Document Detail

A chronological framework for the British Quaternary based on Bithynia opercula.
Jump to Full Text
MedLine Citation:
PMID:  21804567     Owner:  NLM     Status:  MEDLINE    
Marine and ice-core records show that the Earth has experienced a succession of glacials and interglacials during the Quaternary (last ∼2.6 million years), although it is often difficult to correlate fragmentary terrestrial records with specific cycles. Aminostratigraphy is a method potentially able to link terrestrial sequences to the marine isotope stages (MIS) of the deep-sea record. We have used new methods of extraction and analysis of amino acids, preserved within the calcitic opercula of the freshwater gastropod Bithynia, to provide the most comprehensive data set for the British Pleistocene based on a single dating technique. A total of 470 opercula from 74 sites spanning the entire Quaternary are ranked in order of relative age based on the extent of protein degradation, using aspartic acid/asparagine (Asx), glutamic acid/glutamine (Glx), serine (Ser), alanine (Ala) and valine (Val). This new aminostratigraphy is consistent with the stratigraphical relationships of stratotypes, sites with independent geochronology, biostratigraphy and terrace stratigraphy. The method corroborates the existence of four interglacial stages between the Anglian (MIS 12) and the Holocene in the terrestrial succession. It establishes human occupation of Britain in most interglacial stages after MIS 15, but supports the notion of human absence during the Last Interglacial (MIS 5e). Suspicions that the treeless 'optimum of the Upton Warren interstadial' at Isleworth pre-dates MIS 3 are confirmed. This new aminostratigraphy provides a robust framework against which climatic, biostratigraphical and archaeological models can be tested.
Kirsty E H Penkman; Richard C Preece; David R Bridgland; David H Keen; Tom Meijer; Simon A Parfitt; Tom S White; Matthew J Collins
Related Documents :
22777107 - Fate of dietary phytosteryl/-stanyl esters: analysis of individual intact esters in hum...
7279117 - Accumulation of peptides by choroid plexus in vitro: tyr-d-ala-gly as a model.
8448197 - Specificity for various imino-acid-residues of a proline-specific dipeptidylcarboxypept...
20041747 - The fate of amino acids during simulated meteoritic impact.
12509157 - Electrochemical properties and fourier transform-infrared spectroscopic investigations ...
11459807 - Saturated ffas, palmitic acid and stearic acid, induce apoptosis in human granulosa cells.
Publication Detail:
Type:  Journal Article; Research Support, Non-U.S. Gov't     Date:  2011-07-31
Journal Detail:
Title:  Nature     Volume:  476     ISSN:  1476-4687     ISO Abbreviation:  Nature     Publication Date:  2011 Aug 
Date Detail:
Created Date:  2011-08-25     Completed Date:  2011-10-06     Revised Date:  2012-02-27    
Medline Journal Info:
Nlm Unique ID:  0410462     Medline TA:  Nature     Country:  England    
Other Details:
Languages:  eng     Pagination:  446-9     Citation Subset:  IM    
BioArCh, Department of Archaeology, University of York, York YO10 5DD, UK.
Export Citation:
APA/MLA Format     Download EndNote     Download BibTex
MeSH Terms
Amino Acids / analysis
Archaeology / methods*
Chronology as Topic*
Fresh Water
Gastropoda* / chemistry,  classification
Great Britain
Proteins / chemistry
Grant Support
076905//Wellcome Trust; GR076905MA//Wellcome Trust
Reg. No./Substance:
0/Amino Acids; 0/Proteins

From MEDLINE®/PubMed®, a database of the U.S. National Library of Medicine

Full Text
Journal Information
Journal ID (nlm-journal-id): 0410462
Journal ID (pubmed-jr-id): 6011
Journal ID (nlm-ta): Nature
ISSN: 0028-0836
ISSN: 1476-4687
Article Information
Download PDF

nihms-submitted publication date: Day: 4 Month: 8 Year: 2011
Electronic publication date: Day: 31 Month: 7 Year: 2011
pmc-release publication date: Day: 25 Month: 2 Year: 2012
Volume: 476 Issue: 7361
First Page: 446 Last Page: 449
ID: 3162487
PubMed Id: 21804567
DOI: 10.1038/nature10305
ID: wtpa36013

A chronological framework for the British Quaternary based on Bithynia opercula
Kirsty E.H. Penkman1
Richard C. Preece2
David R. Bridgland3
David H. Keen4
Tom Meijer5
Simon A. Parfitt67
Tom S. White2
Matthew J. Collins1
1BioArCh, Departments of Archaeology & Chemistry, University of York, York YO10 5DD, UK
2Department of Zoology, University of Cambridge, Downing Street, Cambridge CB2 3EJ UK
3Department of Geography, University of Durham, South Road, Durham DH1 3LE
4Institute of Archaeology and Antiquity, University of Birmingham, Birmingham B15 2TT, UK
5Cainozoic Mollusca, Netherlands Centre for Biodiversity, Naturalis, P.O. Box 9517, 2300 RA Leiden, The Netherlands
6Institute of Archaeology, University College London, 31-34 Gordon Square, London WC1H 0PY, UK
7Department of Palaeontology, The Natural History Museum, Cromwell Road, London SW7 5BD, UK
Correspondence: Correspondence and requests for materials should be addressed to K.E.H.P. (
Deceased 16 April 2006

Despite the importance of the terrestrial record for climate models, the difficulties of assigning specific sedimentary sequences to individual climate cycles restricts the use of these data in climate modelling. The British Quaternary is exceptional for the number of recorded sites and their biodiversity, which has fluctuated markedly due to the mid-latitude situation of this ephemeral island. A consensus has emerged from attempted differentiation between interglacials in Britain using river terrace stratigraphy6,8 and biostratigraphy3-5 (Table 1).

This study revisits research pioneered by Miller et al. (predominantly on bivalves)1 and Bowen et al. (predominantly on gastropod shells)2 who used the extent of racemization in the amino acid L-isoleucine (to its diastereomer D-alloisoleucine, yielding an A/I value) in non-marine mollusc shells to build an aminostratigraphy of terrestrial sequences that could be linked to the marine oxygen isotope stratigraphy. Following debate concerning certain correlations, we developed a revised method of extraction and analysis9. Shells of freshwater gastropods (Bithynia and Valvata) from many of the original sites10 have been re-analysed, confirming much of the A/I stratigraphy. However, it emerged that within-site and within-stage variability increases in shells from older sites. This variability probably results from diagenetic alteration of the biomineral carbonate from aragonite to the more thermodynamically stable calcite10,11.

Our new method has five significant revisions, three of which reduced within-site variability. First, inter-species variation was minimised by analysing only a single genus of freshwater gastropod (Bithynia). Second, variability in amino acid concentration and D/L values was significantly lowered when samples were crushed to ≤ 500 μm and exposed to prolonged wet chemical oxidation (48 hours, 12% wt./vol. NaOCl, room temperature), destroying any contamination and leaving a functionally closed-system protein fraction defined as ‘intra-crystalline’9,12. Third, the calcitic operculum, which in life closes the aperture of the shell, was analysed instead of the aragonitic shell. Opercula display less within-site variation and greater stability than shells10,11, and show subtle but minimal intraspecific differences in racemization (Supplementary Data 1). Further modifications included the analysis of a range of different amino acids13 (rather than only a single measure of racemization), which allows an estimate of ‘Intra-crystalline Protein Decomposition’ (IcPD). This integrates data from amino acids with differing rates of racemization (Asx >> Ala > Val ~ Glx) with the extent of dehydration of serine ([Ser]/[Ala]) to estimate age (Fig. 1). Finally, comparisons were made between free amino acids (FAA), liberated by diagenesis, and the total extent of racemization (THAA), in order to test closed-system conditions14.

The intra-crystalline fraction maintains constant chemical conditions so that the extent of protein degradation can be attributed to the thermal history of the sample. Within the study area differences in thermal history have been minor during the past century and chiefly related to burial depth and the thermal diffusivity of the overburden, mediated by the presence/absence of vegetation and/or snow cover (Supplementary Figure 1 and Discussion). Opercula with similar levels of protein degradation are therefore thought to be of equivalent age, assuming that similarly small thermal gradients existed during past interglacials, when most of the racemization would have occurred.

The consistency of our method has been tested by measuring opercula from British interglacial stratotypes and/or sites with independent geochronology (Table 1; Fig. 1, Supplementary Data 1). All stratotypes yielding Bithynia have been analysed, but stratotypes have not been formally defined for all stages15. Sites with independent geochronology can be used to calibrate IcPD results but, as only 7 of our pre-Holocene sites have associated dates, we have not done this here. Nevertheless, an age-dependent increase in the level of IcPD is seen from the Holocene to the Early Pleistocene, using a combination of fast (e.g. Asx) and slow (e.g. Val) racemizing amino acids to span this range.

Increasing protein decomposition within opercula is also consistent with increasing river terrace elevation (and therefore age) in Quaternary fluvial archives (Table 1 and Supplementary Data 1 and 2, Figure 2). The formation of river terraces is attributed to climatic forcing and uplift, linking aggradation and incision phases with climatically induced changes in sediment and water supply6,8,16. Assemblages of amino acid values from the Thames sequence, the most complete British fluvial archive17-19, clearly correspond with discrete terrace aggradations (Fig. 2 and Supplementary Data 2). Four interglacials after the Anglian (MIS 12) stage are represented in this system, assigned to MIS 11, 9, 7 and 5e on the basis that each aggradation formed during a complete glacial/interglacial cycle6,16. Although this relationship might not hold for all rivers20, a similar pattern exists between Ala D/L values and terraces in other systems, such as the Severn/Avon21, Trent/Witham22 and Nene/Welland23. Support for these interpretations comes from integrating several lines of evidence (e.g. biostratigraphy4-5 and some of the original A/I data16), not all of which are wholly independent. However, the ability of the method to differentiate between terrace aggradations (Supplementary Data 2) is not reliant on other data and sites where the age attribution is based fundamentally on amino acid data are not assigned ‘consensus MIS ages’ in Table 1.

Bithynia is generally rare in cold-stage contexts, although it occurred commonly in the ‘Upton Warren interstadial’ deposit at Isleworth. This was originally thought to fall within the ‘Middle Devensian’ (MIS 3) on the basis of a radiocarbon date of ~43 ka BP24. The Isleworth opercula IcPD is consistently higher than from Cassington, a site tentatively correlated with MIS 5a25, but lower than Last Interglacial opercula. Radiocarbon therefore provides only a minimum age for the Isleworth deposits. Our IcPD data indicate an earlier age and suggest that this new method can potentially be used to distinguish marine isotope sub-stages beyond the limits of radiocarbon dating.

Aminostratigraphic data also provide independent support for biostratigraphic age models developed for the Middle Pleistocene5,26,27. In the early Middle Pleistocene, the water vole Arvicola is thought to have replaced its ancestor Mimomys savini within a relatively short time over large regions of Europe3,27. This hypothesis gains support from our new data, which show that opercula from sites yielding Arvicola show less protein degradation than those containing M. savini (Table 1).

The occurrence of Corbicula (a bivalve) and Hippopotamus in the British Pleistocene is mutually exclusive5,26. At British sites securely attributable to the Last Interglacial (MIS 5e) Corbicula is absent; conversely, after MIS 12, Hippopotamus is only known from the Last Interglacial, and is therefore widely regarded as an ‘indicator species’ for MIS 5e4. Our data support these conclusions, as post-Anglian sites with Hippopotamus show less protein breakdown than sites yielding Corbicula, with levels of protein degradation consistent with attribution to MIS 5e.

The comparisons above demonstrate the remarkable consistency of our new method with independent lines of evidence. This comprehensive dating framework enables us to explore the British archaeological record. Our data show that human occupation occurred within at least two distinct pre-Anglian stages, the older (Pakefield) associated with Mimomys and the younger (Waverley Wood) with Arvicola. The conclusion that Waverley Wood is younger than the Cromerian stratotype at West Runton supports the biostratigraphic age model27 and contradicts a conclusion reached in an earlier aminostratigraphical study2. Our data can provide age constraints for other archaeological assemblages, enabling attribution to specific marine isotope stages in younger deposits. The development of Levallois technology, characterized by the removal of flakes from specifically prepared cores, is unknown in Britain before MIS 928. Archaeological evidence from MIS 9 is sparse, but the far better record from sites attributed to MIS 7 shows that Levallois industries had become dominant in southern England; our data support this view (Table 1; Fig. 3).

In recent years it has become clear that humans were absent from Britain during the Last Interglacial; earlier claims to the contrary have been shown to be based on misinterpretation of archaeological sites previously thought to be of Last Interglacial age (such as Aveley, Crayford, Grays, Purfleet and Stutton), invariably now assigned to earlier stages29 (Supplementary Data 1). Our results confirm that no British archaeological site can be attributed to the Last Interglacial (Fig. 3), a conclusion consistent with human absence during this stage7,29.

This stratigraphical framework provides a secure basis for relating the British terrestrial British sequence to global Quaternary climate records. This is fundamental to geological and archaeological research but, as importantly, it enables the rich British record to be used to test the ability of climate models to simulate pre-late Quaternary palaeoclimates. This dating technique offers a means of correlating terrestrial with marine and ice-core records, thereby increasing the confidence of model predictions30. Moreover, the calcitic opercula of bithyniid (or similar) gastropods occur commonly in many Quaternary sequences, offering potential for development of regional aminostratigraphies around the world.


FN2Supplementary Information Supplementary Information is linked to the online version of the paper at

FN3Author contributions K.E.H.P., M.J.C., R.C.P. and D.H.K. designed the study. R.C.P., D.H.K., T.M., D.R.B., S.A.P., T.S.W. and K.E.H.P. supplied samples. K.E.H.P. undertook the analyses and processed the data. K.E.H.P, M.J.C, T.S.W. and R.C.P. wrote the paper. All authors discussed the results and commented on the manuscript.

FN4Author information Reprints and permissions information is available at

FN5The authors declare no competing financial interests.


We thank P. Allen, N. Ashton, D. Bain, M. Bates, S. Boreham, D. Bowen, R. Briant, C. Buckingham, J. Clayden, G. R. Coope, A. Cruickshanks, P. Dark, B. Demarchi, M. Greenwood, T. van Kolfschoten, H. Langford, S. Lewis, D. Maddy, R. Markham, D. Mayhew, H. Roe, J. Rose, D. Schreve, R. Scott, K. Scott, C. Stringer, R.Waghorne, M. Warren and F. Wenban-Smith for providing some of the material analysed and general discussion. C. Helmsley and J. Todd released material from the Natural History Museum, London, for destructive analysis. R. Allen provided technical support. G. Peeters gave permission to reproduce images of Bithynia. The analyses were funded by English Heritage, NERC and the Wellcome Trust (grant GR076905MA). This is a contribution to the Ancient Human Occupation of Britain (AHOB) project funded by the Leverhulme Trust.

1. Miller GH,Hollin JT,Andrews JT. Aminostratigraphy of UK Pleistocene depositsNatureYear: 1979281539543
2. Bowen DQ,Hughes S,Sykes GA,Miller GH. Land-sea correlations in the Pleistocene based on isoleucine epimerization in non-marine molluscsNatureYear: 19893404951
3. von Koenigswald W,van Kolfschoten T. Turner CThe early Middle Pleistocene in EuropeYear: 1996211226Balkema
4. Schreve DC. Differentiation of the British late Middle Pleistocene interglacials: the evidence from mammalian biostratigraphyQuaternary Science ReviewsYear: 20012016931705
5. Keen DH. Towards a late Middle Pleistocene non-marine molluscan biostratigraphy for the British IslesQuaternary Science ReviewsYear: 20012016571665
6. Bridgland DR. The record from British Quaternary river systems within the context of global fluvial archivesJournal of Quaternary ScienceYear: 201025433446
7. Ashton N,Lewis SG. Deserted Britain: declining populations in the British late Middle PleistoceneAntiquityYear: 200276388396
8. Bridgland DR,Maddy D,Bates M. River terrace sequences: templates for Quaternary geochronology and marine-terrestrial correlationJournal of Quaternary ScienceYear: 200419203218
9. Penkman KEH,Kaufman DS,Maddy D,Collins MJ. Closed-system behaviour of the intra-crystalline fraction of amino acids in mollusc shellsQuaternary GeochronologyYear: 2008322519684879
10. Penkman KEH,et al. Testing the aminostratigraphy of fluvial archives: the evidence from intra-crystalline proteins within freshwater shellsQuaternary Science ReviewsYear: 2007262958296919684880
11. Penkman KEH,Preece RC,Keen DH,Collins MJ. Amino acid geochronology of the type Cromerian of West Runton, Norfolk, UKQuaternary InternationalYear: 2010228253721217810
12. Sykes GA,Collins MJ,Walton DI. The significance of a geochemically isolated intracrystalline fraction within biomineralsOrganic GeochemistryYear: 19952310591065
13. Kaufman DS,Manley WF. A new procedure for determining DL amino acid ratios in fossils using reverse phase liquid chromatographyQuaternary Science ReviewsYear: 1998179871000
14. Preece RC,Penkman KEH. New faunal analyses and amino acid dating of the Lower Palaeolithic site at East Farm, Barnham, SuffolkProceedings of the Geologists’ AssociationYear: 2005116363377
15. Bowen DQ. A revised correlation of Quaternary deposits in the British IslesGeological Society of London, Special Report No. 23Year: 1999174
16. Bridgland DR. River terrace systems in north-west Europe: an archive of environmental change, uplift and early human occupationQuaternary Science ReviewsYear: 20001912931303
17. Gibbard P. The Pleistocene History of the Lower Thames ValleyYear: 1994Cambridge University Press
18. Bridgland DR. Quaternary of the ThamesYear: 1994Chapman and Hall
19. Bridgland DR. The Middle and Upper Pleistocene sequence in the Lower Thames: a record of Milankovitch climatic fluctuation and early human occupation of southern BritainProceedings of the Geologists’ AssociationYear: 2006117281305
20. Bridgland DR,et al. The Palaeolithic occupation of Europe as revealed by evidence from the rivers: data from IGCP 449Journal of Quaternary ScienceYear: 200621437455
21. Maddy D,Keen DH,Bridgland DR,Green CP. A revised model for the Pleistocene development of the River Avon, WarwickshireJournal of the Geological Society of LondonYear: 1991148473484
22. White TS,Bridgland DR,Howard AJ. White TS,Bridgland DR,Howard AJ,White MJThe Quaternary of the Trent Valley and Adjoining Regions: Field GuideYear: 20071023Quaternary Research Association
23. Boreham S,White TS,Bridgland DR,Howard AJ,White MJ. The Quaternary history of the Wash fluvial networkProceedings of the Geologists’ AssociationYear: 2010121393409
24. Coope GR,Angus RB. An ecological study of a temperate interlude in the middle of the last glaciation, based on fossil Coleoptera from Isleworth, MiddlesexJournal of Animal EcologyYear: 197544365391
25. Maddy D,et al. The Upper Pleistocene deposits at Cassington, near Oxford, EnglandJournal of Quaternary ScienceYear: 199813205231
26. Meijer T,Preece RC. A review of the occurrence of Corbicula in the Pleistocene of North-west EuropeNetherlands Journal of Geosciences – Geologie en MijnbouwYear: 200079241255
27. Preece RC,et al. Biostratigraphic and aminostratigraphic constraints on the age of the Middle Pleistocene glacial succession in North Norfolk, UKJournal of Quaternary ScienceYear: 200924557580
28. White MJ,Ashton N. Lower Palaeolithic core technology and the origins of the Levallois method in North-Western EuropeCurrent AnthropologyYear: 200344598609
29. Lewis SG,Ashton N,Jacobi R. Ashton N,Lewis SG,Stringer CThe Ancient Human Occupation of BritainYear: 2010125164Elsevier
30. Jansen E,et al. Solomon S,et al.Climate Change 2007: The Physical Science Basis. Contribution of Working Group I to the Fourth Assessment Report of the Intergovernmental Panel on Climate ChangeYear: 2007Cambridge University Press

Article Categories:
  • Article

Previous Document:  14-3-3 proteins act as intracellular receptors for rice Hd3a florigen.
Next Document:  Perpendicular switching of a single ferromagnetic layer induced by in-plane current injection.