Elsevier

Quaternary Science Reviews

Volume 218, 15 August 2019, Pages 107-121
Quaternary Science Reviews

Unravelling the oxygen isotope signal (δ18O) of rodent teeth from northeastern Iberia, and implications for past climate reconstructions

https://doi.org/10.1016/j.quascirev.2019.04.035Get rights and content

Highlights

  • Oxygen isotopes analyses on rodent contributes to continental environment knowledge.

  • Iberia requires a specific regional equation for past temperatures estimation.

  • Prey-predator interactions influence oxygen isotope temporal information recorded.

  • Seasonality bias and Iberian context are considered in the methodological proposal.

  • Complementary palaeoenvironmental methods yielded matching results at Xaragalls cave.

Abstract

Small mammals, especially rodents, constitute valuable proxies for continental Quaternary environments at a regional and local scale. Recent studies have demonstrated the relation between the stable oxygen isotope composition of the biogenic phosphate from rodent teeth (δ18Op), and the oxygen isotope composition of meteoric waters18Omw), which is related to air temperatures at mid and high latitudes. This work explores the δ18Op of rodent tooth enamel (from Murinae and Arvicolinae subfamilies) to investigate the palaeoenvironmental conditions in northeastern Iberia during Marine Isotope Stage 3 (MIS 3; ca. 60-30 ka). Fourteen new δ18Op analyses from modern samples in conjunction with forty-six δ18Op analyses previously published are used to decipher the isotope record of present-day rodent teeth in this region. Two main factors should be considered in Iberian palaeoenvironmental reconstructions: the singular nature of Iberian δ18Omw records and the potential seasonality bias of small-mammal accumulation. Methodological proposals are made with a view to ensuring the correct interpretation of the δ18Op of small mammals in reconstructing past air temperatures. This methodology is applied to the MIS 3 sequence of the Cova dels Xaragalls site (Vimbodí-Poblet, Tarragona, Spain), where fifty-one δ18O analyses were performed on wood mouse (Apodemus sylvaticus) lower incisors. A spring-early summer accumulation of small mammals is suggested for the layers at Cova dels Xaragalls. In agreement with previous environmental studies of the site, variations in the δ18Op values suggest slight fluctuations in the climatic conditions throughout the sequence, which are consistent with the stadial-interstadial alternations that characterized MIS 3. Complementary palaeoenvironmental methods determine cooler conditions than nowadays, but within a globally stable climatic period.

Introduction

The Iberian Peninsula is located at mid latitudes, with an area of 582,000 km2 and an average altitude of 660 m. This peninsula constitutes the southwestern extremity of the Eurasian continent, from which it is partially isolated by the Pyrenean Mountains. Today, Iberia experiences temperate climatic conditions, which nonetheless vary spatially due to the proximity of the Atlantic Ocean, the Mediterranean Sea and the Pyrenean Mountains. The specific orography of the Iberian Peninsula adds further complexity by structuring the climate and the landscape, with the Central Meseta located at high altitudes (660 m), surrounded by several ranges such as the Sierra Nevada and the Cantabrian Mountains. The Galician-Cantabrian and Pyrenean mountain systems shelter the rest of the peninsula from the Atlantic Ocean and the continental cold air masses coming from the northwest and the northeast, respectively. The combination of all these factors gives the Iberian Peninsula exceptional environmental conditions in relation to the rest of the Eurasian continent.

The Late Pleistocene glacial regime and subsequent glacial-interglacial fluctuations had an impact both on flora and fauna, including human populations throughout western Europe and the Iberian Peninsula (Uriarte, 2003; Arrizabalaga, 2004). In southern Europe, Marine Isotope Stage 3 (MIS 3; ca. 60-30 ka) was characterized by climate dynamics that alternated between warming and cooling periods of sea-surface temperatures, which on the continent generated phases of forest development and expansion of semi-arid areas, respectively (Fletcher et al., 2010; Harrison and Sanchez Goñi, 2010). However, pollen and small-mammal studies have shown that these alternations are not easily resolved in regional and local contexts, suggesting Iberia never underwent a complete loss of woodland, even during stadials or Heinrich events (Fletcher et al., 2010; López-García et al., 2014). Small-vertebrate assemblages, which reflect local environments, reveal cooler and wetter conditions for MIS 3. It has been observed that the coexistence of cold- and temperate-adapted species varies with the stadial and interstadial fluctuations, although woodland-dwelling species are always frequent (Fernández-García et al., 2016; López-García et al., 2014). The Iberian Peninsula served as a macro-refugium for many floral and faunal species during stadial periods, sheltering them from harsher climatic episodes until more favourable environmental conditions allowed their geographic radiation (Hewitt, 2000; Sommer and Nadachowski, 2006).

To obtain a more complete view of past changes in climate and biodiversity, it is necessary to expand the continental palaeoenvironmental record, which is underrepresented compared to marine and ice-core records. Geochemical approaches based on stable oxygen isotope compositions (δ18O) represent a promising tool for obtaining high-resolution environmental records from regional and local contexts. Isotope compositions measured from mammalian bone and tooth fossils permit the quantification of climatic parameters, due to the interdependence of climatic variables such as air temperatures, the oxygen isotope composition of meteoric waters (δ18Omw) and the oxygen isotope composition of body tissues (Dansgaard, 1964; Kolodny et al., 1983; Longinelli, 1984; Longinelli and Nuti, 1973; Luz et al., 1984; Rozanski et al., 1993). These isotopic data can be combined with palaeoecological data inferred from vertebrate assemblages in order to obtain a coherent and refined picture of continental palaeoenvironments (e.g. Freudenthal et al., 2014; Royer et al., 2013b, 2014). Advances in chemical techniques and analytical methodologies now offer an opportunity to perform geochemical analyses on small-mammal teeth, which are particularly relevant in documenting high-resolution climatic changes at a regional or a local scale (e.g. Barham et al., 2017; Freudenthal et al., 2014; García-Alix, 2015; Grimes et al., 2003; Héran et al., 2010; Jeffrey et al., 2015; Leichliter et al., 2017; Lindars et al., 2001; Navarro et al., 2004).

Unfortunately, interpreting the oxygen isotope composition of small-mammal skeletal apatite is not straightforward, and several questions concerning its application to the fossil record have recently been raised (Barham et al., 2017; Jeffrey et al., 2015; Peneycad et al., 2019; Royer et al., 2014, 2013a, 2013b). The question of prey-predator interactions is considered to be of paramount importance in deciphering the isotopic signal recorded in accumulated fossil rodent remains, especially for regions with a specific climatic mode such as the Iberian Peninsula. The main purpose of this work is thus to develop an isotopic framework for environmental and climatic reconstructions for the Iberian Peninsula, based on the oxygen isotope composition of phosphate (δ18Op) from present-day rodent teeth recovered from pellets. A first step aims to assess the specific role of the climatic context of the Iberian Peninsula, whilst a second one seeks to achieve a better understanding of δ18O from small-mammal teeth, focusing on the origin of the remains and their period of production. A refinement of the interpretation of the δ18Op of fossil rodent tooth phosphate in terms of palaeotemperature reconstructions is finally applied to Cova dels Xaragalls assemblage. This Iberian Late Pleistocene sedimentary sequence, rich in small-vertebrate remains, thus offers the opportunity to reconstruct climate parameters in a continental environment contemporaneous with MIS 3.

Section snippets

Cova dels Xaragalls (Tarragona, Spain)

Cova dels Xaragalls is located in Poblet Forest in the municipality of Vimbodí-Poblet (Tarragona), on the left margin of the Castellfollit Creek in the head of the Francolí River basin at 590 m a.s.l. (Fig. 1A). It is a fossiliferous cave of phreatic origin hosted within Mesozoic limestones and Paleozoic schist. The site can be separated into two main areas: a Holocene sequence is developed at the entrance, and at the interior termination of the cave system, in the “Sala Gran” gallery, there is

Modern samples from northeastern Iberia

Fourteen lower incisors from present-day rodents were collected from pellets to analyse their oxygen isotope composition (δ18O). These pellets were collected from five different sites located in northeastern Iberia (Fig. 1, Fig. 2; Table 1): Serinyà (Girona), Moià (Barcelona), Prades (Tarragona), Balaguer (Lleida) and El Catllar (Tarragona). The sites are distributed within the same latitudinal range (from 41°N to 42°N) but at different altitudes ranging from 188 m a.s.l. at Serinyà to 1000 m

Results and discussion

The reconstruction of past air temperatures from the oxygen isotope composition of rodent teeth is a two-step procedure: 1) the measured δ18Op values of the fossil rodent teeth allow the estimation of the δ18O values of local meteoric water (δ18Omw) and, 2) the calculated δ18Omw values can be used to estimate past air temperatures. Since pioneering works in the 1980's (Longinelli, 1984; Luz et al., 1984; Luz and Kolodny, 1985), many studies have explored the complex relationship between the

Conclusions

Oxygen isotope compositions were measured in rodent teeth accumulated in modern owl pellets from five different sites located in northeastern Iberia and complemented with previously published δ18O results from rodent teeth from the Iberian Peninsula. The peculiar orography and climatic mode of the Iberian Peninsula are emphasized by this study, which documents low δ18Op values and a large annual range of δ18Omw in comparison to southern France. On the basis of recent δ18Omw values extracted

Acknowledgements

The authors are grateful to Aitor Burguet Coca, Joan Burguet Ardiaca, Marta Puig Domènech, David Funosas, Marius Domingo de Pedro and Josep Maria Vergés for providing pellet samples. We also thank the team from the Laboratoire de Géologie of Lyon for allowing us to perform the isotope analysis, especially to Romain Amiot and Magali Seris. We also thank Christiane Denys, Emmanuelle Stoetzel and Hugues-Alexandre Blain for their help and advice during the preparation of the manuscript. We are also

References (96)

  • H.C. Fricke et al.

    The correlation between 18O/16O ratios of meteoric water and surface temperature: its use in investigating terrestrial climate change over geologic time

    Earth Planet. Sci. Lett.

    (1999)
  • A. García-Alix

    A multiproxy approach for the reconstruction of ancient continental environments. The case of the Mio–Pliocene deposits of the Granada Basin (southern Iberian Peninsula)

    Glob. Planet. Change

    (2015)
  • A. Gehler et al.

    Triple oxygen isotope analysis of bioapatite as tracer for diagenetic alteration of bones and teeth

    Palaeogeogr. Palaeoclimatol. Palaeoecol.

    (2011)
  • S.T. Grimes et al.

    Is small beautiful? A review of the advantages and limitations of using small mammal teeth and the direct laser fluorination analysis technique in the isotope reconstruction of past continental climate change

    Palaeogeogr. Palaeoclimatol. Palaeoecol.

    (2008)
  • S.T. Grimes et al.

    Palaeogene palaeoclimate reconstruction using oxygen isotopes from land and freshwater organisms: the use of multiple palaeoproxies

    Geochim. Cosmochim. Acta

    (2003)
  • S.P. Harrison et al.

    Global patterns of vegetation response to millennial-scale variability and rapid climate change during the last glacial period

    Quat. Sci. Rev.

    (2010)
  • G. Hartman et al.

    Isotopic evidence for Last Glacial climatic impacts on Neanderthal gazelle hunting territories at Amud Cave, Israel

    J. Hum. Evol.

    (2015)
  • M.A. Héran et al.

    Cenozoic long-term terrestrial climatic evolution in Germany tracked by δ18O of rodent tooth phosphate

    Palaeogeogr. Palaeoclimatol. Palaeoecol.

    (2010)
  • M. Hernández Fernández et al.

    Bioclimatic analysis of rodent palaeofaunas reveals severe climatic changes in Southwestern Europe during the Plio-Pleistocene

    Palaeogeogr. Palaeoclimatol. Palaeoecol.

    (2007)
  • A. Jeffrey et al.

    Influences on the stable oxygen and carbon isotopes in gerbillid rodent teeth in semi-arid and arid environments: implications for past climate and environmental reconstruction

    Earth Planet. Sci. Lett.

    (2015)
  • Y. Kolodny et al.

    Oxygen isotope variations in phosphate of biogenic apatites, I. Fish bone apatite rechecking the rules of the game

    Earth Planet. Sci. Lett.

    (1983)
  • C. Lécuyer et al.

    Thermal excursions in the ocean at the Cretaceous-Tertiary boundary (northern Morocco): δ18O record of phosphatic fish debris

    Palaeogeogr. Palaeoclimatol. Palaeoecol.

    (1993)
  • C. Lécuyer et al.

    Oxygen isotope exchange between dissolved phosphate and water at temperatures ≤135°C: inorganic versus biological fractionations

    Geochim. Cosmochim. Acta

    (1999)
  • J.A. Lee-Thorp et al.

    Aspects of the chemistry of modern and fossil biological apatites

    J. Archaeol. Sci.

    (1991)
  • J. Leichliter et al.

    Stable carbon isotope ecology of small mammals from the Sterkfontein Valley: implications for habitat reconstruction

    Palaeogeogr. Palaeoclimatol. Palaeoecol.

    (2017)
  • E.S. Lindars et al.

    Phosphate δ18O determination of modern rodent teeth by direct laser fluorination: an appraisal of methodology and potential application to palaeoclimate reconstruction

    Geochim. Cosmochim. Acta

    (2001)
  • A. Longinelli

    Oxygen isotopes in mammal bone phosphate: a new tool for paleohydrological and paleoclimatological research?

    Geochim. Cosmochim. Acta

    (1984)
  • A. Longinelli et al.

    Oxygen isotope measurements of phosphate from fish teeth and bones

    Earth Planet. Sci. Lett.

    (1973)
  • J.M. López-García et al.

    Environmental and climatic context of neanderthal occupation in southwestern Europe during MIS3 inferred from the small-vertebrate assemblages

    Quat. Int.

    (2014)
  • B. Luz et al.

    Oxygen isotope variations in phosphate of biogenic apatites, IV. Mammal teeth and bones

    Earth Planet. Sci. Lett.

    (1985)
  • B. Luz et al.

    Fractionation of oxygen isotopes between mammalian

    Geochim. Cosmochim. Acta

    (1984)
  • N. Navarro et al.

    Oxygen isotope compositions of phosphate from arvicoline teeth and Quaternary climatic changes, Gigny, French Jura

    Quat. Res.

    (2004)
  • B.H. Passey et al.

    Tooth enamel mineralization in ungulates: implications for recovering a primary isotopic time-series

    Geochim. Cosmochim. Acta

    (2002)
  • E. Peneycad et al.

    Variability in the oxygen isotope compositions of modern rodent tooth carbonate: implications for palaeoclimate reconstructions

    Palaeogeogr. Palaeoclimatol. Palaeoecol.

    (2019)
  • D.W. Podlesak et al.

    Turnover of oxygen and hydrogen isotopes in the body water, CO2, hair, and enamel of a small mammal

    Geochim. Cosmochim. Acta

    (2008)
  • A.J.E. Pryor et al.

    Quantification and propagation of errors when converting vertebrate biomineral oxygen isotope data to temperature for palaeoclimate reconstruction

    Palaeogeogr. Palaeoclimatol. Palaeoecol.

    (2014)
  • A. Royer et al.

    What does the oxygen isotope composition of rodent teeth record?

    Earth Planet. Sci. Lett.

    (2013)
  • A. Royer et al.

    Late Pleistocene (MIS 3-4) climate inferred from micromammal communities and δ18O of rodents from Les Pradelles, France

    Quat. Res.

    (2013)
  • A. Royer et al.

    Summer air temperature, reconstructions from the last glacial stage based on rodents from the site Taillis-des-Coteaux (Vienne), Western France

    Quat. Res.

    (2014)
  • D.P. Schrag et al.

    The oxygen isotopic composition of seawater during the Last Glacial Maximum

    Quat. Sci. Rev.

    (2002)
  • G. Skrzypek et al.

    Reassessment of recommendations for processing mammal phosphate δ18O data for paleotemperature reconstruction

    Palaeogeogr. Palaeoclimatol. Palaeoecol.

    (2016)
  • P. Sunyer et al.

    Wood mouse population dynamics: interplay among seed abundance seasonality, shrub cover and wild boar interference

    Mamm. Biol.

    (2016)
  • U. von Grafenstein et al.

    A 200 year mid-European air temperature record preserved in lake sediments: an extension of the δ18Op-air temperature relation into the past

    Geochim. Cosmochim. Acta

    (1996)
  • A. Zazzo et al.

    Experimentally-controlled carbon and oxygen isotope exchange between bioapatites and water under inorganic and microbially-mediated conditions

    Geochim. Cosmochim. Acta

    (2004)
  • P. Andrews

    Owls, Caves and Fossils. Predation, Preservation and Accumulation of Small Mammal Bones in Caves, with an Analysis of the Pleistocene Cave Faunas from Westbury-sub-Mendip, Somerset, UK

    (1990)
  • Á. Arrizabalaga

    Paleoclimatología y cronología del Würm reciente: un intento de síntesis

    Zephyrus

    (2004)
  • G.J. Bowen

    The Online Isotopes in Precipitation Calculator, Version 3.1 (4/2017)

    (2017)
  • M.T. Clementz

    New insight from old bones: stable isotope analysis of fossil mammals

    J. Mammal.

    (2012)
  • Cited by (5)

    • Environment and climate during the Neanderthal-AMH presence in the Garraf Massif mountain range (northeastern Iberia) from the late Middle Pleistocene to Late Pleistocene inferred from small-vertebrate assemblages

      2022, Quaternary Science Reviews
      Citation Excerpt :

      On the other hand, the H5 to H3 events are characterized, according to Sánchez-Goñi et al. (2000), by a pattern divided into three phases: 1) the first comprising relatively high percentages of Euro-Siberian trees, such as deciduous Quercus and Ericaceae shrubs, as well as the end of a temperate and humid terrestrial phase; 2) a middle phase with an optimal development of steppe vegetation, thus reflecting synchronous terrestrial and oceanic cooling; 3) a ceiling associated with an increase in the proportions of Euro-Siberian trees and Ericaceae, reflecting a new temperate and humid period at average terrestrial latitudes and North Atlantic Ocean latitudes. In the southern Mediterranean region, the sites with small-vertebrate studies associated with the H5 event are Abric Romaní layer E (López-García and Cuenca-Bescós, 2010; Burjachs et al., 2012; Fernández-García et al., 2020), Xaragalls cave layer C4 (López-García et al., 2012c; Fernández-García et al., 2019), Fumane cave units A7 to A6 (López-García et al., 2015b), and Grotta del Broion Q3-1-P (Sala, 1980; Colamussi, 2002; Berto and Rubinato, 2013). The H4 event has been recognized in Fumane cave units A3 to A1 (López-García et al., 2015b) and Grotta del Broion layers I4-1 to H6-3 (Sala, 1980; Colamussi, 2002; Berto and Rubinato, 2013).

    • Combined palaeoecological methods using small-mammal assemblages to decipher environmental context of a long-term Neanderthal settlement in northeastern Iberia

      2020, Quaternary Science Reviews
      Citation Excerpt :

      In case of predation, the δ18Op should reflect the δ18Omw at the time and space each rodent was captured (Fernández-García et al., 2019; Peneycad et al., 2019; Royer et al., 2013a, 2013b). This work follows the three-step strategy proposed for δ18Op from rodent tooth accumulated in Iberia (Fernández-García et al., 2019) for estimating mean annual temperatures (MAT): calculation of δ18Omw from δ18Op throughout the linear oxygen isotope fractionation equation determined by Royer et al. (2013a) [δ18Op = 1.21 (±0.20) x δ18Omw + 24.76 (±2.70)];

    • The end of Late Glacial in north-eastern Iberia: the small mammal assemblage from Cudó cave (Mont-Ral, Tarragona)

      2023, Earth and Environmental Science Transactions of the Royal Society of Edinburgh
    View full text