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Intestinal parasites in the Neolithic population who built Stonehenge (Durrington Walls, 2500 BCE)

Published online by Cambridge University Press:  20 May 2022

Piers D. Mitchell*
Affiliation:
Department of Archaeology, University of Cambridge, Henry Wellcome Building, Cambridge CB2 1QH, UK
Evilena Anastasiou
Affiliation:
Department of Archaeology, University of Cambridge, Henry Wellcome Building, Cambridge CB2 1QH, UK
Helen L. Whelton
Affiliation:
Organic Geochemistry Unit, School of Chemistry, University of Bristol, Cantock's Close, Bristol BS8 1TS, UK
Ian D. Bull
Affiliation:
Organic Geochemistry Unit, School of Chemistry, University of Bristol, Cantock's Close, Bristol BS8 1TS, UK
Mike Parker Pearson
Affiliation:
Institute of Archaeology, UCL, 31-34 Gordon Square, London WC1H 0PY, UK
Lisa-Marie Shillito
Affiliation:
School of History, Classics and Archaeology, Newcastle University, Newcastle upon Tyne NE1 7RU, UK
*
Author for correspondence: Piers D. Mitchell, E-mail: pdm39@cam.ac.uk

Abstract

Durrington Walls was a large Neolithic settlement in Britain dating around 2500 BCE, located very close to Stonehenge and likely to be the campsite where its builders lived during its main stage of construction. Nineteen coprolites recovered from a midden and associated pits at Durrington Walls were analysed for intestinal parasite eggs using digital light microscopy. Five (26%) contained helminth eggs, 1 with those of fish tapeworm (likely Dibothriocephalus dendriticus) and 4 with those of capillariid nematodes. Analyses of bile acid and sterol from these 5 coprolites show 1 to be of likely human origin and the other 4 to likely derive from dogs. The presence of fish tapeworm reveals that the Neolithic people who gathered to feast at Durrington Walls were at risk of infection from eating raw or undercooked freshwater fish. When the eggs of capillariids are found in the feces of humans or dogs it normally indicates that the internal organs (liver, lung or intestines) of animals with capillariasis have been eaten, and eggs passed through the gut without causing disease. Their presence in multiple coprolites provides new evidence that internal organs of animals were consumed. These novel findings improve our understanding of both parasitic infection and dietary habits associated with this key Neolithic ceremonial site.

Type
Research Article
Creative Commons
Creative Common License - CCCreative Common License - BY
This is an Open Access article, distributed under the terms of the Creative Commons Attribution licence (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted re-use, distribution and reproduction, provided the original article is properly cited.
Copyright
Copyright © The Author(s), 2022. Published by Cambridge University Press

Introduction

Durrington Walls is a large Neolithic henge located just 2.8 km from Stonehenge, Wiltshire (UK) (Fig. 1). Prior to its construction as a henge, it was the site of a large settlement estimated to start in 2535–2475 cal BCE (95% probability) and in use for 0–55 years (95% probability), possibly for no more than a decade (Parker Pearson et al., Reference Parker Pearson, Pollard, Richards, Thomas and Welham2015: 51). Its period of occupation broadly coincides with the construction of Stonehenge's sarsen circle and trilithons, suggesting that this was the builders' village for Stonehenge stage 2 (Parker Pearson et al., Reference Parker Pearson, Cleal, Marshall, Needham, Pollard, Richards, Ruggles, Sheridan, Thomas, Tilley, Welham, Chamberlain, Chenery, Evans, Knüsel, Linford, Martin, Montgomery, Payne and Richards2007, Reference Parker Pearson, Pollard, Richards, Thomas, Tilley and Welham2020: 169–171). Analysis of animal bone and food residues in pottery from Durrington Walls shows that it was a place of feasting, especially during the winter months (Albarella and Serjeantson, Reference Albarella, Serjeantson, Miracle and Milner2002; Wright et al., Reference Wright, Viner-Daniels, Parker Pearson and Albarella2014; Craig et al., Reference Craig, Shillito, Albarella, Viner-Daniels, Chan, Cleal, Ixer, Jay, Marshall, Simmons, Wright and Parker Pearson2015; Chan et al., Reference Chan, Viner, Parker Pearson, Albarella, Ixer, Leary and Kador2016).

Fig. 1. Map indicating location of the Durrington Walls and Stonehenge.

Only a very limited amount is known about parasite infection in the prehistoric population of Britain up to the Neolithic (Mitchell, Reference Mitchell2013; Anastasiou, Reference Anastasiou and Mitchell2015). In the Mesolithic layers of peat at Goldcliff in South Wales (5840–5620 BCE) whipworm eggs were recovered, which may have come from humans (Trichuris trichiura) or pigs (Trichuris suis) (Dark, Reference Dark2004). We have no data at all for parasites affecting people in Neolithic Britain. This is in contrast to the quite extensive research undertaken in the rest of Europe at the well preserved Neolithic alpine lakeside settlements in France, Germany and Switzerland (Bouchet et al., Reference Bouchet, Petrequin, Paicheler and Dommelier1995; Dommelier et al., Reference Dommelier, Bentrad, Bouchet, Paicheler and Pétrequin1998; Le Bailly et al., Reference Le Bailly, Leuzinger, Schlichtherle and Bouchet2005, Reference Le Bailly, Leuzinger, Schlichtherle and Bouchet2007; Maicher et al., Reference Maicher, Bleicher and Le Bailly2019), Spain (Maicher et al., Reference Maicher, Hoffmann, Côté, Palomo Pérez, Saña Segui and Le Bailly2017) and also Mesolithic Sweden (Bergman, Reference Bergman2018) and Ireland (Perri et al., Reference Perri, Power, Stuijts, Heinrich, Talamo, Hamilton-Dyer and Roberts2018). Clearly research investigating parasites at Neolithic sites in Britain is needed.

The aim of this study is to investigate firstly whether those humans and animals living at the Neolithic settlement of Durrington Walls were infected by parasites, and secondly whether we can detect the eggs of non-infective parasites that help us to better understand the diet and food behaviours of the population. Since the Stonehenge environs are one of the most thoroughly investigated regions of prehistoric Britain, this contributes to a growing corpus of evidence and knowledge about Neolithic lifeways.

Materials and methods

Durrington Walls

The settlement of Durrington Walls (and the adjacent site of Woodhenge) is located 2.8 km northeast of Stonehenge. The 2 sites were formerly linked by the river Avon, from which one avenue leads to Stonehenge and the other to Durrington Walls (Parker Pearson et al., Reference Parker Pearson, Cleal, Marshall, Needham, Pollard, Richards, Ruggles, Sheridan, Thomas, Tilley, Welham, Chamberlain, Chenery, Evans, Knüsel, Linford, Martin, Montgomery, Payne and Richards2007, Reference Parker Pearson, Pollard, Richards, Thomas, Tilley and Welham2020: 409–497; French et al., Reference French, Scaife, Allen, Parker Pearson, Pollard, Richards, Thomas and Welham2012). Excavations outside the east entrance of Durrington Walls by the Stonehenge Riverside project in 2004–2007 uncovered 7 house floors, substantial midden deposits and over 100 pits. The main midden, shared by 6 of the houses, contained a large assemblage of Grooved Ware pottery, worked stone tools and over 38 000 animal bones, all associated with feasting activities. Some 90% of the bones come from pigs, with less than 10% from cattle. The majority of the pigs was killed at around 9 months of age, consistent with farrowing in spring and slaughter in winter (Wright et al., Reference Wright, Viner-Daniels, Parker Pearson and Albarella2014). Isotopic analysis indicates the livestock were brought to the site from many different regions of southern Britain, providing a proxy for the catchment from which the people themselves derived (Viner et al., Reference Viner, Evans, Albarella and Parker Pearson2010; Evans et al., Reference Evans, Parker Pearson, Madgwick, Sloane and Albarella2019; Madgwick et al., Reference Madgwick, Lamb, Sloane, Nederbragt, Albarella, Parker Pearson and Evans2019, Reference Madgwick, Lamb, Sloane, Nederbragt, Albarella, Parker Pearson and Evans2021).

Some of the pits contained coprolites (Fig. 2). These are partially mineralized ancient fecal material, the size and morphology of which indicate they likely come from omnivores and not herbivores. Identifying the species of coprolite on the basis of morphology is difficult, and this varies substantially depending on the age, diet and health of an individual (Shillito et al., Reference Shillito, Blong, Green and Van Asperen2020a). However, biomolecular methods can provide a more conclusive indication of species, and have been used to distinguish between different mammals at archaeological sites (Harrault et al., Reference Harrault, Milek, Jardé, Jeanneau, Derrien and Anderson2019; Romaniuk et al., Reference Romaniuk, Panciroli, Buckley, Chowdhury, Willars, Herman, Troalen, Shepherd, Clarke, Sheridan, van Dongen, Butler and Bendrey2020; Shillito et al., Reference Shillito, Whelton, Blong, Jenkins, Connolly and Bull2020b).

Fig. 2. Fragments of the human coprolite DW11465.

Microscopy

Nineteen coprolites from the midden area were available for analysis. Sample preparation and analysis was undertaken in the Ancient Parasites Laboratory at the University of Cambridge using our routine methodology (Anastasiou and Mitchell, Reference Anastasiou and Mitchell2013). A 1 g subsample of each coprolite was disaggregated (made into a liquid suspension) by adding 5 mL 0.5% trisodium phosphate to the subsample. Material within the size range of interest was isolated from the disaggregate using stacked microsieves with mesh measuring 300, 160 and 20 μm. The material trapped on the 20 μm sieve was washed free of the mesh. This would contain any helminth eggs present, as the typical size range of eggs from helminths in northern Europe is 20–150 μm (Garcia, Reference Garcia2016: 1233). The suspension was centrifuged at 4000 rpm (3100 g) for 5 min, and the supernatant then removed. The remaining pellet was mixed with glycerol and the entire subsample was viewed on a digital light microscope (Olympus BX40F microscope with GXCAM-9 digital camera) at 400× magnification to visualize any preserved parasite eggs.

Fecal biomarker analysis

Those coprolites found to contain parasite eggs underwent further investigation to determine if the feces originated from humans or other animals that produce similar shaped feces, such as dogs. The use of fecal lipid biomarkers is a well-established method for determining coprolite species of origin (Bull et al., Reference Bull, Lockheart, Elhmmali, Roberts and Evershed2002; Shillito et al., Reference Shillito, Bull, Matthews, Almond, Williams and Evershed2011; Harrault et al., Reference Harrault, Milek, Jardé, Jeanneau, Derrien and Anderson2019; Shillito et al., Reference Shillito, Whelton, Blong, Jenkins, Connolly and Bull2020b) and identifying the presence of human and animal fecal waste in archaeological sediments (Brown et al., Reference Brown, Van Hardenbroek, Fonville, Davies, Mackay, Murray, Head, Barratt, McCormick, Ficetola, Gielly, Henderson, Crone, Cavers, Langdon, Whitehouse, Pirrie and Alsos2021). Approximately, 0.5 g of the coprolite was crushed using a mortar and pestle, then passed through a 2 mm sieve. Suitable amounts of two internal standards (hyocholic acid and preg-5-en-3β-ol; 50 μL, 0.1 mg mL−1 solution) were added to the powdered samples. The lipids were then microwave extracted using an Ethos EX microwave-assisted extraction system [10 min ramp to 70°C (1000 W), 10 min hold at 70°C (1000 W) and 20 min cool down] using 10 mL of 2:1 DCM/MeOH (v/v). The total lipid extract (TLE) obtained was subsequently hydrolysed and the sterol and bile acid fractions were isolated as outlined in Elhmmali et al. (Reference Elhmmali, Roberts and Evershed1997) and Bull et al. (Reference Bull, Simpson, Dockrill and Evershed1999). The fractions containing the target biomarkers were then analysed by gas chromatography and gas chromatography-mass spectrometry. Each of the coprolites yielded lipid profiles adequate for source identification. Four of the 5 coprolites analysed (DW248.614, DW082.1, DW248.616.1 and DW12164) were identified as likely dog in origin, and 1 coprolite was identified as likely human in origin (DW11465) (Fig. 3) by comparing with established values for each species (Wildgrube et al., Reference Wildgrube, Stockhausen, Petri, Füssel and Lauer1986; Leeming et al., Reference Leeming, Ball, Ashbolt and Nichols1996; Elhmmali et al., Reference Elhmmali, Roberts and Evershed1997; Bull et al., Reference Bull, Lockheart, Elhmmali, Roberts and Evershed2002; Prost et al., Reference Prost, Birk, Lehndorff, Gerlach and Amelung2017).

Fig. 3. Partial gas chromatograms illustrating the distribution of steroid compounds in (A) human (DW11465) and (B) carnivore (DW082.1) coprolites, where ● denotes n-alcohols, and their corresponding bile acids in (C) human (DW11465) and (D) carnivore (DW082.1), where ■ denotes hydroxy fatty acid methyl esters (TMS derivatives) and ⧫ denotes ω-hydroxy fatty acid methyl esters (TMS derivatives). IS denotes added internal standards: Preg-5-en-3β-ol is the sterol standard and hyocholic acid is the standard for bile acids.

Results

Five of the 19 coprolites contained parasite eggs. One likely dog coprolite (DW248.616.1) contained the eggs of fish tapeworm (Fig. 4). These each had a smooth opercular outline without opercular shoulders. Egg size ranged from 52 to 56 μm × 35 to 42 μm. These characteristics would be compatible with Dibothriocephalus sp. (also known as Diphyllobothrium sp.). Four other coprolites contained capillariid eggs, identified by their lemon-shape, network-like surface pattern, and dimensions of 50–56 μm × 30–31 μm (Fig. 5). One of these coprolites was of likely human origin (DW11465) and the other 3 from dogs (DW082.1, DW248.614 and DW12164). One coprolite contained 4 capillariid eggs, and the other 3 each contained 1 egg. The surface pattern was the same for all the capillariids identified, suggesting they were of the same species. Dimensions are detailed in Table 1.

Fig. 4. Fish tapeworm (likely Dibothriocephalus dendriticus) eggs from coprolite DW248.616.1 at Durrington Walls: (A) egg with operculum intact, dimensions 56 × 40 μm2; (B) operculum lost, dimensions 56 × 42 μm2. Scale bar indicates 20 μm.

Fig. 5. Capillariid egg from coprolite DW12164 at Durrington Walls. Images (A) and (B) are from the same egg; the surface structure of the egg is visible highlighting the network-like pattern on the surface (B). Scale bars indicate 20 μm.

Table 1. Details of the fish tapeworm and capillariid eggs found in the coprolites

Discussion

Species identification

Today the species of fish tapeworm found in freshwater fish in northern Europe are Dibothriocephalus dendriticus and Dibothriocephalus latus (Chappell and Owen, Reference Chappell and Owen1969; Scholz et al., Reference Scholz, Garcia, Kuchta and Wicht2009; Brewster, Reference Brewster2016). Therefore it would be reasonable to investigate whether these eggs are compatible with either of those species. Research comparing the egg dimensions of different species of fish tapeworm has found that the typical size of D. dendriticus eggs range from 53 to 66 μm in length to 38 to 45 μm in width, while those of D. latus range from 60 to 81 μm × 40 to 58 μm (Leštinová et al., Reference Leštinová, Soldánová, Scholz and Kuchta2016). Since our eggs have dimensions of 52–56 μm × 35–42 μm, they would be most compatible with D. dendriticus. However, the ancient nature of these eggs means that over time their size might potentially have changed, so there will be a greater level of uncertainty regarding the species compared with if these had been modern samples.

A considerable number of parasitic helminths in the Capillariidae family is found in modern Europe. While dimensions and eggshell surface structure can help differentiate subgroups, few have eggs that possess sufficiently distinctive morphological appearance on the microscope for reliable diagnosis to the species level (Bouchet, Reference Bouchet1997; Fugassa et al., Reference Fugassa, Taglioretti, Gonçalves, Araújo, Sardella and Denegri2008; Borba et al., Reference Borba, Machado-Silva, Le Bailly and Mayo Iñiguez2019). They predominantly infect animals, but some may occasionally infect humans. Today the species most commonly found to infect humans is Capillaria hepatica. While infection results in eggs in the liver, it does not result in eggs being found in the human stool. If eggs of C. hepatica are found in the human stool it typically results from spurious infection (false parasitism), when raw or undercooked liver is eaten and the eggs contained are released following digestion of the liver tissue (Garcia, Reference Garcia2016: 209). Bearing in mind the surface network-like pattern and the dimensions, our images share some characteristics with the capillariid Aonchotheca bovis, which infects cattle (Justine and Ferte, Reference Justine and Fertú1988). Since we know that cattle were slaughtered and eaten at the site, it is plausible to suggest that the capillariid eggs found in 4 of the coprolites got there when humans and their dogs ate the internal organs of infected animals such as cattle in the preceding days.

Prehistoric lifeways revealed through parasite remains

Here we have found evidence for parasite eggs in the preserved feces of humans and their dogs that gathered at Durrington Walls around 4500 years ago. Not only is this a key discovery due to the important nature of the site, but this is the earliest evidence for parasite infection in Britain where we can be confident of the species of the hosts. Previous research has found whipworm eggs (Trichuris sp.) in peat layers in South Wales dating to around 5840–5620 BC (Mesolithic period), but it is unknown whether they were from human or pig infection (Dark, Reference Dark2004). In humans, roundworm (Ascaris sp.) and whipworm eggs were found at a Bronze Age farming settlement at Brean Down in Somerset (2100–600 BC) (Jones, Reference Jones and Bell1990), while eggs of fish tapeworm (D. dendriticus and D. latus), Echinostoma sp., giant kidney worm (Dioctophyma renale), Capillaria sp. and probable pig whipworm (T. suis) were recovered from human coprolites at the marsh dwelling settlement at Must Farm in the fens of East Anglia (800–900 BC) (Ledger et al., Reference Ledger, Grimshaw, Fairey, Whelton, Bull, Ballantyne, Knight and Mitchell2019b). The contrasting species of parasite found at these two Bronze Age sites highlights how prehistoric lifestyle was key for explaining the profile of parasites that we might find in a population. This contrast has been found in Mesolithic and Neolithic sites in other regions of Europe as well, with populations living in lakeside villages often having more zoonotic species, and a broader range of species, than those who farmed crops and herded animals in dryer regions (Le Bailly et al., Reference Le Bailly, Leuzinger, Schlichtherle and Bouchet2007; Anastasiou, Reference Anastasiou and Mitchell2015; Maicher et al., Reference Maicher, Hoffmann, Côté, Palomo Pérez, Saña Segui and Le Bailly2017; Anastasiou et al., Reference Anastasiou, Papathanasiou, Schepartz and Mitchell2018; Ledger and Mitchell, Reference Ledger and Mitchell2019). Over time we also see a gradual change from the Neolithic pattern of both zoonotic parasites and geohelminths such as roundworm and whipworm, to the later dominance of geohelminths and sometimes disappearance of zoonoses at some sites where they previously existed (Reinhard et al., Reference Reinhard, Ferreira, Bouchet, Sianto, Dutra, Iniguez, Leles, Le Bailly, Fugassa, Pucu and Araújo2013).

The presence of fish tapeworm eggs in 1 of the 19 coprolites suggests that the dog that deposited this piece of feces had previously eaten raw or undercooked freshwater fish and contracted fish tapeworm. This adds to our growing knowledge of parasites in Neolithic dogs (Tolar and Galik, Reference Tolar and Galik2019; Tolar et al., Reference Tolar, Galik, Le Bailly, Dufour, Caf, Toskan, Buzan, Zver, Janzekovic and Veluscek2020; Maicher et al., Reference Maicher, Maigrot, Mazurkevich, Dolbunova and Le Bailly2021). While modern infection would lead to a high number of eggs in the feces, in ancient coprolites recovered from middens it is not uncommon for egg counts to be low, likely due to destruction of the eggs by fungi and insects over the centuries (see Ledger et al., Reference Ledger, Anastasiou, Shillito, Mackay, Bull, Haddow, Knusel and Mitchell2019a for similar egg counts at a comparable Neolithic site). Since only 1 of the 19 coprolites contained fish tapeworm eggs, this would suggest either that infection was not common at the site, or that some helminth eggs originally present in other coprolites did not survive the 4500 years in the ground. This contrasts with the Bronze Age marshland settlement of Must Farm, where every human coprolite contained the eggs of either Echinostoma sp. or Dibothriocephalus sp., from eating raw fish and other aquatic animals (Ledger et al., Reference Ledger, Grimshaw, Fairey, Whelton, Bull, Ballantyne, Knight and Mitchell2019b). It is likely that preservation has played a role here; deposits at Durrington Walls are from dryland contexts in contrast to the exceptional preservation in the waterlogged deposits of Must Farm. Fish tapeworm has been found at a number of prehistoric European sites during the Mesolithic and Neolithic, and at that time is thought to reflect the component of the diet made up by hunting and gathering wild foods (Le Bailly and Bouchet, Reference Le Bailly and Bouchet2013).

We should consider whether this dog may have contracted the fish tapeworm infection while residing at Durrington Walls, or elsewhere. Since the settlement at Durrington Walls appears to have been occupied on a largely seasonal basis, predominantly in the winter periods, it is possible that the dog had arrived already infected with the parasite. At Durrington Walls no bones of freshwater fish were recovered, despite excellent preservation of faunal remains, and there was no evidence of freshwater fish oil in the pottery analysed. This would suggest that any consumption of fish by dogs could have occurred elsewhere, in the settlements scattered across southern Britain where the people who came to Durrington Walls in the winter would have spent the rest of the year. Stable isotope analysis of collagen extracted from the few human remains found at Durrington Walls (Craig et al., Reference Craig, Shillito, Albarella, Viner-Daniels, Chan, Cleal, Ixer, Jay, Marshall, Simmons, Wright and Parker Pearson2015) does not rule out the consumption of freshwater fish over several years prior to death, but if so this was likely to have been away from the site.

The capillariid eggs found in 1 human and 3 dog coprolites do not indicate infection, but rather reflects the consumption of the internal organs of animals. If the liver or lungs of animals were eaten without being thoroughly cooked, then the capillariid eggs they contained could have passed through the intestinal tract and end up in the feces due to spurious infection (false parasitism). These findings emphasize the importance of coprolites in providing evidence for consumption of items that are not visible through other lines of evidence (Blong et al., Reference Blong, Adams, Sanchez, Jenkins, Bull and Shillito2020; Shillito et al., Reference Shillito, Blong, Green and Van Asperen2020a). Earlier archaeological research on animal bone and pottery residues undertaken at Durrington Walls indicates that feasts were held at the site involving large numbers of people and animals who travelled to the area, likely part of seasonal gatherings and ceremonies associated with Stonehenge and its surrounding monuments (Craig et al., Reference Craig, Shillito, Albarella, Viner-Daniels, Chan, Cleal, Ixer, Jay, Marshall, Simmons, Wright and Parker Pearson2015; Evans et al., Reference Evans, Parker Pearson, Madgwick, Sloane and Albarella2019; Madgwick et al., Reference Madgwick, Lamb, Sloane, Nederbragt, Albarella, Parker Pearson and Evans2019, Reference Madgwick, Lamb, Sloane, Nederbragt, Albarella, Parker Pearson and Evans2021), and show that principally pork and beef were consumed (Albarella and Serjeantson, Reference Albarella, Serjeantson, Miracle and Milner2002; Wright et al., Reference Wright, Viner-Daniels, Parker Pearson and Albarella2014). While compound specific isotope analysis of C16:0 and C18:0 fatty acids in pottery can distinguish between carcases and dairy fats, they cannot distinguish fats from organs compared to other parts of the animal carcases. It is also possible that residues in pottery may relate to storage of materials for craft purposes rather than food preparation (Shillito, Reference Shillito2019). Coprolites on the other hand, contain items that were unequivocally ingested by an individual. It is possible that the capillariid eggs in these coprolites could have been consumed by the people living at Durrington Walls when they ate the internal organs of cattle during these feasts. The left overs may then have been fed to their dogs, explaining the capillariid eggs in their coprolites.

Conclusion

Here we have investigated fecal remains of humans and dogs that gathered at the large settlement of Durrington Walls during the Late Neolithic period. Using bile acid and sterol analysis we were able to determine the likely species of origin of each coprolite that contained parasite eggs. One coprolite from a dog contained the eggs of fish tapeworm, indicating it had likely eaten raw or undercooked fish and contracted the parasite. This is intriguing as there is very little other evidence of fishing (marine or fresh water) during the British Late Neolithic period. Four coprolites contained the eggs of Capillariidae nematodes, most probably indicating that both humans and dogs had eaten the internal organs of animals infected by this parasite. These results provide a new line of evidence for the consumption of animal organs, which has not been possible using more traditional forms of archaeological evidence.

Acknowledgements

The Stonehenge Riverside project that excavated the coprolite samples was funded by the AHRC (grant AH/H000879/1). The authors are grateful to Dr Matt Le Bailly for his opinion on the potential species of the capillariid eggs.

Author contributions

P. M. and L.-M. S. conceived and designed the study. E. A. and P. M. performed the microscopy analysis. H. W., I. B. and L.-M. S. analysed the bile acids and sterols. M. P. P. excavated the site where the coprolites were found. P. M. wrote the article, with E. A., H. W., I. B., M. P. P. and L.-M. S. contributing to the paper.

Conflict of interest

The authors declare there are no conflicts of interest.

Ethical standards

Not applicable – the study did not involve research on live animals.

References

Albarella, U and Serjeantson, D (2002) A passion for pork: meat consumption at the British Late Neolithic site of Durrington Walls. In Miracle, P and Milner, N (eds), Consuming Passions and Patterns of Consumption. Cambridge: Cambridge University Press, pp. 3349.Google Scholar
Anastasiou, E (2015) Parasites in European populations from prehistory to the industrial revolution. In Mitchell, PD (ed.), Sanitation, Latrines and Intestinal Parasites in Past Populations. Farnham: Ashgate, pp. 203217.Google Scholar
Anastasiou, E and Mitchell, PD (2013) Simplifying the process for extracting parasitic worm eggs from cesspool and latrine sediments: a trial comparing the efficacy of widely used techniques for disaggregation. International Journal of Paleopathology 3, 204207.CrossRefGoogle Scholar
Anastasiou, E, Papathanasiou, A, Schepartz, LA and Mitchell, PD (2018) Infectious disease in the ancient Aegean: intestinal parasitic worms in the Neolithic to Roman period inhabitants of Kea, Greece. Journal of Archaeological Science Reports 17, 860864.CrossRefGoogle Scholar
Bergman, J (2018) Stone age disease in the north – human intestinal parasites from a Mesolithic burial in Motala, Sweden. Journal of Archaeological Science 96, 2632.CrossRefGoogle Scholar
Blong, JC, Adams, ME, Sanchez, G, Jenkins, DL, Bull, ID and Shillito, L-M (2020) Younger Dryas and early Holocene subsistence in the northern great basin: multiproxy analysis of coprolites from the Paisley Caves, Oregon, USA. Archaeological and Anthropological Sciences 12, 224.CrossRefGoogle Scholar
Borba, VH, Machado-Silva, JR, Le Bailly, M and Mayo Iñiguez, A (2019) Worldwide paleodistribution of capillariid parasites: paleoparasitology, current status of phylogeny and taxonomic perspectives. PLoS ONE 14, e0216150.CrossRefGoogle ScholarPubMed
Bouchet, F (1997) Intestinal capillariasis in Neolithic inhabitants of Chalain (Jura, France). The Lancet 349, 256.CrossRefGoogle Scholar
Bouchet, F, Petrequin, P, Paicheler, JC and Dommelier, S (1995) Première approche paléoparasitogique du site Néolithique de Chalain (Jura, France). Bulletin de la Société de Pathologie Exotique 88, 265268.Google Scholar
Brewster, B (2016) Aquatic Parasite Information: A Database on Parasites of Freshwater and Brackish Fish in the United Kingdom (PhD thesis). Kingston University London, London, UK.Google Scholar
Brown, AG, Van Hardenbroek, M, Fonville, T, Davies, K, Mackay, H, Murray, E, Head, K, Barratt, P, McCormick, F, Ficetola, GF, Gielly, L, Henderson, ACG, Crone, A, Cavers, G, Langdon, PG, Whitehouse, NJ, Pirrie, D and Alsos, IG (2021) Ancient DNA, lipid biomarkers and palaeoecological evidence reveals construction and life on early medieval lake settlements. Scientific Reports 11, 11807.CrossRefGoogle ScholarPubMed
Bull, ID, Simpson, IA, Dockrill, SJ and Evershed, RP (1999) Organic geochemical evidence for the origin of ancient anthropogenic soil deposits at Tofts Ness, Sanday, Orkney. Organic Geochemistry 30, 535556.CrossRefGoogle Scholar
Bull, ID, Lockheart, MJ, Elhmmali, MM, Roberts, DJ and Evershed, RP (2002) The origin of faeces by means of biomarker detection. Environment International 27, 647654.CrossRefGoogle ScholarPubMed
Chan, B, Viner, S, Parker Pearson, M, Albarella, U and Ixer, R (2016) Resourcing Stonehenge: patterns of human, animal and goods mobility in the Late Neolithic. In Leary, J and Kador, T (eds), Moving On in Neolithic Studies: Understanding Mobile Lives. Oxford: Oxbow, pp. 2844.Google Scholar
Chappell, LH and Owen, RW (1969) A reference list of parasite species recorded in freshwater fish from Great Britain and Ireland. Journal of Natural History 3, 197216.CrossRefGoogle Scholar
Craig, OE, Shillito, L-M, Albarella, U, Viner-Daniels, S, Chan, B, Cleal, R, Ixer, R, Jay, M, Marshall, P, Simmons, E, Wright, E and Parker Pearson, M (2015) Feeding Stonehenge: cuisine and consumption at the Late Neolithic site of Durrington Walls. Antiquity 89, 10961109.CrossRefGoogle Scholar
Dark, P (2004) New evidence for the antiquity of the intestinal parasite Trichuris (whipworm) in Europe. Antiquity 78, 676681.CrossRefGoogle Scholar
Dommelier, S, Bentrad, S, Bouchet, F, Paicheler, JC and Pétrequin, P (1998) Parasitoses liées à l'alimentation chez les populations du site Néolithique de Chalain (Jura, France). Anthropozoologica 27, 4149.Google Scholar
Elhmmali, MM, Roberts, DJ and Evershed, RP (1997) Bile acids as a new class of sewage pollution indicator. Environmental Science and Technology 31, 36633668.CrossRefGoogle Scholar
Evans, J, Parker Pearson, M, Madgwick, R, Sloane, H and Albarella, U (2019) Strontium and oxygen isotope evidence for the origin and movement of cattle at Late Neolithic Durrington Walls, UK. Archaeological and Anthropological Sciences 2019, 11.Google Scholar
French, C, Scaife, R, Allen, MJ, Parker Pearson, M, Pollard, J, Richards, C, Thomas, J and Welham, K (2012) Durrington Walls to west Amesbury by way of Stonehenge: a major transformation of the Holocene landscape. The Antiquaries Journal 92, 136.CrossRefGoogle Scholar
Fugassa, MH, Taglioretti, V, Gonçalves, MLC, Araújo, A, Sardella, NH and Denegri, GM (2008) Capillaria spp. eggs in Patagonian archaeological sites: statistical analysis of morphometric data. Memorias do Instituto Oswaldo Cruz 103, 104105.CrossRefGoogle Scholar
Garcia, LS (2016) Diagnostic Medical Parasitology. Washington, DC: ASM Press.CrossRefGoogle Scholar
Harrault, L, Milek, K, Jardé, E, Jeanneau, L, Derrien, M and Anderson, DG (2019) Faecal biomarkers can distinguish specific mammalian species in modern and past environments. PLoS ONE 14, e0211119.CrossRefGoogle ScholarPubMed
Jones, AKG (1990) Coprolites and faecal concretions. In Bell, M (ed.), Brean Down: Excavations 1983–1987. London: English Heritage, pp. 242245.Google Scholar
Justine, J-L and Fertú, H (1988) Redescription de Capillaria bovis (Schnyder, 1906) (Nematoda, Capillariinae). Bulletin du Museum National d'Histoire Naturelle Section A: Zoologie Biologie et Ecologie Animales 10, 693709.Google Scholar
Le Bailly, M and Bouchet, F (2013) Diphyllobothrium in the past: review and new records. International Journal of Paleopathology 3, 182187.CrossRefGoogle ScholarPubMed
Le Bailly, M, Leuzinger, U, Schlichtherle, H and Bouchet, F (2005) Diphyllobothrium: Neolithic parasite? Journal of Parasitology 91, 957959.CrossRefGoogle ScholarPubMed
Le Bailly, M, Leuzinger, U, Schlichtherle, H and Bouchet, F (2007) ‘Crise économique’ au Néolithique à la transition Pfÿn-Horgen (3400 BC): contribution de la paléoparasitologie. Anthropozoologica 42, 175185.Google Scholar
Ledger, ML and Mitchell, PD (2019) Tracing zoonotic parasite infections throughout human evolution. International Journal of Osteoarchaeology. doi: 10.1002/oa.2786Google Scholar
Ledger, ML, Anastasiou, E, Shillito, L-M, Mackay, H, Bull, ID, Haddow, SD, Knusel, CJ and Mitchell, PD (2019a) Parasite infection at the early farming community of Çatalhöyük, Turkey (7100–6150 BC). Antiquity 93, 573587.CrossRefGoogle Scholar
Ledger, ML, Grimshaw, E, Fairey, M, Whelton, HL, Bull, ID, Ballantyne, R, Knight, M and Mitchell, PD (2019b) Intestinal parasites at the Late Bronze Age settlement of must farm, in the fens of East Anglia, UK (9th century B.C.E.). Parasitology 146, 15831594.CrossRefGoogle Scholar
Leeming, R, Ball, A, Ashbolt, N and Nichols, P (1996) Using faecal sterols from humans and animals to distinguish faecal pollution in receiving waters. Water Research 30, 28932900.CrossRefGoogle Scholar
Leštinová, K, Soldánová, M, Scholz, T and Kuchta, R (2016) Eggs as a suitable tool for species diagnosis of causative agents of human Diphyllobothriosis (Cestoda). PLoS Neglected Tropical Diseases 10, e0004721.CrossRefGoogle Scholar
Madgwick, R, Lamb, A, Sloane, H, Nederbragt, A, Albarella, U, Parker Pearson, M and Evans, J (2019) Multi-isotope analysis reveals that feasts in the Stonehenge environs and across Wessex drew people and animals from throughout Britain. Science Advances 5, eaau6078.CrossRefGoogle ScholarPubMed
Madgwick, R, Lamb, A, Sloane, H, Nederbragt, A, Albarella, U, Parker Pearson, M and Evans, J (2021) A veritable confusion: use and abuse of isotope analysis in archaeology. Archaeological Journal 178, 361385.CrossRefGoogle Scholar
Maicher, C, Hoffmann, A, Côté, NML, Palomo Pérez, A, Saña Segui, M and Le Bailly, M (2017) Paleoparasitological investigations on the Neolithic lakeside settlement of La Draga (Lake Banyoles, Spain). The Holocene 27, 16591668.CrossRefGoogle Scholar
Maicher, C, Bleicher, N and Le Bailly, M (2019) Spatializing data in paleoparasitology: application to the study of the Neolithic lakeside settlement of Zürich-Parkhaus-Opéra, Switzerland. The Holocene 29, 11981205.CrossRefGoogle Scholar
Maicher, C, Maigrot, Y, Mazurkevich, A, Dolbunova, E and Le Bailly, M (2021) First contribution of paleoparasitology to the study of coprolites from the Neolithic site Serteya II (NW Russia). Journal of Archaeological Science: Reports 38, 103093.Google Scholar
Mitchell, PD (2013) The origins of human parasites: exploring the evidence for endoparasitism throughout human evolution. International Journal of Paleopathology 3, 191198.CrossRefGoogle ScholarPubMed
Parker Pearson, M, Cleal, R, Marshall, P, Needham, S, Pollard, J, Richards, C, Ruggles, C, Sheridan, A, Thomas, J, Tilley, C, Welham, K, Chamberlain, A, Chenery, C, Evans, JA, Knüsel, C, Linford, N, Martin, L, Montgomery, J, Payne, A and Richards, M (2007) The age of Stonehenge. Antiquity 81, 617639.CrossRefGoogle Scholar
Parker Pearson, M, Pollard, J, Richards, C, Thomas, J and Welham, K (2015) Stonehenge: Making Sense of a Prehistoric Mystery. York: CBA.Google Scholar
Parker Pearson, M, Pollard, J, Richards, C, Thomas, J, Tilley, C and Welham, K (2020) Stonehenge for the Ancestors. Part 1: Landscape and Monuments. Leiden: Sidestone.Google Scholar
Perri, AR, Power, RC, Stuijts, I, Heinrich, S, Talamo, S, Hamilton-Dyer, S and Roberts, C (2018) Detecting hidden diets and disease: zoonotic parasites and fish consumption in Mesolithic Ireland. Journal of Archaeological Science 97, 137146.CrossRefGoogle Scholar
Prost, K, Birk, JJ, Lehndorff, E, Gerlach, R and Amelung, W (2017) Steroid biomarkers revisited – improved source identification of faecal remains in archaeological soil material. PLoS ONE 12, e0164882.CrossRefGoogle ScholarPubMed
Reinhard, KJ, Ferreira, LF, Bouchet, F, Sianto, L, Dutra, JMF, Iniguez, A, Leles, D, Le Bailly, M, Fugassa, M, Pucu, E and Araújo, A (2013) Food, parasites, and epidemiological transitions: a broad perspective. International Journal of Paleopathology 3, 150157.CrossRefGoogle ScholarPubMed
Romaniuk, A, Panciroli, E, Buckley, M, Chowdhury, MP, Willars, C, Herman, JS, Troalen, L, Shepherd, AN, Clarke, DV, Sheridan, A, van Dongen, BE, Butler, I and Bendrey, R (2020) Combined visual and biochemical analyses confirm depositor and diet for Neolithic coprolites from Skara Brae. Archaeological and Anthropological Sciences 12, 274.CrossRefGoogle Scholar
Scholz, T, Garcia, HH, Kuchta, R and Wicht, B (2009) Update on the human broad tapeworm (genus Diphyllobothrium), including clinical relevance. Clinical Microbiology Reviews 22, 146160.CrossRefGoogle Scholar
Shillito, L-M (2019) Building Stonehenge? An alternative interpretation of lipid residues in Grooved Ware from Durrington Walls. Antiquity 93, 10521060.CrossRefGoogle Scholar
Shillito, L-M, Bull, ID, Matthews, W, Almond, MJ, Williams, JM and Evershed, RP (2011) Biomolecular and micromorphological analysis of suspected faecal deposits at Neolithic Catalhoyuk, Turkey. Journal of Archaeological Science 38, 18691877.CrossRefGoogle Scholar
Shillito, L-M, Blong, JC, Green, EJ and Van Asperen, E (2020a) The what, how and why of archaeological coprolite analysis. Earth Science Reviews 207, 103196.CrossRefGoogle Scholar
Shillito, L-M, Whelton, HL, Blong, JC, Jenkins, DL, Connolly, TJ and Bull, ID (2020b) Pre-Clovis occupation of the Americas identified by human faecal biomarkers in coprolites from Paisley Caves, Oregon. Science Advances 6, eaba6404.CrossRefGoogle Scholar
Tolar, T and Galik, A (2019) A study of dog coprolite from Late Neolithic pile dwelling site in Slovenia. Archaeological Discovery 7, 2029.CrossRefGoogle Scholar
Tolar, T, Galik, A, Le Bailly, M, Dufour, B, Caf, N, Toskan, B, Buzan, E, Zver, L, Janzekovic, F and Veluscek, A (2020) Multi-proxy analysis of waterlogged preserved Late Neolithic canine excrements. Vegetation History and Archaeobotany 30, 107118.CrossRefGoogle Scholar
Viner, SJ, Evans, J, Albarella, U and Parker Pearson, M (2010) Cattle mobility in prehistoric Britain: strontium isotope analysis of cattle teeth from Durrington Walls (Wiltshire, UK). Journal of Archaeological Science 37, 28122820.CrossRefGoogle Scholar
Wildgrube, HJ, Stockhausen, H, Petri, J, Füssel, U and Lauer, H (1986) Naturally occurring conjugated bile acids, measured by high-performance liquid chromatography, in human, dog and rabbit bile. Journal of Chromatography 353, 207213.CrossRefGoogle ScholarPubMed
Wright, E, Viner-Daniels, S, Parker Pearson, M and Albarella, U (2014) Age and season of pig slaughter at Late Neolithic Durrington Walls (Wiltshire, UK) as detected through a new system for recording tooth wear. Journal of Archaeological Science 52, 497514.CrossRefGoogle Scholar
Figure 0

Fig. 1. Map indicating location of the Durrington Walls and Stonehenge.

Figure 1

Fig. 2. Fragments of the human coprolite DW11465.

Figure 2

Fig. 3. Partial gas chromatograms illustrating the distribution of steroid compounds in (A) human (DW11465) and (B) carnivore (DW082.1) coprolites, where ● denotes n-alcohols, and their corresponding bile acids in (C) human (DW11465) and (D) carnivore (DW082.1), where ■ denotes hydroxy fatty acid methyl esters (TMS derivatives) and ⧫ denotes ω-hydroxy fatty acid methyl esters (TMS derivatives). IS denotes added internal standards: Preg-5-en-3β-ol is the sterol standard and hyocholic acid is the standard for bile acids.

Figure 3

Fig. 4. Fish tapeworm (likely Dibothriocephalus dendriticus) eggs from coprolite DW248.616.1 at Durrington Walls: (A) egg with operculum intact, dimensions 56 × 40 μm2; (B) operculum lost, dimensions 56 × 42 μm2. Scale bar indicates 20 μm.

Figure 4

Fig. 5. Capillariid egg from coprolite DW12164 at Durrington Walls. Images (A) and (B) are from the same egg; the surface structure of the egg is visible highlighting the network-like pattern on the surface (B). Scale bars indicate 20 μm.

Figure 5

Table 1. Details of the fish tapeworm and capillariid eggs found in the coprolites