The studied sites fail to develop s sensu stricto because endokarstic deposits undergo different sedimentary processes from those affecting conventional ss. Although they can experience either post-depositional geogenic or nic effects, it is noteworthy that these environments are less subaerially exposed and less affected by atmospheric weathering processes (freeze-thaw, solifluction, leaching and cementation). Therefore, endokarstic deposits develop less pedological postdepositional modifications than open air sites17.
Early-Middle Palaeolithic. Gran Dolina site recorded industries sting from the Lower Pleistocene, from about 1.0 to 0.125 Ma18. High EF values of Zn and Cu were founded at level TD 9 (Fig. 2 and Supplementary Table S1). This level TD 9 is located near to a guano deposit with an age of 0.45 Ma19,20. These data are in agreement with previous endokarstic geochemical studies containing bat guano, showing Cu and Zn pollution in the vicinity of the dung5. Although modern deposits of bat guano are enriched in N and P as primary geochemical signal, deposits of diagenetically altered guano are enriched in Zn and Cu due to increased organic matter degradation ociated with decreased availality of nitrogen and sulphur21. It ought to be highlighted that the time estimation for this early stages of diagenesis ociated with organic matter degradation is only of decades. This implies that the geochemical values that persist in the archaeological record do indeed record the palaeochemistry of the sediment near the time of its deposition21.
Zn and Cu are essential micronutrients for plant development and activation of enzymes; it has also been doented that the concentration of these metals or elements in plants is closely related to the levels of the elements in the s22. In the studied site, only the closed samples TD9-10 and TD9-11 show an increase in metals plausibly related to guano (Fig. 2 and Supplementary Table S1). The Pear coefficient (Cu-Zn = 0.95) confirms the common distribution of these heavy metals in Gran Dolina and points that the Cu and Zn signal due to guano has been preserved and did not suffer differential leaching. Thus, the overall pattern of the pollutant behavior observed for Gran Dolina suggests low molity of heavy metals in the profile, ociated with the occurrence of bonates and organic matter.
From an archaeological point of view, the bat guano deposits do not point towards an occasional compost of the cave by the inhatants, because the aculation of appreciable amounts of guano is only possible during non-occupational periods23. In fact, the level TD-9 has not yielded any fossil remains24. Later on, Homo populations occupied the cave, and three sublevels inside TD-10 with abundant fossil remains and lithic industry can be identified25. Nevertheless, human inhatants were not in contact with the studied palaeoguano deposit because it was sealed. In any case, this study confirms that guano deposits, uquitous in caves, represent the source for the heavy metal input to Homo environments.
Middle Palaeolithic. Deposits have been studied at Gorham’s (level IV) and Vanguard Caves, where well-preserved hehs have been reported26. Sediment samples with outstanding heavy metal contents (V-9; V-10 and V-21 from Vanguard and GOR-1 and GOR-2 from Gorham’s) have been collected at the levels precisely characterized by occurrence of these hehs (Figs. 2 and 3). In the case of a heh sample from Gorham’s Cave (GOR-2) the values reached (Ni = 493.8 ppm; Cu = 1592.6 ppm; Zn = 4158.1 ppm) can be considered as a Cu-Zn-Ni polluted s by modern criteria16, and it becomes the est doented evidence of pollution generated by Homo, and perhaps a milestone in the so-called Anthropocene27.
The values obtained at Gorham’s heh are so high that require a detailed explanation. The presence of Zn, Ni and Cu in wood ash remains are related to their presence in plants as micronutrients, but these element aculations might be also promoted by sea spray, percolation and aculated by hehs active bon.
In order to discuss metal sources, Zn isotopic ysis was performed, which is a rot proxy to identify anthropogenic Zn origin28. The Zn isotopic values were obtained from two samples (with 8 replicates) GOR-2 (spliced as GOR-2a and GOR 2b) and GOR-12 (Supplementary Table S2). Both correspond to samples with high EFZn, and GOR-2 was recovered from a Neanderthal well preserved heh (Fig. 4). Values from GOR-2 and GOR-12 reached δ66ZnMC 3-0749 L = + 0.79 ± 0.02‰ (2 SD) (n = 4) and δ66ZnMC 3-0749L = + 0.52 ± 0.02‰ (2SD) (n = 3), respectively (Supplementary Table S2). Temperatures in open fires do not reach the 906°C required for Zn vaporization and Zn isotope fractionation, but if it occurred it can explain why we reached heavy values in fire residues because light fly ashes show light values28. Therefore, hehs preserve an original isotopic signal that allows us to disd a marine source [δ66Zn = + 0.3–0.4‰ for the marine soluble fraction of Atlantic marine aerosols29] and suggests altered organic matter as main origin, similar to deep ss30 [δ66Zn = + 0.22 to + 0.76‰].
We acknowledge Dr. C. Finlay and archaeological team for Gorham’s picture.
Organic guano, linked to rds and bats appeared at Level I and II of Gorham’s Cave. No evidence of Zn and Cu percolation from these recent deposits have been found, and pollen and macro-botanical stratigraphy is well established for the Gorham’s Cave levels without any suggestion of picle percolation31. Previous micromorphological indicates extensive diagenesis and the presence of charred and rubefied guano in most comtion zones32. Therefore, Gorham’s high levels seem to be related to heh reutilization, occurrence of fires within palaeoguano substrate and diagenesis.
Another important finding in this site is that the highest Zn and Cu contents are not only found at well-defined hehs, but along entire levels in both caves. This is also exemplified in Vanguard Cave, level 9 (Fig. 3, shaded level), where the highest Zn levels are located and where evidence of human activities (bone remains, tools) has been observed. The absence of these enrichments in levels above and below the hehs points towards an in situ enrichment since no migration of these elements can be detected along the sedimentary profile. The pattern of Zn along the entire level can be attributed to different mechanisms like ash fly and/or wood ash redistribution. Wood ash fly is also enriched in Zn and Cu and would be distributed along the cave when the fire was active by convection. The studied caves do not show vertical cracks or chimneys, and fumes must go along the entire cave. Redistribution of ashes from hehs to ing areas has been described previously in Neanderthal sites33. The use of ash has been linked to their thermal and aseptic properties. This evidence indicates that Zn and Cu sediment content can be used as an anthropic proxy, when extensive diagenesis and/or guano inputs can be disded.
In this sense, the experimental fires conducted with wood from three different tree species growing in limestones in a National Park (far from potential pollution sources), showed heavy metal enrichment with respect to the geochemical base line (Supplementary Table S1), specially of Cu and Zn. The continuous fires developed in the same cave hehs, as well as the effect of ash spreading in the ground of ing areas by Homo populations33, contributed to the concentration of these elements in the ss, and therefore, the risk of heavy metal exposure increased as well. In those levels with human-activity evidence, the concentration of the heavy metals in heh levels, as well as in laterally equivalent levels, might depend on the continuity of the hehs th time.
All these data show that Neanderthals were exposed to an environment enriched in heavy metals and fumes inside the caves they occupied. Although in some cases, some of these levels can be considered polluted (according to criteria based on ecological effects16), it is not possible to conclude whether they reached toxic levels with only this evidence. However, this environment might have made the Zn exposure worse in the case of Neanderthals as their diet had a high cosumption of shellfish34, marine resources35, and red meat36, related to very high Zn intake. Zn is an important micronutrient and its consumption is vital for human reproduction and long-term evolution37; however, high Zn intake can cause chronic Zn toxicity triggering anemia and impaired immune function, but normally Zn excess is excreted (European Union Comission- Scientific Committee on Food)38.
It is expected that fumes from fires should be the most damaging factor in these restricted cave environments because ash fly contain higher levels of dioxins and heavy metals than the bottom ash39. Neanderthals and anatomical modern humans used fires from at least 300 kyr in a complex way40,41. It is worth questioning if long-term Neanderthal exposure to fire-derived contaminants might have played an important role in their hi. Plausibly, for a limited metapopulation42, a decrease in fertility ociated to smoke43 might have played a role in Neanderthal population dynamics. Interestingly, recent studies have dnstrated that several Neanderthal-derived alleles were affected by behaviour, suggesting that Neanderthal alleles continued to shape human ology44.
Upper Palaeolithic. Levels represented by El Pirulejo45 are quite different to the previous ones (Fig. 2) since guano and well defined hehs are not present. As postulated in a former study46, levels of Pb at level P/3 (Upper Magdalenian) are outstanding, which can be linked to the use of galena. A few fragments of this mineral have been recovered in this site. Galena is lead sulphide (PbS) that has been used since prehistoric times as a source of pigment, as a raw material to manufacture beads, pendants or other objects, and to sprinkle over the dead in mortuary cernies47. The latter was the case of its earliest identified use in El Mirón cave (Spain), ociated with an Upper Palaeolithic burial (Magdalenian)48. Nevertheless, the presence of Bronze Age burials in upper levels and the concentration of Pb located just at P/3 to P/2 transition could also indicate contamination by degradation and leaching of galena fragments or other metal objects from the upper burials.
In resume, We have doented evidence of palaeopollution in Homo environments, which in some cases were related to Homo activities. Data obtained from Gran Dolina indicate that caves contain deposits enriched in heavy metals due to diagenetical processes affecting bat guano, but direct contact with Homo did not take place at this site. Middle Palaeolithic (Neanderthal) populations from Gorham’s and Vanguard Caves appear to have lived in environments with high levels of Cu and Zn due to comtion activities, promoted by fly ash and wood ash redistribution, and ociated with guano altered deposits. The difference in these element contents between both Gibraltar caves can be related to a higher occupation/re-utilization in Gorham’s and/or higher input from guano deposits (including charred and rubefied guano), not present in Vanguard. The high concentration of Zn-Cu in Gorham’s can have also been promoted by compaction and diagenesis from the original deposits.
This uquity of certain heavy metals allows us to identify these elements as an anthropogenic geochemical proxy when the sedimentary input of guano and extensive diagenesis is disded. The highest Pb content and galena mineral is found during the Upper Palaeolithic at the site of El Pirulejo, suggesting a common use of this mineral.
All these data indicate that Homo species inhated caves with high heavy metal levels, at least from the Middle Palaeolithic. Therefore, the influence of long-term heavy metal s exposure may have been very limited, but it depends on how they interacted with these sediments.
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