the interglacial LSP 1A locality,C. edwardiishows values similar to those observed at Inglis 1A. In contrast, the data forS. gracilisshows a preference for consuming browsing prey species. Further, its restricted range of carbon isotope values suggests thatS. gracilismay have concentrated its feeding within a particular habitat. Examination of stable carbon isotope values among species at higher trophic levels reveals that some intricacies of ancient food webs can be discerned.

Refinement of reconstructed ancient food webs based on the nitrogen isotopic compositions of amino acids from bone collagen: A case study of archaeological herbivores from Tell Ain el-Kerkh, Syria

We determined the stable nitrogen isotopic composition (δ 15 N) of amino acids in bone collagen from samples of three archaeological herbivores (cattle, sheep, and goats), collected from the Tell Ain el-Kerkh Neolithic site in Syria. Bulk collagen δ 15 N values exhibited significant differences between the three species (by up to 3.2‰), and were strongly correlated with those of glycine (R 2 = 0.87), the most abundant amino acid in bone collagen. On the other hand, the δ 15 N values of two other minor amino acids (glutamic acid and phenylalanine) in the different samples were within narrow ranges (0.9‰ and 0.5‰, respectively), and exhibited either weak or no correlation with those of bulk collagen. The trophic position estimated by the δ 15 N values of glutamic acid and phenylalanine (2.0 ± 0.1) is consistent with that of herbivores. These results suggest that the δ 15 N values of bulk bone collagen may vary among herbivores, partly on account of their differing amino acid compositions, whereas the trophic position of different herbivores is faithfully preserved in the δ 15 N values of glutamic acid and phenylalanine.

Reconstruction of an Aquatic Food Web: Viking Haithabu vs. Medieval Schleswig

In the last two decades, the analysis of stable isotopes of carbonate and collagen from archaeological bone finds became a useful tool in the reconstruction of ancient food webs. Nevertheless there is still only little information available about aquatic food webs, in particular concerning brackish water ecosystems. The Schlei Fjord in Schleswig-Holstein, Germany, is such an ecosystem and was investigated to determine stable isotopic values for nitrogen, carbon and oxygen from bone collagen and carbonate in archaeological bone finds. Wild birds, mammals and fish bones from the Viking settlement Haithabu and the medieval town of Schleswig have been analyzed in this study to determine stable isotope values for marine and limnic species and to investigate possible isotopic gradients for mixing fresh water and salt water ecosystems.

Are calcium isotopes a reliable monitor of trophic level in marine settings?

AbstractRecent research has shown that calcium isotopes are fractionated by metabolic processes, leading to a decrease in 44Ca/40Ca ratio with increasing trophic level. If so, calcium isotopes could provide information on trophic relationships within foodwebs millions of years older than what we have been able to study thus far with alternative methods (i.e., nitrogen isotopes (δ15N), Sr/Ca). To explore whether δ44Ca values provided marine trophic level information, we measured the δ44Ca composition of tooth enamel and bone from modern marine mammals representing a 2.5 order range in trophic level. Marine mammal enamel δ44Ca values clustered into two groups—mammals foraging on vegetation or invertebrates exhibited higher δ44Ca values than those foraging on fish or other marine mammals. We next examined whether this correlation was preserved in the fossil record by examining a 15 Ma marine fauna from southern California and observed that the relationship between δ44Ca values of specimens followed the same pattern as observed in modern faunas, but the mean δ44Ca values were significantly different from modern δ44Ca values for mammals of similar trophic level. We conclude that the relative spacing of δ44Ca values amongst fossil taxa can serve as a valuable tool for defining trophic level of extinct organisms and can provide critical information on relationships within ancient foodwebs. Copyright © 2003 John Wiley & Sons, Ltd.