On the other hand, the biometric analysis of I. alonensis shell widths and heights indicates a narrow selection pattern of land snail sizes. The comparative analysis between the archaeological specimens and modern land snails raised in the laboratory suggest that most of the gathered individuals were older than one year, and those younger than 45 weeks were not gathered at all. Such a strong age selection pattern suggest sustainable exploitation of I. alonensis based on knowledge of its reproductive cycle.

Anthropogenic accumulations of large snails dated during the Gravettian period (31.3–26.9 kyr cal BP) have been reported on the basis of taxonomic, taphonomic and biometric data and their association with occupational features, lithic and faunal assemblages. Land snails found in the Gravettian levels of Cova de la Barriada reveal the existence of mono-specific gathering strategies focused on large pulmonate gastropods during the Early Upper Palaeolithic. Taphonomic analyses indicate significant differences between the breakage patterns documented for the Gravettian levels of Cova de la Barriada and those produced by other land snail accumulators such as birds, hedgehogs, badgers, mices and rats. The most significant difference is the high representation of complete shells. Such a pattern is very uncommon in the shell remains left by other land snail predators, which systematically destroy part of the shell spiral, the sides or the aperture for gaining access to flesh. As it has been observed before, mechanical breakage due to sedimentary compaction was responsible for some land-snail fractures, as reported with other zooarchaeological remains. However, the high frequencies of complete specimens and their clear spatial association with combustion structures advocate for the cultural origin of the land snail accumulations as food remains. Furthermore, the micro-DXR analysis indicates differences in the aragonitic composition between live and fossil specimens, suggesting that the archaeological samples were heated under controlled conditions (below 375°C) given the null conversion of aragonite into calcite. Recent experiments on the prehistoric cooking process of the large edible land snails Helix sp. indicate that roasting land snails on embers between 5-8 minutes is the most plausible technique documented at Pupicina cave, on the eastern Adriatic area, leaving barely visible traces of burning [57] . In addition, our analytical protocol using DXR indicates that because of post-depositional bleaching, fossil specimens without clear macroscopic evidence of burning were heated as well, given the presence of different aragonitic signals not found in modern specimens. Furthermore, charcoal data from the combustion structure BM, which delivered 112 complete land snails, provides fresh evidence about the fuel employed in the cooking process of the land snails: Pinus nigra/sylvestris and juniper charcoals, most of them between 2 and 15 timber rings. The structure BM is different from other examples of combustion structures used to cook land snails dated to the Capsian in Algeria. The Capsian examples consist on hearth pits delimited by vertical stone slabs and filled by two layers of heated stones between which the land snails are boiled by heating radiation [58] .

2. Cultural and economic implications of land snail consumption during the Early Upper Palaeolithic

The body of archaeological evidence about the consumption of edible land snails by humans prior to the Late Glacial Maximum is scarce, and its interpretation as food remains is rarely accepted for such an old chronology [17]–[18]. In Table 8 and Figure 9, we present a list of Upper Palaeolithic contexts recording the first cite about the use of terrestrial gastropods as a food resource, with the corrected chronology and taxonomic identification.

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larger image TIFF original image Download: Figure 9. Map of Upper Palaeolithic sites of the Mediterranean basin displaying the earliest occurrence of land snails as food remains. Bold numbers indicate the calibrated chronology in ka yrs (see also table 8). The black & white symbols denote Early Upper Palaeolithic sites with a consistent pattern of small prey exploitation including shellfish and lacking evidence of land snail consumption. https://doi.org/10.1371/journal.pone.0104898.g009

The first acknowledged evidence of land snail consumption by humans [17] comes from the Mumba-Höle site (Tanzania), a reference archaeological sequence of East Africa. Melhman [59] reported the existence of middens of the large land snail Achatina sp. in both beds III-lower and V dated to 31070±500. It is worth noting that such accumulations occurred in association with rich artefact assemblages, oyster shell beds and crescent microliths. Melhman interpreted the lithic industry of level V as a Middle Stone Age (MSA) and Later Stone Age (LSA) transitional industry. However, new excavations at this site and the production of new dates allow revision of the previous cultural interpretation of level V as a transitional industry to a full LSA lithic assemblage [60]. Recent contributions on the chronology of the archaeological sequence[61], through optically stimulated luminescence dating of quartz and feldspar grains, yielded however, older ages for levels III inf (36.8±3.4 kyrs) and V upper (49.1±4.3 kyrs). The specific study of the land snail assemblages remains unpublished.

In the Levant, the Ksar 'Aqil (Beirut) site yielded land-snail accumulations in Level 3b of Tixier's excavations [62], dated to between 22,000 and 23,000 BP uncalibrated [63]. It is difficult to maintain, with the current data, the older use of land snails as food resource in this region. For instance, further north, at Üçagizli Cave (Hatay, Turkey), a well-documented archaeological sequence of the Initial Upper Palaeolithic and the Ahmarian dated to 44–33 kyrs cal BP [64], there were found several land snail species, including Pomatias elegans, Xeropicta sp. and Helix cf. engaddensis, which accumulated through natural processes. Despite the significant representation of the small game at the site, with several species of fish, leporids, birds, tortoises and shellfish, there is no evidence for the use of pulmonate gastropods as food.

In the Argolid, Franchthi Cave and Klissoura Cave 1 have been thoroughly investigated, yielding a different chronological pattern for the consumption of Helix figulina, the main edible land snail species documented in the Late Pleistocene and Early Holocene archaeological deposits of this region. At Klissoura Cave 1, Helix figulina land snails occur from the Upper Palaeolithic to the Mesolithic. The shells found in the Uluzzian and the Early Aurignacian units (Layers V and IV) lack evidence of human modification [65]. In contrast, land snails become moderately abundant from the Upper Aurignacian (Level IIIc), with evidence of high percentages of broken lips, interpreted as evidence of human consumption, growing exponentially up to the Mesolithic (Layers 3–5). No radiocarbon information is available for Layer IIIc, whose chronology spans between the dates of the underlying Middle Aurignacian units (IIIe-IIIg), dated to 35–36 kyrs cal BP, and the overlying Upper Palaeolithic levels (III″), dated to c. 28 kyrs cal BP [66]. The antiquity of land snail exploitation documented at this site is not mirrored at the neighbouring Franchthi cave, where food debris of Helix figulina occurs much later, in the Epigravettian units (S2-T3) dated to 15–12 kyr cal BP [67].

At Haua Fteah cave in Cyrenaica, land snail accumulations interpreted as food debris were reported in the pre-Aurignacian, Iberomaurisian, Capsian and Neolithic layers of McBurney excavations [68]–[69]. New excavations [70]–[71] have documented land snails throughout the whole archaeological sequence. Detailed quantitative information about land snail occurrence is available for the uppermost part of the sequence, Layers III-X, from the Historic period up to the Libyco-Capsian [72]. At these layers, as well as in the neighbour site of Hagfet al-Gama, the shells of Helix melanostoma, Rumina decollata, and Trochoidea cretica are thought to represent food debris. For the earlier prehistoric occupations at Hauah Fteah, preliminary data indicates land snails were used as food resources during the Oranian (c. 14–10 ka cal BP) to a lesser extent than during the Lybico-Capsian, whereas during the Dabban period (c. 40–15 ka cal BP) their use seems occasional, and no food molluscs are documented during the Mousterian layers [70]. Future works at this site are needed to elucidate the beginning of the systematic and continuous exploitation of land snails along the Dabban occupations, whose radiocarbon record covers a chronological span of more than 25,000 calendric years [71].

In the Balkans and Italy, cultural accumulations of land snails have been reported from the Late glacial and the Early Holocene onwards [52], [73]–[76] but not during earlier periods. For instance, Level G of Riparo Mochi (Aurignacian) yielded land snail accumulations (not taxonomically determined), but on the basis of the taphonomic evidence such as perforation marks, the lack of burning traces and spatial distribution, Stiner [3] suggested they were accumulated by avian and small mammal predators. In southern Italy, Grotta della Serratura, a long cave sequence spanning the Gravettian, Evolved Epigravettian and Late Epigravettian occupations is paradigmatic. Despite the presence of marine and terrestrial molluscs throughout the sequence, the consumption of Helix cf. ligata is just documented in the Late Epigravettian layers [75]. In contrast, in Sicily, the pulmonate gastropod Eobania vermiculata is found throughout the archaeological sequence from Grotta d'Oriente, from the Late Upper Palaeolithic to the Late Mesolithic, even though there is no evidence of human collection for food consumption [77]. Other Late Glacial and Early Holocene Italian sites such as Grotta della Madonna a Praia a Mare and Grotta del Mezzogiorno have provided abundant evidence of Helix cf. ligata land snail shells [78]–[79]. However, its interpretation as food remains is still inconclusive because the malacological assemblages come from old excavations.

In the Magreb, at Grotte des Pigeons, recent malacological studies [80] demonstrate an intensive exploitation of land snails associated to the grey series of Iberomaurisian affiliation dated to 15–12.5 kyrs cal BP. In contrast, the land snails found in the underlying yellow series were not the result of human agency. At the same site, a few large specimens of Otala punctata were reported in the Aterian levels, associated with thin ash lenses dating to around 80,000 BP, suggesting “a very small scale exploitation”[80∶13] even though no detailed description and quantification are available for such an older occurrence.

Finally, at Cueva de Nerja (south Iberian Peninsula), accumulations of Iberus alonensis are found throughout the archaeological sequence, from the Gravettian to the Chalcolithic. The oldest occurrence is documented in Levels 13 and 11 of the Vestíbulo chamber, where continental gastropods are dominant during the Gravettian and during the subsequent Solutrean occupations [81]–[82].

According to this review, the exploitation of edible land snails is a subsistence activity restricted to anatomically modern humans post-dating the Middle to Upper Palaeolithic transition, geographically restricted to some of the warmest European regions during the final stages of the MIS 3. During the beginning of the Early Upper Palaeolithic, edible land snails appear have accumulated in archaeological deposits through natural processes and/or non-human predators in the Eastern and Central Mediterranean as well as the Magreb. Our study reveals, however, that the exploitation of large edible land snails in the Iberian Mediterranean region is clear from the beginning of the Gravettian techno-complex c. 31.3–26.6 kyr cal BP onwards as indicated by the Solutrean and Magdalenian levels of Nerja cave. While the information about the taxonomic composition, taphonomy and biometrics of some key sites for the Early Upper Palaeolithic, Haua Fteah and Ksar 'Aqil, is rather limited, the remaining datasets clearly point to a later occurrence, associated with posterior Epigravettian or Iberomaurisian contexts after the Late Glacial maximum as documented in Grotte des Pigeons, Grotta della Serratura or Franchthi Cave. The main question posed by the Gravettian accumulations of land snails found at Barriada and Nerja caves addresses the origin of such a new economic behaviour, not reported in the Iberian Peninsula during the Middle Palaeolithic nor the Aurignacian periods.

Cova de la Barriada suggests that the exploitation of I. alonensis land snails by humans entailed a rigid mono-specific gathering strategy and a clear age-size selection pattern, culturally transmitted and maintained through generations. Their incorporation into the human subsistence systems during the beginning of the Gravettian could be interpreted as a regionally specific component of a broader range of complementary foraging and gathering activities focused on small prey [29], entailing a marked gender or age-related division of labour operating in a context of population growth [83].

Considering both the exploitation of marine molluscs during the Middle Palaeolithic and the lack of evidence on land snail consumption in Early Upper Palaeolithic contexts prior to the 31 ka yrs cal BP, there are no arguments to interpret the incorporation of land snails into the human diet in terms of different cognitive capabilities between Neanderthals and Anatomic Modern Humans. Rather, as the eastern and southern Iberian record indicates, the appearance of this new subsistence activity was coeval with other demographically driven transformations such as the significant increase of the number of sites [84]–[86], and beginning of the production of portable art [87]–[88].