Nitrogen isotope analyses of reindeer (Rangifer tarandus), 45,000 BP to 9,000 BP: Palaeoenvironmental reconstructions

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Palaeogeography, Palaeoclimatology, Palaeoecology 262 (2008) 32 – 45 www.elsevier.com/locate/palaeo

Nitrogen isotope analyses of reindeer (Rangifer tarandus), 45,000 BP to 9,000 BP: Palaeoenvironmental reconstructions Rhiannon E. Stevens a,⁎, Roger Jacobi b , Martin Street c , Mietje Germonpré d , Nicholas J. Conard e , Susanne C. Münzel e , Robert E.M. Hedges f a McDonald Institute for Archaeological Research, University of Cambridge, Downing Street, Cambridge, CB2 3ER, UK The British Museum, 38-46 Orsman Road, London, N1 5QJ, and Department of Palaeontology, Natural History Museum, London SW1 5BD, England, UK c Römisch-Germanisches Zentralmuseum, Forschungsbereich Altsteinzeit, Schloss Monrepos, 56567 Neuwied, Germany d Department of Palaeontology, Royal Belgian Institute for Natural Sciences, Vautierstraat 29, 1000 Brussels, Belgium e Institut für Ur und Frühgeschichte und Archäologie des Mittelalters, Eberhard-Karls-Universität Tübingen, Schloss Hohentübingen, Burgsteige 11, D-72010 Tübingen, Germany Research Laboratory for Archaeology and the History of Art (RLAHA), University of Oxford, Dyson Perrins Building, South Parks Road, Oxford, OX1 3QY, UK b

f

Received 2 September 2006; received in revised form 14 January 2008; accepted 25 January 2008

Abstract Pleistocene faunal δ15N variations are thought to reflect changes in climatic and environmental conditions. Researchers are still unclear, however, which climatic/environmental parameter is the primary control on Pleistocene faunal δ15N values. Through extensive nitrogen isotope analysis of Late Pleistocene reindeer (Rangifer tarandus) collagen we investigated whether permafrost development during the Late Pleistocene coincided with changes in δ15N values. After 45 ka BP reindeer δ15N declined, with lowest δ15N values observed after the Last Glacial Maximum (LGM), between 15 and 11 ka BP. The decline in δ15N appears to be of a greater magnitude in more northern regions than in the South of France, a pattern similar to that previously observed for horse. On a global scale, ecosystem δ15N is controlled by the relative openness of the nitrogen cycle, which in turn is controlled by climate. Low soil and plant δ15N are observed in cold and/or wet regions and high δ15N are seen in hot and/or arid areas. The regional pattern in reindeer δ15N decline mimics the pattern of climatic deterioration in Europe culminating at the LGM, with climate cooling being more intense in northern Europe than in southern Europe. However, the lowest reindeer δ15N values are observed after temperatures started to rise. This may have been due to a lag in the response of the nitrogen cycle to increasing temperatures. Alternatively it may have been linked to the influence of permafrost degradation on soil and plant δ15N and thus faunal δ15N. The renewed climatic cooling during the Younger Dryas did not see a fall in reindeer δ15N. Limited data does, however, suggest a post Younger Dryas depletion in reindeer δ15N values. © 2008 Elsevier B.V. All rights reserved. Keywords: Isotope; Nitrogen; Palaeoclimate; Palaeoenvironment; Reindeer; Bone

1. Introduction Palaeodietary reconstructions using isotope techniques are based on the principle that food sources contain different isotope signatures, which are passed along the food chain to their consumers (Schoeninger and DeNiro, 1984; Ambrose and

⁎ Corresponding author. Fax: +44 1223 333503. E-mail address: [email protected] (R.E. Stevens). 0031-0182/$ - see front matter © 2008 Elsevier B.V. All rights reserved. doi:10.1016/j.palaeo.2008.01.019

DeNiro, 1986; Bocherens et al., 1999; Richards and Hedges, 1999; Privat et al., 2002). Although diet is the principal control determining bone collagen isotope values, climate and local environment can also create small-scale isotopic variability (van Klinken et al., 1994; Cormie and Schwarcz, 1996; Gröcke et al., 1997; Schwarcz et al., 1999). From small-scale variability in bone collagen nitrogen isotope signatures researchers have in recent years attempted to reconstruct palaeoenvironmental conditions at specific sites, over time and across regions (e.g. Gröcke et al., 1997; Iacumin et al., 1997, 2000; Drucker et al.,

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2000; Richards and Hedges, 2003; Drucker et al., 2003; Stevens and Hedges, 2004). A number of studies have focused on the Late Pleistocene, with a lowering of faunal nitrogen isotope values roughly coinciding with the widespread climatic cooling culminating at the Last Glacial Maximum (LGM, 22,000– 18,000 BP) (Drucker et al., 2003; Stevens and Hedges, 2003; Stevens, 2004). However, in studies to date, the magnitude and timing of the variation in faunal δ15N over the last 45,000 years is still fairly unclear due to a lack of continuity of data from any single species, both temporally and spatially. Furthermore, the environmental controls directly influencing faunal δ15N during the Late Pleistocene are unknown. Permafrost development has, however, been suggested as a parameter that could possibly cause variation in Late Pleistocene herbivore δ15N values (Stevens and Hedges, 2003; Drucker et al., 2003; Stevens and Hedges, 2004). The aim of this study was to determine whether permafrost development during the Late Pleistocene coincided with changes in faunal δ15N values and thus whether it could be the primary environmental control influencing Late Pleistocene faunal δ15N values. To improve the continuity of Late Pleistocene faunal δ15N data we selected a single species, reindeer (Rangifer tarandus), for investigation. Reindeer are adapted to temperate and cold environments. They have large feet which facilitate walking on snow and digging through snow for winter forage, long thick winter pelage with hollow guards hairs and a close underfur for extra insulation, valvular nostrils, broad short furry ears and short fury tails (Banfield, 1977; Leader-Williams, 1988; Weinstock, 2000). Today reindeer inhabit arctic tundra, subarctic taiga, mountainous areas – where they occupy the alpine tundra and subalpine forest zones – and boreal coniferous forest, which they only visit in winter (Heptner et al., 1966; Banfield, 1977; Weinstock, 2000). Reindeer typically occupy habitats with between 300 mm and 700 mm of rainfall per year, average January temperatures of − 70 °C to − 10 °C and average July temperatures of 0 °C to 17 °C (Delpech, 1983). Snow cover correlates with habitat suitability, with a maximum depth of 60 cm being acceptable to the reindeer (Baker, 1978; Boyle, 1990). Reindeer are mixed feeders. In summer months they mainly consume a wide range of vascular plants and to a lesser extent lichen, whereas in winter months their diet is much less varied, with lichen of greater importance in lower latitudes and graminoids and moss of greater importance in the high arctic (Weinstock, 2000). During the Late Pleistocene in Northern Eurasia reindeer was the most abundant large herbivore occupying regions subject to permafrost development and regions proximal to the ice sheets. Thus reindeer is a good species to investigate potential correlations between permafrost development and faunal δ15N values. Reindeer obtain their nitrogen from their food, i.e. plants. Thus their nitrogen isotope signatures reflect those of the plants they consume. In modern ecosystems plant δ15N is dependent on multiple factors including soil δ15N, soil development, nutrient availability (nitrogen and phosphorus), mycorrhizal associations, soil acidity and nitrogen cycling. However, the predominant mechanism determining soil and plant δ15N is the extent to which the nitrogen cycle is an open or closed system. The “openness” of

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the nitrogen cycling system can be determined by the relative importance of within-ecosystem nitrogen cycling versus the relative importance of inputs and outputs (Handley et al., 1999). In cold and/or wet ecosystem inputs and outputs are limited and within-ecosystem cycling of nitrogen between live organic and dead organic pools is dominant. As little nitrogen is lost from the system, soil and plant δ15N remain low (Handley et al., 1999). This is particularly true in permafrost regions where low soil temperatures lead to low mineralization rates and limited availability of inorganic nitrogen. In hot and/or arid ecosystems this cycle is interrupted, with proportionally more nitrogen flowing from organic to mineral nitrogen pools, which are subject to preferential loss of 14N through processes such as leaching, denitrification and ammonia volatilisation, resulting in enrichment of soil and plant δ15N (Austin and Vitousek, 1998; Handley et al., 1999). Thus, on a global scale, ecosystem δ15N is controlled by the relative openness of the nitrogen cycle which in turn is controlled by climate, resulting in low δ15N observed in cold and/ or wet areas and high δ15N seen in hot and/or arid areas (Amundson et al., 2003). Although some of the lowest plant δ15N values are observed in arctic and tundra regions we are not aware of any study that has directly look at the influence of permafrost development or degradation on soil or plant δ15N values. 2. Materials and methods 2.1. Sample selection The continuity of Late Pleistocene reindeer data was improved by collecting and analysing the isotopes of reindeer bones from a number of European Late Pleistocene sites and through collation of published reindeer δ15N results. Nitrogen isotope values from 294 reindeer are included in this study. 121 samples were collected, prepared and analysed by R. Stevens at the Research Laboratory for Archaeology and the History of Art, Oxford (RLAHA) as part of a NERC D.Phil studentship (NER/S/A/2000/03522). 32 results were extracted from the Oxford Radiocarbon Database. A further 141 results were taken from the published literature (Drucker et al., 2000 (n = 39); Iacumin et al., 2000 (n = 22); Drucker et al., 2003 (n = 80)). The reindeer samples were sourced from 52 sites – in the UK and Ireland (21 sites, 60 samples, from here on grouped as UK), Belgium (4 sites, 11 samples), Germany (11 sites, 74 samples), southern France (13 sites, 127 samples) and Siberia (3 sites, 22 samples) (Fig. 1). The majority of these sites contained archaeological as well as palaeontological material. A full provenance for each sample can be found in the online supplementary dataset. Only 55 of the samples were directly radiocarbon dated. However, other samples collected and analysed in this study were indirectly dated through radiocarbon dates of associated material (see online supplementary dataset). Results collated from published literature were assigned to a time block based on the chronology available from the published literature (established either via radiocarbon dating or via radiocarbon dates from associated material). Data was separated into archaeological time blocks as many of the samples have not been radiocarbon dated. The duration of time blocks used in this study is based on those

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used by Huijzer and Vandenberghe (1998) in their reconstruction of Late Pleistocene permafrost development and degradation. Although employing time periods of varying duration (and thus number of samples) can affect the chronological analysis of the data, we selected this method in order to test for isotope differences between periods with known permafrost histories. Unless otherwise stated dates quoted in the text are in uncalibrated 14C Years BP. This takes into consideration controversies regarding the feasibility of radiocarbon calibration beyond 26,000 calibrated years BP (the limit of IntCal04) and ongoing efforts to extend this (discussion e.g. van Andel, 1998, 2005; van der Plicht, 1999). Dates younger than 26,000 BP were also not calibrated in order to maintain a single chronological scale throughout the discussed dataset. However, all dates were calibrated with CalPal Online (which uses the CalPal_2007_HULU calibration curve) and can be found in the supplementary dataset. 2.2. Stable isotope methods Samples were prepared according to the procedure used by the Oxford Radiocarbon Accelerator Unit (ORAU) (with some modifications) (Bronk Ramsey et al., 1999). Bone samples were obtained using a drill. The surface of the bone was drilled away to remove any surface contamination and then a second aliquot of powder (approximately 300–500 mg) was drilled out and collected. For samples that had been (or were suspected to have been) conserved with PVA glue, a solvent extraction pretreatment was used to remove the adhesive. Pre-treatment involved heating the sample at 40 °C for an hour in distilled water, then repeating the heating process using acetone, distilled water, methanol and distilled water respectively. Collagen was extracted by a modified Longin method (Longin, 1971; Brown et al., 1988): samples were demineralised in 0.5 M aq. HCl at 4 °C until all the mineral had dissolved. Samples were then rinsed with distilled water and 0.1 M Sodium hydroxide was added for 30 minutes to remove humic acids. Samples were then rinsed with distilled water and gelatinised in a pH 3 solution for 48 h at 75 °C. Then the filtered supernatant containing the soluble collagen was collected, frozen and lyophilized. Between 2.5 and 3.5 mg of collagen was loaded into a tin capsule for continuous flow combustion and isotopic analysis. Samples were analysed using an automated Carlo Erba carbon and nitrogen elemental analyser coupled with a continuous flow isotope ratio-monitoring mass spectrometer (PDZ Europa Geo 20/20 mass spectrometer). Results are reported in units per mil (‰) and δ15N values were measured relative to the AIR (atmospheric nitrogen) standards. Where possible each sample was run in duplicate or triplicate. Replicate measurement errors on laboratory standards (comprising in-house standards of nylon and

Fig. 2. Boxplot of 294 reindeer δ15N plotted over time.

alanine calibrated against IAEA standards and modern bovine bone collagen as a standard “unknown”) were less than 0.2‰ over the period of analysis. For 14C dated samples the analytical errors are larger, potentially as large as ±0.3‰ (Peter Ditchfield pers. Comm.). Radiocarbon dating of three bones (A/VC/B/7, A/GON/ B/45, A/DMC/B/13) was conducted on the collagen extracted for isotope analysis. Prior to radiocarbon dating samples were rehydrolyzed and ultra-filtered by the use of a Vivaspin 15, Sartorius ultra filter (30-kDa molecular-mass cutoff) prior to lyophilization so that molecules over 30 kDa were retained. The C/N ratios calculated for all of the samples in this study were between 2.9 and 3.6, a range considered to be indicative of good collagen preservation (DeNiro, 1985; Ambrose, 1990). Data from the ORAU database include analyses of bone, antler and a single tooth. Antler is a type of bone that grows rapidly. The relationship between bone and antler collagen δ15N values has not been investigated. For this study they are assumed to be equivalent; however, they should been considered with caution in absence of such a systematic investigation. Reindeer adult dentine δ15N is systematically 15N enriched relative to bone, even in late growing teeth which form post-weaning (Drucker et al., 2001). Thus the single reindeer tooth δ15N result must be considered with caution. 3. Results The δ15N values of 294 reindeer can be seen in Fig. 2 and in the online supplementary dataset. Collectively the reindeer δ15N values range from 0.4 to 6.3‰ with a mean δ15N value of 3.3‰ (± 1.2‰). The change in reindeer δ15N over time is considerable (Fig. 2). Pre 20 ka BP reindeer mean δ15N (4.2‰

Fig. 1. Site locations in British Isles, Germany, France, and Belgium. 1 = Kents Cavern, 2 = Pixie's Hole, 3 = Chelm's Combe, 4 = Gough's Old Cave 5 = Badgerhole, 6 = Hyena Den, 7 = Wolf Den, 8 = Aveline's Hole, 9 = Paviland, 10 = Fox Hole Cave, 11 = Castlepook Cave, 12 = Lynx Cave, 13 = Ossom's Cave, 14 = Mother Grundy's Parlour, 15 = Pinhole Cave, 15 = Dead Man's Cave, 17 = Kinsey Cave, 18 = Sewell's Cave, 19 = Victoria Cave, 20 = Bart's Shelter, 21 = Shelter Cave, 22 = Chaleux, 23 = Goyet Cave, 24 = Trou da Somme, 25 = Trou de Nutons, 26 = Karstein rockshelter, 27 = Andernach, 29 = Gönnersdorf, 30 = Wildscheuer Cave, 31 = Abri Stendel, 32 = Breitenbach, 33 = Wiesbaden-Igstadt, 34 = Geissenklösterle, 35 = Hohlefels, 36 = Buttentalhöhle, 37 = Kastelhohle, 38 = Le Bois Ragot, 39 = Ferme de la Bouvière, 40 = Vergisson, Saint Romans, 41 = Grotte du Tai, 42 = Les Peyrugues, 43 = Laugerie-Haute est, 44 = Le Flageolet, 45 = Les Jamblanc, 46 = Moulin-neuf, 47 = St-Germain la Rivière, 48 = Combe Sauniere, 49 = Le Brassot. 50 = Afontova Gora II, 51 = Kashtanka, 52 = Listvenka. Map generated from ESRI map data using ArcGIS v.9.1.

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Table 1 Statistical assessment of differences between the mean δ15N of each time block (results of one way ANOVA with post hoc Bonferroni correction) 9–10 9–10 10–11 11–13 13–15 15–30 20–27 27–32 32–36 36–45

10–11

11–13

13–15

N/A p ≤ 0.001 p = 0.003

p ≤ 0.001 N/A

p = 0.003

p ≤ 0.001 p ≤ 0.001 p = 0.001 p ≤ 0.001 p = 0.001

N/A p = 0.006 p ≤ 0.001 p = 0.010 p ≤ 0.001 p = 0.008

15–20

20–27

p ≤ 0.001 p = 0.006 N/A p ≤ 0.001

p = 0.003 p ≤ 0.001 p ≤ 0.001 p ≤ 0.001 N/A

27–32

32–36

36–45

p = 0.001 p = 0.010

p ≤ 0.001 p ≤ 0.001 p = 0.004

p = 0.001 p = 0.008

N/A

p = 0.003

s.d. 1.0‰ (n = 77)) is significantly higher than that of post 20 ka BP reindeer (2.9‰ s.d. 1.1‰ (n = 217)) (Independent Student's t-test, p ≤ 0.001). The lowest δ15N values are observed during the Late Glacial interstadial (13–11 ka BP) (Table 1, Fig. 2). The mean reindeer δ15N values for the majority of time blocks are statistically significantly different (one-way anova with post hoc bonferroni correction, see Table 1 for further details). The standard deviations within each time block are relatively similar (Table 2), with substantial variability in δ15N observed. The observed pattern of δ15N over time appears to vary between geographic regions, however, this pattern is less statistically robust than the chronological trend observed for the reindeer collectively. Fig. 3 shows the reindeer δ15N plotted by country. Within each time block the range in δ15N values can be as much as 6‰ (Fig. 3A), however, only nine of the results are statistically considered to be outliers (Fig. 3B). Within a time block reindeer δ15N can differ between countries, e.g. at 13– 11 ka BP Siberian reindeer δ15N range from 1.3‰ to 2.3‰, whereas the δ15N of reindeer from the south of France range from 2.6‰ to 4.4‰. Mean reindeer δ15N significantly differed between the following countries within the following time blocks: 32–27 ka BP Germany and the UK (p = 0.036); 27–20 ka BP Siberia and France (p = 0.002); 15–13 ka BP France and Germany (p ≤ 0.001) and France and Siberia (p ≤ 0.001); 13– 11 ka BP Belgium and Siberia (p = 0.014), France and Germany, France and the UK and France and Siberia (p = 0.004, p = 0.003, p = 0.001, respectively). Within the 45–36 ka, 36–32 ka, 20– 15 ka, 11–10 ka, 10–9 ka BP time blocks mean reindeer δ15N did not significantly differ between countries. In addition, the δ15N of reindeer from a single country can differ between time blocks, e.g. reindeer from Germany have δ15N values that range from 1.4‰ to 2.9‰ at 13–11 ka BP, whereas at 33–32 ka BP they range from 4.1‰ to 5.6‰. Mean reindeer δ15N in Germany significantly differs between 11–10 kaBP and both 36–32 ka and 32–27 ka BP (p = 0.040 and p = 0.001, respectively); between 13–11 ka BP and 45–36 ka BP, 36–32 ka BP and 32–27 ka BP (p ≤ 0.001, p ≤ 0.001, p = 0.001, respectively); between 15–13 ka BP and 45–36 ka BP, 36–32 ka BP and 32– 27 ka BP(p ≤ 0.001, p ≤ 0.001, p ≤ 0.001, respectively); and between 20–15 ka BP and 36–32 ka BP (p ≤ 0.001) (one-way anova with post hoc bonferroni correction). The trends in reindeer δ15N for different geographic regions are shown most clearly in Fig. 3C (Outliers were not removed during calculation of means and standard deviations). At 45– 36 ka BP, reindeer δ15N values in the UK are similar to those in

N/A p = 0.004

N/A N/A

Germany. UK reindeer δ15N values then gradually decline, ranging from approximately 2‰ to 3.5‰ at 32–27 ka BP. Between 27 ka BP and 13 ka BP, only one sample was analysed from the UK mainly due to lack of animals present in the UK because of harsh climatic conditions. UK reindeer δ15N values during the Late Glacial interstadial (13–11 ka BP) are similar to those at 32–27 ka BP, although the number of samples is considerably different. UK reindeer δ15N values are higher by around 1.5‰ in the Younger Dryas (11–10 ka BP) and early Holocene (10–9 ka BP) relative to values in the Late Glacial interstadial. Within the UK only the 13–11 ka BP and 11–10 ka BP time blocks, however, have mean δ15N values that differ significantly (p = 0.002, one-way anova with post hoc bonferroni correction). In certain time blocks, UK reindeer δ15N values are similar to those from Germany (e.g.13–11 ka BP), whereas in other time blocks (e.g. 32–27 ka BP), they are lower by around 1‰ to 2‰. Sufficient data from the south of France are only available after 27 ka BP. At 27–20 ka BP reindeer δ15N values in the south of France are relatively high, ranging from around 3‰ to 6‰. In the subsequent time block (20–15 ka and 15–13 ka BP) reindeer δ15N in the south of France is significantly lower (p ≤ 0.001 and p ≤ 0.001 respectively) by approximately 1‰. Although reindeer data from the south of France are limited in number during the Late Glacial interstadial (13–11 ka BP), their δ15N values appear to be higher than during the preceding time block (15–13 ka BP). Throughout the time periods covered, reindeer from the south of France have δ15N values that are generally higher than those from Germany and the UK by around 1‰ to 2‰. Belgian reindeer δ15N results are concentrated at 13–11 ka BP and are slightly higher than

Table 2 Statistical summary of reindeer δ15N values according to time block Time period Number of Mean Standard in ka BP individual deviation

Minimum Maximum Median

9–10 10–11 11–13 13–15 15–20 20–27 27–32 32–36 36–45

1.9 1.5 0.4 0.6 1.1 2.7 1.8 1.7 2.9

8 33 47 61 68 39 15 14 9

3.2 3.4 2.4 2.6 3.3 4.4 3.7 4.4 3.9

1.0 1.2 1.1 1.0 0.7 0.9 1.2 1.0 1.0

4.6 5.8 6.2 4.8 5.2 6.3 5.7 6.0 5.8

3.3 3.4 2.3 2.7 3.2 4.2 3.6 4.5 3.7

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Fig. 3. A: Reindeer δ15N plotted by country and time block. B: Box plots of Reindeer δ15N by country and time block. Box plots show the median, minimum, and maximum values, the inter-quartile range, and outliers. C: Mean reindeer δ15N and standard deviation Grey square = Siberia, white circle= Germany, grey diamond = UK, white square = Belgium, black circle= south of France. Country that box plot applies to can be seen by referring to samples directly above and below in A and C.

those in the UK and Germany at this time. Siberian reindeer δ15N results are available from three time blocks, with those at 27–20 ka BP being significantly higher by around 2‰ than those between at 15–13 ka BP and 13–11 ka BP (p ≤ 0.001 and p ≤ 0.001 respectively). This shows that the variation in reindeer δ15N values is not just a phenomenon of North West Europe. German reindeer δ15N values initially rise from

approximately 3‰ to 5‰ at 45–36 ka BP to around 4‰ to 6‰ at 36–32 ka BP. From 32 ka BP to 11 ka BP German reindeer δ15N values fall, with typical values of 1‰ to 3‰ observed during the Late Glacial interstadial. Mean reindeer δ15N in Germany is slightly higher (by approximately 0.5‰) during the Younger Dryas than during the Late Glacial interstadial.

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Fig. 4. δ15N of radiocarbon dated reindeer from Germany between 45 ka and 9 ka BP.

Of the radiocarbon-dated samples analysed, only those from Germany are present throughout most of the time period covered in this study and are relatively evenly distributed chronologically. The results of these samples alone (n = 21) show very clearly the gradual decline in reindeer δ15N values over the Late Pleistocene. (R2 = 0.4807) (Fig. 4). 4. Discussion During the Late Pleistocene, reindeer δ15N declined, with lowest δ15N values being seen after the LGM, between 18 ka BP and 11 ka BP. When time blocks are used to chronologically divide results this decline appears to be gradual, however, the use of time blocks could potentially mask the real chronological trend in δ15N (Fig. 2). δ15N of radiocarbon-dated reindeer from Germany also suggest that this decline was gradual (Fig. 4). δ15N values were higher during the Younger Dryas and early Holocene than during the Late Glacial interstadial. However, the timing and the magnitude of the changes in reindeer δ15N vary between different geographic regions. Although data are not available for each time period from all regions, a general geographical pattern can be seen. At 45–32 ka BP δ15N in the UK and Germany were similar. After 32 ka BP reindeer δ15N values were lower, although the depletion was greater in the UK than in Germany. In the south of France, δ15N values became lower after c.20 ka BP, however, data are limited prior to 27 ka BP. Thus the onset of the decline in reindeer δ15N appears to be earlier and of a greater magnitude in more northern regions than in the South of France. 4.1. Species comparisons Geographical variations in faunal δ15N have only been previously reported for horses and bovids (Stevens and Hedges, 2003; Drucker et al., 2003; Stevens and Hedges, 2004; Stevens, 2004). Although the δ15N of reindeer, horse and bovid collagen are not directly comparable due to their differing diets and physiologies, the pattern of δ15N variation over time can be compared. Even though data are limited, geographical variations in Bos/bovine δ15N values appear to be comparable to reindeer with relatively high values in both northern and southern Europe at 33–26 ka BP and divergent δ15N values at 18–11 ka BP, with lowest values being seen in northern Europe, higher values in

southern France and highest values in Italy (Iacumin et al., 1997; Drucker et al., 2003; Stevens, 2004). In contrast to large bovines, horse δ15N data are more plentiful. European horse δ15N values between 40 ka BP and 25 ka BP were relatively constant, in contrast to the gradually declining reindeer δ15N values. However, data from each country (UK, Germany, Belgium and south of France) during this time period are limited which may prevent recognitions of trends. Between 27 ka BP and 20 ka BP horse δ15N in the UK, Belgium (extremely limited data) and in the south of France were lower than pre-27 ka BP values. A rise in horse δ15N in the south of France after the LGM (c. 20–18 ka BP) is mirrored in the reindeer δ15N results. During the early part of the Late Glacial interstadial the pattern of horse δ15N values was very similar to that of reindeer, with particularly low horse δ15N being seen in the UK, Germany and Belgium, whereas in the South of France δ15N was slightly higher. However, as the Late Glacial interstadial progressed and subsequently during the Younger Dryas (11–10 ka BP) horse δ15N in the UK, Germany and Belgium rose dramatically. Due to the limited number of radiocarbon dated reindeer at this time it is impossible to tell if reindeer δ15N values rise through the Late Glacial interstadial, however, it is clear that reindeer δ15N was higher during the Younger Dryas in the UK and Germany than in the Late Glacial interstadial. Where data are available, horse δ15N in Italy remains relatively high and constant during periods where δ15N in more northern regions declined. Thus a lowering and subsequent rise in δ15N is observed during the Late Pleistocene for both reindeer and horse. This regional pattern in δ15N decline mimics the general pattern of climatic deterioration in Europe culminating at the LGM, with climate cooling beginning earlier and being more intense in northern Europe than in southern Europe (Huijzer and Vandenberghe, 1998). 4.2. Comparison with climatic record Although temperatures generally declined between 45 ka BP and the LGM, the climate is thought to have been extremely variable and the decline in temperature was interrupted by multiple short lived warm episodes (Table 3). At 45–36 ka BP temperature had already started to decline, with plant and insect data suggesting the mean temperature of the warmest month was between 10 °C and 11 °C and periglacial data suggesting the mean temperature of the coldest month was between − 27 °C and − 20 °C (Huijzer and Vandenberghe, 1998). Permafrost was not present in Northwest Europe during the early part of this time window. However, by 38 ka BP discontinuous permafrost had developed (Fig. 5A), suggesting mean annual air temperature were between − 8 °C and − 4 °C (Huijzer and Vandenberghe, 1998). Most of France was permafrost free at this time (Huijzer and Vandenberghe, 1998). Conditions were relatively arid although a slight precipitation increase occurred between 38 and 36 ka BP. A short-lived period of climatic warming at around 38–36 ka BP may have resulted in some permafrost degradation (Kasse et al., 1995). At 45–36 ka BP reindeer δ15N in the UK and Germany (both subject to discontinuous permafrost) was relatively high compared to those from same countries in subsequent periods.

Table 3 Summary of climatic conditions between 45 ka and 9 ka BP (data summarized from Coope and Brophy, 1972; Vandenberghe and Pissart, 1993; Kasse et al., 1995; Walker, 1995; Isarin, 1997; Huijzer and Vandenberghe, 1998; Lowe et al., 1999; Renssen and Vandenberghe, 2003; Vandenberghe et al., 2004) Temperature

Precipitation

Permafrost

9–10

Early Holocene

• Wetter

• No Permafrost

10–11

• Younger Dryas

• Relatively arid in the British Isles, Germany and Belgium

• Continuous permafrost in north Britain • Discontinuous permafrost in southern Britain, Belgium, and northern Germany • No permafrost in most of France

11–13

• Late Glacial

• Wetter

• No Permafrost in N.W. or S.W. Europe

13–15

• Late Pleniglacial

• Extremely Arid

• Permafrost boundaries continued to migrate further north

15–20

• Late Pleniglacial

• Warm interglacial climatic conditions • Temperatures similar to today • Mean temperature of warmest month = 15 °C to 17 °C • Climatic cooling • Re-advance of ice sheets • Mean annual temperature in northern Britain = b−8 °C • Mean annual temperature in southern Britain, Belgium, and northern Germany = − 4 °C to − 8 °C • Mean annual temperature in France = N− 4 °C • Rapid warming in British Isles & Germany, • Thermal maximum in British Isles, Germany and S.W. Europe • Mean temperature of the warmest month = 16 °C and 18 °C • First sustained warming in S.W Europe at 15 ka BP • Rapid warming in N Europe after 13.5 ka BP • Mean annual temperature in Uk and Belgium = − 9 °C to 1 °C • Mean temperature of coldest month = −21 °C to − 9 °C • Polar desert over most of Europe Mean temperature of warmest month = 8 °C to 11 °C • Mean temperature of coldest month = −21 °C to − 9 °C • Mean annual temperature in N.W. Europe = −8 °C • Low biological productivity • Mean temperature of warmest month = 8 °C • Mean temperature of coldest month = −25 °C to − 20 °C • Mean annual temperature in N.W. Europe =b − 8 °C • Significant climatic cooling • Ice sheet advance • Mean temperature of warmest month = 10 °C • Mean temperature of coldest month = −12 °C to−20 °C • Mean annual temperature in N.W. Europe − 8 °C to −2 °C • Mean temperature of warmest month = 10 °C to 11 °C • Mean temperature of coldest month = −27 °C to − 20 °C • Mean annual temperature in N.W. Europe = −8 °C to− 4 °C • Mean annual temperature in S.W. Europe =N − 4 °C

• Extremely arid

• Continuous permafrost marginal to thawing ice sheet

20–27

• Late Pleniglacial

27–32

• Mid Pleniglacial

32–36

• Mid Pleniglacial

36–45

• Mid Pleniglacial

• Slightly wetter but moisture locked up in ice sheets.

• A Slightly wetter but moisture locked up in ice sheets • Slightly Wetter

• Discontinuous permafrost extended north from northern France and Germany • Continuous Permafrost in British Isles, most of Germany and Belgium • Discontinuous permafrost extended down to the South of France • Permafrost development and advancement • No Permafrost in France and Germany or

• ?? Discontinuous permafrost in British Isles?? • Arid although a slight precipitation • No permafrost at start of interval increase occurred between 38 and • Permafrost developed by 38 ka BP in N.W. Europe 36 ka BP • Slight warming and permafrost degradation between 38 ka BP and 36 ka BP • No Permafrost in France

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Time Interval ka BP (uncal) Time period

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Fig. 5. Change in the distribution of Permafrost during the late Pleistocene. A = 41–38 ka BP, B = 36–32 ka BP, C = 27–20 ka BP, D = 20–14 ka BP, E = 13–11 ka BP (Late Glacial), F = 11–10 ka BP (Younger Dryas). Map redrawn from Huijzer and Vandenberghe (1998), and Renssen and Vandenberghe (2003). Map generated from ESRI map data using ArcGIS v.9.1.

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At 36–32 ka BP the climate was very similar to, but slightly warmer than the previous time interval, with botanical and coleopteran data suggesting the mean temperature of the warmest month was around 10 °C (Huijzer and Vandenberghe, 1998). Periglacial and botanical evidence suggest the mean annual air temperature was between −8 °C and −2 °C and mean temperature of the coldest month was between −12 °C and −20 °C (Huijzer and Vandenberghe, 1998). The discontinuous permafrost boundary shifted through the Netherlands several times during this time block (Fig. 2B) (Huijzer and Vandenberghe, 1998). Reindeer δ15N in Germany (permafrost free in central and southern Germany from which samples were obtained) was slightly higher than during the previous time interval, whereas in the UK (discontinuous permafrost possibly present) it was slightly lower. Between 32 and 27 ka BP climate cooled significantly and by 27 ka full glacial conditions were present. Biological productivity of the whole ecosystem was extremely low. Coinciding with this climatic cooling reindeer δ15N in Britain and Germany declined. The extent of the depletion was greater in the British Isles than in Germany. At 27–20 ka BP the mean temperature of the warmest month in northwest Europe was around 8 °C according to botanical and coleopteran evidence (Vandenberghe et al., 2004). However, there was a strong north-south thermal gradient (much stronger than today) and mean annual temperature in more northern regions was probably no more than 4 °C (Vandenberghe et al., 2004). Mean temperature of the coldest months was between − 25 °C and − 20 °C, thus the annual temperature range was large. Although annual precipitation rates were relatively high toward the start of this time interval (Huijzer and Vandenberghe, 1998) water became locked up in ice sheets, glaciers and permafrost, thus water availability was limited. Continuous permafrost was present throughout the UK (with the exception of areas covered by ice sheet), most of Germany and Belgium. Discontinuous permafrost extended from northern to southern France (Huijzer and Vandenberghe, 1998) (Fig. 5). Reindeer δ15N values in the south of France at this time interval were relatively high in comparison to subsequent periods. δ15N data from northern Europe are extremely limited during this time interval as the greater part of northern Europe was a barren cold desert with almost no biota present (Walker, 1995). During the time interval 20–13 ka BP the ice sheet decayed and progressively retreated to the north, resulting in permafrost formation in areas previously covered by ice (Huijzer and Vandenberghe, 1998). Precipitation rates during this time period were low and widespread loess accumulation suggests a high degree of aridity (Huijzer and Vandenberghe, 1998). However, ice sheet and permafrost melting would potentially increase water availability in certain areas. During the early part of this time interval (20–15 ka BP) conditions were still arctic. Sparse palaeobotanical and coleopteran data suggest mean temperatures of the warmest month were between 8 °C and 11 °C. The mean annual temperature in northern regions was around − 8 °C. The southern limit of continuous permafrost was marginal to the thawing ice sheet and discontinuous permafrost extended from across northern France into northern Germany (Huijzer and Vandenberghe, 1998) (Fig. 5D). Reindeer δ15N

41

values in both Germany and the south of France were lower than in earlier time intervals, however, values in the south of France were higher than those in Germany. During the later part of this time interval (15–13 ka BP) periglacial evidence suggests that as the permafrost boundaries migrated northwards, the zones of continuous and discontinuous permafrost became very narrow. Between 20 ka BP and 13 ka BP coleopteran data suggest mean annual temperatures in the UK and Belgium ranged from around − 9 °C to 1 °C. By 13 ka BP coleopteran evidence suggests that temperatures could have been rising as fast as 1 °C per decade (Coope and Brophy, 1972). By 15 ka BP to 13 ka BP reindeer δ15N values in Germany had declined further, whereas in France they rose very slightly. During this time interval Belgian reindeer δ15N values were similar to those of German reindeer. During the Late Glacial interstadial (13–11 ka BP), sustained widespread warming became established (Walker, 1995; Lowe et al., 1999). Temperatures rose very rapidly and between 13ka BP and 12.5 ka BP present-day temperatures were exceeded in Southern Europe and the British Isles (Walker, 1995). During the thermal maximum the mean temperature of the warmest month was between 16 °C and 18 °C (Walker, 1995). Permafrost was absent from Western Europe during the Late Glacial interstadial (Fig. 5E). Reindeer δ15N values in the UK, Belgium, Germany and Siberia were very low. Similarly horse δ15N values in the UK, Germany and Belgium were very low at the start of this time interval, however, they rose rapidly during this time interval (Stevens and Hedges, 2004). Only improving the chronology of reindeer δ15N through radiocarbon dating will allow us to determine if the rise in horse δ15N is mirrored in reindeer. An abrupt cooling occurred during the Younger Dryas (11– 10 ka BP) and alpine glaciers and ice sheets re-advanced (Vandenberghe and Pissart, 1993). Coleopteran data suggests mean temperatures of the warmest month were around 10 °C (Walker, 1995). In northern Britain continuous permafrost developed (suggesting mean annual temperatures of b − 8 °C), whereas discontinuous permafrost extended across southern Britain, Belgium and northern Germany (suggesting mean annual temperatures between − 8 °C and −4 °C) (Fig. 2F) (Isarin, 1997). Most of France was permafrost free at this time with mean annual temperature exceeding − 4 °C (Isarin, 1997). Younger Dryas reindeer δ15N values were higher in both the UK and Germany than during the Late Glacial interstadial. The rise in δ15N values appears to have been greater in the UK than in Germany, however, this may be a function of limited data from Germany. During the early Holocene (10 ka BP to 9 ka BP) temperatures rose rapidly, with conditions comparable to today being established by 9 ka BP. In northwest Europe Betula, Pinus and Corylus woodland replaced steppe tundra communities and in southern Europe Pinus, Corylus and Quercus woodland rapidly succeeded Artemesia dominated steppe vegetation (Walker, 1995). Mean temperatures of the warmest month were between 15 °C and 17 °C in the British Isles (Walker, 1995). Early Holocene reindeer δ15N values in the UK were slightly lower than those in the Younger Dryas.

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4.3. Potential parameters influencing reindeer δ15N With diet as the primary control on animal collagen δ15N, it might be suggested that the variation in Late Pleistocene reindeer δ15N was caused by dietary adaptation (to include more plants with low δ15N signatures) and physiological adaptations in response to changing climatic conditions. Reindeer eat relatively large amounts of lichen, particularly when the availability of other plants is limited. Consequently reindeer are typically nutritionally deficient as lichen is poor in protein (Drucker et al., 2001). When lichen is the predominant dietary intake, reindeer recycle their body protein into urea in order to cope with the low protein diet (Soveri, 1992). Elevated δ15N values have been reported in nutritionally stressed animals, which potentially may be caused by additional isotopic fractionation due to body protein mobilisation for the metabolic nitrogen pool (Hobson et al., 1993; Drucker et al., 2001). As climatic conditions became colder and drier towards the LGM, the availability of plant foods became more limited and thus the amount of lichen consumed by reindeers is likely to have increased. The physiological response to the increased nutritional stress as a result of dietary change should theoretically have resulted in a rise in reindeer δ15N coinciding with climatic deterioration. However, our results show the opposite of this, with δ15N falling as climatic conditions declined, suggesting dietary change is not the primary mechanism controlling Late Pleistocene reindeer δ15N. Furthermore, the gradual lowering of faunal δ15N during the Late Pleistocene is relatively consistent across species. Reindeer, horse, red deer and large bovines can all live within the same ecosystem, however, they exploit different ecological niches and are thus unlikely to all change their diets and physiologies at the same time and in the same way. Thus, we agree with previous studies (Richards and Hedges, 2003; Drucker et al., 2003; Stevens and Hedges, 2003, 2004) that dietary change is unlikely to be a primary mechanism causing the changes in Pleistocene faunal δ15N. The variations in reindeer δ15N are more likely to be due to a change in the isotopic composition of the plants they consume rather than the species of plants they select. Plant δ15N is dependent on soil δ15N, soil development, nutrient availability (nitrogen and phosphorus), mycorrhizal associations, soil acidity and nitrogen cycling (see Stevens and Hedges, 2004 for further details). However, the predominant mechanism determining soil and plant δ15N is the extent to which the nitrogen cycle is an open or closed system. i.e. the relative importance of within-ecosystem nitrogen cycling versus the relative importance of inputs and outputs (Handley et al., 1999). This in turn is controlled by climate, resulting in low δ15N observed in cold and/or wet areas and high δ15N seen in hot and/or arid areas (Amundson et al., 2003). If water availability was controlling nitrogen cycling during the Late Pleistocene, we would expect to see a rise in reindeer δ15N values when conditions became more arid and water availability became limited as water became locked up in ice sheets and permafrost. The reindeer δ15N results at 20–15 ka and 15–13 Ka BP show the opposite of this and, furthermore, declined at 13–11 ka BP when conditions became wetter. Thus it appears that water

availability is not the primary control on nitrogen cycling in the Late Pleistocene. Permafrost development has previously been suggested to coincide with faunal δ15N declines (Drucker et al., 2003; Stevens and Hedges, 2003, 2004). Although this may be the case for horse and bovids in the south of France (Drucker et al., 2003), it is not true of horse and reindeer δ15N in more northern regions. Moreover permafrost degradation occurred relatively rapidly after the LGM, when faunal δ15N in northern regions noticeably declined. By the Late Glacial interstadial, permafrost was absent from Western Europe. However, the lowest faunal δ15N values in northern regions are observed at the start of the Late Glacial interstadial. We suggest that the variations in reindeer δ15N during the late Pleistocene are linked to the influence of temperature and permafrost degradation on soil and plant δ15N. The gradual decline in reindeer δ15N values between 45 ka BP and the LGM could be a record of the nitrogen cycle's response to falling temperatures. Although reindeer δ15N values were relatively high at 45 ka BP to 36 ka BP compared to later reindeer δ15N values, they were significantly lower than those from oxygen isotope stage 5A, when warm temperate conditions were present in the UK (Stevens unpublished data). The lowering temperatures would have resulted in gradual changes in nitrogen cycles, moving them from open to closed systems, thus resulting in a decline in ecosystem δ15N. The most noticeable drop in reindeer δ15N occurs between 27– 20 ka BP and 13–11 ka BP. In Southern and Central France the decline in reindeer δ15N values coincides with permafrost degradation, with higher values observed at 27–20 ka BP when discontinuous permafrost was present and lower values at 20– 15 ka BP during permafrost degradation. The first sustained warming occurred in southern Europe around 15 ka BP. The slight rise in reindeer and horse δ15N in the south of France at this time suggests initial climate warming had influenced ecosystem δ15N. The more limited magnitude of the depletion in reindeer δ15N in Southern France may relate to the fact that the permafrost in this region was discontinuous rather than continuous. In more northern regions the lowest reindeer δ15N values occur later at 15–13 ka BP in Germany and at 13–11 ka BP in the UK (although no results are available from the UK during the 15–13 ka BP). Permafrost boundaries migrated northwards between 15 ka and 13 ka BP and extensive permafrost degradation occurred. The greater magnitude of the depletion in reindeer δ15N in northern regions may relate to the previous presence of continuous permafrost. Widespread climatic warming in northwest Europe occurred after 13.5 ka BP (Walker, 1995), yet reindeer and horse δ15N values in the UK, Germany and Belgium were very low at the start of the Late Glacial interstadial. This suggests there was a delay in the response of ecosystem δ15N to the rising temperatures which may be linked to permafrost degradation and soil development. Evidence from modern ecosystems support this possibility, with exceptionally low soil δ15N values of around − 1‰ and plant δ15N values of around−11‰ being reported in the forefront of the retreating Lynmann Glacier (Hobbie et al., 2005). These low

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soil and plant δ15N values are likely to occur because initial N inputs to the soil (e.g. via weathering from primary minerals, atmospheric N deposition, biological fixation) are 15N depleted. The plants in such nutrient-poor environments are likely to have relied on mycorrhizal associations to aid their uptake of nitrogen, as plants do in the present day arctic (Smith and Read, 1997; Hobbie and Hobbie, 2006). Plants with these ericoid and ecto-mycorrhizal association often have very depleted δ 15 N values as low as − 12‰ (Handley and Scrimgeour, 1997). Moreover, in areas proximal to the ice sheets nitrogen cycling had essentially stopped during the LGM and it may have taken some time for the system to re-start. Although temperatures started to rise after the LGM, plant δ15N (and thus reindeer δ15N) remained low. Limited directly radiocarbon dated reindeer δ15N during the Late Glacial interstadial makes it impossible to establish how quickly they responded to increasing temperature, however, horse δ15N rose rapidly during this time interval (Stevens and Hedges, 2004). The Younger Dryas cooling appears not to have been long or severe enough to effect ecosystem δ15N even though discontinuous permafrost extended across the UK. The dates for the Younger Dryas Chronozone used in this study are those defined by Mangerud et al. (1974): 1000 uncalibrated radiocarbon years starting from 11,000 BP and ending at 10,000 BP. However, establishing the duration of Younger Dryas is not straightforward. Firstly the radiocarbon plateau at 10,000 BP affects calculations of the duration and secondly the duration varies regionally (Lotter, 1991). Evidence from the Grip Ice Core suggest the Young Dryas lasted for 1240 Years from 12,890 to 11,650 ice core years BP (Stuiver et al., 1995), whereas laminated varve sediments from Soppensee (Switzerland) suggests a duration of 680 to 720 years (Lotter, 1991). Thus using Mangerud et al's Younger Dryas definition may have resulted in grouping reindeer from regions where the Younger Dryas was short, with those where it was more persistent and may have had a greater affect on the reindeer δ15N values. The few available radiocarbon dated horse δ15N values from the Younger Dryas are however, substantially higher than those from the Late Glacial interstadial (Stevens and Hedges, 2004). Renewed climate warming during the early Holocene (10–9 ka BP) saw reindeer δ15N values in the UK slightly decline. As with the post LGM low reindeer δ15N values, this decline might relate to permafrost degradation, as during the Younger Dryas discontinuous permafrost was present across the UK. Further investigation of the Younger Dryas and early Holocene reindeer δ15N may help elucidate links between permafrost degradation and faunal δ15N. It is clear that the relationship between climate and faunal δ15N is not a direct one to one correlation. The lack of radiocarbon dates for many of the samples forces the grouping of data based on associated dates. With stratigraphic mixing often occurring at archaeological sites several of the non-radiocarbon dated samples could potentially be assigned to the wrong time block. The extensive scatter observed within each time block could be due the grouping of samples. This scatter may relate to rapid climate variation and further radiocarbon dating may help elucidate further chronological trends within this dataset.

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However, several radiocarbon plateaux have occurred during the last 50,000 years potentially causing errors in the radiocarbon dates. Although calibrating some of the dates is possible, some of the significant changes in faunal δ15N values occur during these plateaux, making it extremely hard to determine the rate of change in faunal δ15N. Disparities in the timing of variations in faunal δ15N and climate may also be because the nitrogen cycle is a complex system, which is likely to take time to respond to climate change and that initial responses may not be detected in the isotope record. 5. Conclusions Reindeer δ15N data confirms temporal and geographical trends previously observed in horse and bovid δ15N values, with the onset of the decline being earlier and of a greater magnitude in northern Europe compared to Southern Europe. No correlation was observed between reindeer δ15N and permafrost development. Correlations between reindeer δ15N and permafrost degradation during the Late Pleistocene suggest this parameter may have influenced ecosystem δ15N. A lag in the response of the nitrogen cycle to increasing temperatures is observed which may relate to the influence of permafrost degradation on soil and plant δ15N and thus faunal δ15N. The renewed climatic cooling during the Younger Dryas did not see a fall in reindeer δ15N, however, the limited reindeer data from the UK for the early Holocene suggest permafrost degradation may also influence the post Younger Dryas reindeer δ15N values. The link between climate and faunal δ15N values is complex. Further Pleistocene data and modern studies are required to establish relationships between the two. However, faunal nitrogen isotopes provide insights into past biogeochemical cycles that cannot be currently gained from other palaeoenvironmental proxies. Further isotopic investigations and radiocarbon dating will provide us with a better understanding of how the nitrogen cycle responded during periods of rapid climate transition. Acknowledgements We would like to thank Peter Ditchfield for technical assistance with isotopic analysis. This project was funded by a NERC studentship to R.E.Stevens (NER/S/A/2000/03522) and Europeanfunded “Improving Human potential program: Access to Belgium Collections (ABC)” and “Synthesis” grants to R.E. Stevens. Our thanks go to Jef Vandeberghe of Vrije University Amsterdam and Erik Hobbie of the University of New Hampshire for communications on permafrost histories and mycorrhiza, respectively. Cameron Petrie is thanked for his assistance with graphics. We would like to thank the following institutions and people for providing samples for analysis: Andy Currant at the Natural History Museum London, Generaldirektion Kulturelles Erbe, Rheinland-Pfalz, Tom Lord, The Royal Belgian Institute for Natural Sciences, Wells Museum, The University of Bristol Speleological Society Museum, Torquay Museum, Creswell Crags Museum and Education Centre, University of Cambridge Museum of Archaeology and Anthropology, Buxton Museum, Stoke-OnTrent Potteries Museum & Art Gallery, Lancaster Museum.

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