Large Mammals as VitaminC Sources for MIS3 Hominins: Comparison
View Latest Version
Please note this is a comparison between Version 2 by Catherine Yang and Version 1 by José Luis Guil-Guerrero.

The acquisition of large prey by hominins living during the Marine Isotope Stage 3, including Neanderthals and Anatomically Modern Humans, had nutritional and bioenergetic implications: these contain high fat amounts, provide a high energy return, and the strategies and skills required to acquire small prey were different from those required to acquire the former. Vitamin C availability at several MIS 3 periods could have had a strong seasonal variability and would have been decisive for hominin groups’ survival. 

  • Neanderthals
  • anatomically modern humans
  • vitamin C
  • large fauna

1. Introduction

Hominins living during the Marine Isotope Stage 3 (M3H, ~60–20 ka) were Anatomically Modern Humans (AMH), Denisovans, and Neanderthals. The latter inhabited Western Eurasia from approximately ~430 ka [1], and their demise took place after Anatomically Modern Humans’ (AMH) dispersal, at ~42 ka [2,3][2][3]. Different hypotheses have been formulated for this event: abrupt climate and vegetation change [4[4][5],5], competitive exclusion [6], pathogens [7], assimilation [8[8][9],9], demographic weakness [10], and volcanic eruptions [11]. The proposed mechanisms are not mutually exclusive, and their relative roles may have also varied regionally and temporally [12]. Mitochondrial DNA nucleotide sequence differences among Neanderthals suggest three different geographical populations occurring in Western Europe, Southern Europe, and West Asia [13], while the earliest AMH in Europe are thought to have appeared around ~46 ka, and thus were directly contemporary with the latest European Neanderthals [14].
The demise of Neanderthals could have been linked to the paleoecology of other mammals. The biogeographical analysis of a database of European mammalian fossils for MIS 3 revealed the ecological conditions of this period, in which Neanderthals appear to belong to the extinct southern grouping of Late Pleistocene Megafaunal elements [15]. The geographical distribution of large mammals (>500 kg, corresponding to Bunn’s criteria [16], levels 4–) at MIS 3 confirms a retreat toward the south and west of Neanderthals [15], although it has been proposed that some millennia before their demise, about 59–49 ka, Neanderthals entered southern Siberia [17].

2. Controversy in the Diet of M3H

Northern European M3H had to face a medium with a great shortage of edible plants, with seasonal intensity, so they relied mainly on foods of animal origin for most of the year. For instance, Neanderthals seem to have had a predilection for large- and mega-faunal elements, and the woolly mammoth (Mammuthus primigenius Blumenbach, 1799) was the more prominent animal belonging to the Megafaunal complex. Its extinction is largely attributed to the worldwide wave of extinction of megafauna, which took place prior to the Holocene [18].
Both lithic and faunal assemblages and stable isotope analysis provide a measure of human diets in the past and support the idea that M3H subsistence was based mainly on the consumption of large herbivores [19,20,21,22][19][20][21][22]. Stable isotope analysis of human skeletons has been used successfully for years to determine the type of food animals consumed by M3H. For instance, the use of Ca isotopes allowed the dietary reconstruction of an OIS 5 Neandertal fossil from Southwest France, pointing out a predominantly carnivorous diet, composed of a mixture of various herbivorous prey [23]. The diet of Neanderthals was also assessed by the strontium–calcium (Sr/Ca) and barium–calcium (Ba/Ca) ratios of bones, which predicted that such a diet was composed of about 97% of meat with a weak contribution of vegetables or fish [24]. Recently, the evaluation of C and N stable isotope ratios in bone collagen allowed the assessment of the Paleolithic diet of Siberia and Eastern European hominins, and it was found that the Neanderthal diet in Siberia was based on the consumption of terrestrial animal protein, while for a Neanderthal/Denisovan hybrid the contribution of aquatic food like freshwater fish was suggested [25]. Overall, Paleolithic AMH in Siberia and Eastern Europe procured mainly terrestrial herbivores, such as reindeer, horses, and bison. Moreover, there is evidence that the oldest AMH individuals supplemented their diet with a certain amount of aquatic food [25]. In this context, isotopic analyses suggest that mammoths and plants were important contributors to the diets of the oldest AMH from far Southeast Europe [26], and that both Neanderthals and AMH relied on the same terrestrial herbivores, whereas mobility strategies indicate considerable differences between Neandertal groups, as well as in comparison to AMH, who exploited their environment to a greater extent than Neanderthals [27].
The use of plants as foods by Neanderthals, whether it was seasonal or occasional, has been documented [28,29][28][29]. Such use was inferred from the analyses of dental calculus, which has led to the argument that Neanderthals ate as many plants and used as many species of plants as modern humans do [30]. However, it is likely that a combination of mobility, energetics, and fatty acids requirements prevented high plant use by Neanderthals [31]. It must be taken into account that the consumption of herbivores’ stomach contents, which contain high amounts of carbohydrates, should be considered as a possible source of plant foods, including “medicinal” ones, in the archeological and fossil records [32]. Furthermore, the possible cooking of plant foods by Neanderthals is a hot topic, which currently promotes much debate among researchers.
Another means of reconstructing the diet and behavior of Neanderthals is dental macrowear analysis. Based on comparisons with modern hunter–gatherer populations, Neanderthals shows high dietary variability in Mediterranean evergreen habitats but a more restricted diet in upper latitude steppe/coniferous forest environments, suggesting a significant consumption of high-protein meat resources in this environment [33,34][33][34].
Overall, all the evidence points to the fact that Neanderthals were adapted to an essentially carnivorous diet, which was more marked for Northern European populations. This fact is supported by some morphological features of Neanderthals, such as their large lower thorax, which may represent an adaptation to a high-protein diet [35]. In addition to terrestrial mammals, various studies prove the use of birds and fish by Neanderthals, especially in the northwestern Mediterranean [36,37,38,39[36][37][38][39][40],40], but in all cases the most appreciated part of the prey by hunter–gatherers, given their high-protein diet with little access to carbohydrates, would always have been the fat [41,42][41][42].
Coexistence and hybridization between AMH and Neanderthals are known to have taken place in the Near and Middle East [43]. Therefore, it is more than likely that in some areas of the Neanderthal range, the coexistence of AMH and Neanderthals led to a reduction in their resource pool, and the technologies and cognitive abilities of the former allowed them to access a wider range of resources [44].
All these facts suggest a complex food scenario at the time of the replacement of Neanderthals by AMH. Another factor of uncertainty regarding food use in this period derives from the fact that assemblages checked from the most careful excavations are likely to have been affected by the mixing of materials during their very long curatorial histories [45]; therefore, some fossil finds may be biased and lead to inferences regarding M3H’s use of food.

3. Prevalence of Scurvy in M3H Populations

Ascorbic acid, or vitamin C (Vit C), has antioxidant functions as a free radical scavenger and allows the synthesis of collagen [46,47][46][47]. Today, there is ample consensus that scurvy can be prevented with a Vit C intake of 10 mg/day [48,49][48][49]. Scurvy shows a great variety of symptoms, such as arthralgias, bruising, or joint swelling, and common signs include pedal edema, bruising, mucosal changes, general fatigue, and myalgias [50]. Scurvy for M3H could have been more frequent than supposed. The most important diagnostic features are related to changes in soft tissues. Since these features are often difficult to diagnose in bone, obtaining archeological evidence for this condition is likely to be problematic [51]. Scurvy occurred in earlier human populations, and the subperiosteal lesions associated with scurvy assist in the differential diagnosis [52]. Scurvy’s cranial symptoms consist of porous and hypertrophic lesions of the vault, affecting frontal and parietal bosses, and related signs have been discovered in Paleolithic hominins’ bones. However, most cases of scurvy could have gone unnoticed, given that it is very difficult to attribute some doubtful pathological cases to scurvy since lesions of porotic hyperostosis are also linked to some type of anemia, infections, and/or poor nutrition [53]. In any case, pathologies related to scurvy have been unequivocally identified in some M3H skeletal remains, and some cases can be attributed to omnivorous populations, whether climatic features are considered. So, scurvy probably occurred in long winters, during which Vit C supply would have depended exclusively on animal food sources. Thereby, pathologies attributable to Vit C deficiency in several Neanderthal skeletons from Kiik-Koba (Crimea) have been described [54]. The diagnosis of an adult Neanderthal man in La Ferrassie indicated that he may have suffered scurvy in addition to lung disease [55]. Gardner and Smith [56] inventoried all the pathologies found in Neanderthal bones at the Krapina site, and some cases of porotic hyperostosis were found, which were attributed to scurvy. Other findings in human fossil assemblages from the early Upper Paleolithic (UP) in Mladec (Central Europe) were hemorrhagic processes due to scurvy [57]. In another report on three Neanderthal bones found in the French cave of Combe-Grenal, bony lesions were interpreted as the result of a reaction to chronic hemorrhages, as a possible result of scurvy [58].

4. Vit C Status of Arctic Populations: Implications for MIS 3 Hominins

Human groups that are supposed to have a diet more or less similar to that of Northern European M3H, such as Inuit people, may offer clues as to their Vit C-dependent nutritional status. This human group constitutes the current exception to the reliance on plant foods. For most of the year, Inuit people depend on mammals and fish for subsistence, and their survival is possible due to some amounts of Vit C found in mammal organs, while the gathering of plants is possible only in the short Arctic summers, although some Inuit groups never practice this [59].
Specifically, in the Arctic environment, it was found that Vit C requirements are similar to those in temperate climates, and both Inuit and Caucasoids can subsist on ascorbic acid intakes of less than 15 mg daily without showing clinical evidence of Vit C deficiency [60]. Some studies have suggested that the Inuit are able to obtain a minimum level of Vit C from a diet of frozen/raw, fermented, and dried animal food [61]. Moreover, the daily needs of Vit C also depend on genetic factors: Inuit are genetically characterized by a high Haptoglobin 1 allele frequency, which provides them with a greater antioxidant capacity, and therefore they are less likely to suffer from scurvy [62].
Adaptation to a low intake of Vit C offers a clear evolutionary advantage. The metabolism of Vit C, including absorption and its uptake by several cell types, is inhibited by increasing glucose concentration due to a glucose–ascorbate antagonism: due to their molecular similarity, glucose hinders the entry of Vit C into cells [63]. Thus, Arctic populations that are largely dependent on foods of animal origin, whose diets are low in carbohydrates, would need significantly lower amounts of Vit C than are recommended for Western societies. Then, an evolutionarily adapted human diet based on meat, fat and offal would provide enough Vit C to cover physiological needs and to ward off diseases associated with Vit C deficiency [63]. However, according to Høygaard and Rasmusson [64], who performed studies on the nutrition and physiopathology of Eskimos, analyses of Vit C in their blood reflected hypovitaminosis C and scurvy levels for 47% and 18% of their population, respectively. Other researchers indicated that it is highly probable that Inuit with a traditional nutrition live on the edge of scurvy [65]. It has been stated that a reliance on some animals, such as reindeer (Rangifer tarandus L.), which has been widely cited for both Inuit and several North European M3H populations, could have caused the onset of scurvy. In this regard, Geraci and Smith [59] described the occurrence of subacute scurvy in several Inuit children when consuming frozen reindeer for several days. Consistently, Vit C availability could have been a bottleneck for the survival of M3H, especially in the long winters, when there is a notable shortage of food plants.
Long ago, Levine [66] and Stefansson [67] reported that by following an exclusive animal food diet, it is possible to prevent the onset of scurvy. Interestingly, in all reported cases, such diet included viscera or meat from marine mammals or birds, such as penguins. In this regard, it was argued that the antiscorbutic properties of the meat in the diet of Arctic explorers and inhabitants of the polar regions lie in the fact that the meat was obtained almost entirely from seals and bears, and included not only muscle tissue but other tissues, such as liver [68]. As discussed below, marine mammals and birds are adequate Vit C sources, able to prevent the appearance of scurvy. However, marine mammals were marginally available for M3H, and there are only reports on their exploitation in Gibraltar [69].

5. The Bottleneck of Vitamin C for the Survival of M3H

The reliance of hominins on the acquisition of large mammals during most of the Pleistocene had nutritional and bioenergetic implications: large prey contain high fat amounts, provide a high energy return, and the strategies and skills required to acquire small prey are different from those required to acquire larger prey. Thus, the increased use of plant foods and technological changes that appear in the UP could be explained as adaptations to the decline in large prey in the context of late Quaternary faunal extinction, and the resulting need to acquire smaller prey efficiently and to process higher quantities of plant foods [22,41,70,71,72][22][41][70][71][72].
As for Inuit, the availability of Vit C for M3H could have had a strong seasonal component. However, unlike M3H, Inuit people have regularly available fish all year round, and in some cases, seals, and cetaceans for hunting [59], which are notable Vit C sources, so Inuit people would have rarely suffered deficiency symptoms of this essential nutrient. The problem for the survival of M3H in Northern Europe was that under a very cold climate most of the year, there is an absence of plant foods to obtain Vit C. In this scenario, viscera have been identified as sources of this vitamin, which could have supplied the daily amounts necessary to survive [73]. However, the regular consumption of viscera would have had many added problems. First, this resource is limited because the highest proportion of the edible weight of any hunted mammal corresponds to meat and fat, and thus the dependence on animals supplying minor amounts of viscera, i.e., small prey, could have caused an erratic distribution of viscera to be consumed by the hominin groups. Secondly, viscera contain large amounts of water and bacteria, and therefore are subject to rapid spoilage, so their consumption is a priority after any hunting episode.

References

  1. Arsuaga, J.L.; Martínez, I.; Arnold, L.J.; Aranburu, A.; Gracia-Téllez, A.; Sharp, W.D.; Quam, R.M.; Falguères, C.; Pantoja-Pérez, A.; Bischoff, J.; et al. Neandertal roots: Cranial and chronological evidence from Sima de los Huesos. Science 2014, 344, 1358–1363.
  2. Devièse, T.; Abrams, G.; Hajdinjak, M.; Pirson, S.; De Groote, I.; Di Modica, K.; Toussaint, M.; Fischer, V.; Comeskey, D.; Spindler, L.; et al. Reevaluating the timing of Neanderthal disappearance in Northwest Europe. Proc. Natl. Acad. Sci. USA 2021, 118, e2022466118.
  3. Guil-Guerrero, J.L.; Manzano-Agugliaro, F. Worldwide research trends on Neanderthals. J. Quat. Sci. 2022, 38, 208–220.
  4. Finlayson, C.; Carrión, J.S. Rapid ecological turnover and its impact on Neanderthal and other human populations. Trends Ecol. Evol. 2007, 22, 213–222.
  5. Staubwasser, M.; Drăgușin, V.; Onac, B.P.; Assonov, S.; Ersek, V.; Hoffmann, D.L.; Veres, D. Impact of climate change on the transition of Neanderthals to modern humans in Europe. Proc. Natl. Acad. Sci. USA 2018, 115, 9116–9121.
  6. Banks, W.E.; d’Errico, F.; Peterson, A.T.; Kageyama, M.; Sima, A.; Sánchez-Goñi, M.F. Neanderthal extinction by competitive exclusion. PLoS ONE 2008, 3, e3972.
  7. Houldcroft, C.; Underdown, S.J. Neanderthal genomics suggests a pleistocene time frame for the first epidemiologic transition. Am. J. Phys. Anthropol. 2016, 160, 379–388.
  8. Smith, F.H.; Janković, I.; Karavanić, I. The assimilation model, modern human origins in Europe, and the extinction of Neandertals. Quat. Int. 2005, 137, 7–19.
  9. Lalueza-Fox, C. Neanderthal assimilation? Nat. Ecol. Evol. 2021, 5, 711–712.
  10. Degioanni, A.; Bonenfant, C.; Cabut, S.; Condemi, S. Living on the edge: Was demographic weakness the cause of Neanderthal demise? PLoS ONE 2019, 14, e0216742.
  11. Fitzsimmons, K.E.; Hambach, U.; Veres, D.; Iovita, R. The Campanian Ignimbrite eruption: New data on volcanic ash dispersal and its potential impact on human evolution. PLoS ONE 2013, 8, e65839.
  12. Timmermann, A. Quantifying the potential causes of Neanderthal extinction: Abrupt climate change versus competition and interbreeding. Quat. Sci. Rev. 2020, 238, 106331.
  13. Fabre, V.; Condemi, S.; Degioanni, A. Genetic evidence of geographical groups among Neanderthals. PLoS ONE 2009, 4, e5151.
  14. Haws, J.A.; Benedetti, M.M.; Talamo, S.; Bicho, N.; Cascalheira, J.; Ellis, M.G.; Carvalho, M.M.; Friedl, L.; Pereira, T.; Zinsious, B.K. The early Aurignacian dispersal of modern humans into westernmost Eurasia. Proc. Natl. Acad. Sci. USA 2020, 117, 25414–25422.
  15. Stewart, J.R. Neanderthal extinction as part of the faunal change in Europe during Marine Isotope Stage 3. Acta Zool. Crac.-Ser. A Vertebr. 2007, 50, 93–124.
  16. Bunn, H.T., III. Meat-Eating and Human Evolution: Studies on the Diet and Subsistence Patterns of Plio-Pleistocene Hominids in East Africa; University of California: Berkeley, CA, USA, 1982.
  17. Kolobova, K.A.; Roberts, R.G.; Chabai, V.P.; Jacobs, Z.; Krajcarz, M.T.; Shalagina, A.V.; Krivoshapkin, A.I.; Li, B.; Uthmeier, T.; Markin, S.V.; et al. Archaeological evidence for two separate dispersals of Neanderthals into southern Siberia. Proc. Natl. Acad. Sci. USA 2020, 117, 2879–2885.
  18. Stuart, A.J. Late Quaternary megafaunal extinctions on the continents: A short review. Geol. J. 2015, 50, 338–363.
  19. Richards, M.P.; Trinkaus, E. Out of Africa: Modern human origins special feature: Isotopic evidence for the diets of European Neanderthals and early modern humans. Proc. Natl. Acad. Sci. USA 2009, 106, 16034-9.
  20. Wißing, C.; Rougier, H.; Crevecoeur, I.; Germonpré, M.; Naito, Y.I.; Semal, P.; Bocherens, H. Isotopic evidence for dietary ecology of late Neandertals in North-Western Europe. Quat. Int. 2016, 411, 327–345.
  21. Ben-Dor, M.; Barkai, R. Supersize Does Matter: The Importance of Large Prey in Paleolithic Subsistence and a Method for Measurement of Its Significance in Zooarchaeological Assemblages, in Human–Elephant Interactions: From Past to Present; Konidaris, G., Barkai, R., Tourloukis, V., Eds.; Tübingen University Press: Tübingen, Germany, 2021.
  22. Ben-Dor, M.; Barkai, R. Prey Size Decline as a Unifying Ecological Selecting Agent in Pleistocene Human Evolution. Quaternary 2021, 4, 7.
  23. Dodat, P.J.; Tacail, T.; Albalat, E.; Gómez-Olivencia, A.; Couture-Veschambre, C.; Holliday, T.; Madelaine, S.; Martin, J.E.; Rmoutilova, R.; Maureille, B.; et al. Isotopic calcium biogeochemistry of MIS 5 fossil vertebrate bones: Application to the study of the dietary reconstruction of Regourdou 1 Neandertal fossil. J. Hum. Evol. 2021, 151, 102925.
  24. Balter, V.; Person, A.; Labourdette, N.; Drucker, D.; Renard, M.; Vandermeersch, B. Les Néandertaliens étaient-ils essentiellement carnivores? Résultats préliminaires sur les teneurs en Sr et en Ba de la paléobiocénose mammalienne de Saint-Césaire. Comptes Rendus L’acad. Sci.-Ser. IIA-Earth Planet. Sci. 2001, 332, 59–65.
  25. Kuzmin, Y.V.; Bondarev, A.A.; Kosintsev, P.A.; Zazovskaya, E.P. The Paleolithic diet of Siberia and Eastern Europe: Evidence based on stable isotopes (δ13C and δ15N) in hominin and animal bone collagen. Archaeol. Anthropol. Sci. 2021, 13, 179.
  26. Drucker, D.G.; Naito, Y.I.; Péan, S.; Prat, S.; Crépin, L.; Chikaraishi, Y.; Ohkouchi, N.; Puaud, S.; Lázničková-Galetová, M.; Patou-Mathis, M.; et al. Isotopic analyses suggest mammoth and plant in the diet of the oldest anatomically modern humans from far southeast Europe. Sci. Rep. 2017, 7, 6833.
  27. Wißing, C.; Rougier, H.; Baumann, C.; Comeyne, A.; Crevecoeur, I.; Drucker, D.G.; Gaudzinski-Windheuser, S.; Germonpré, M.; Gómez-Olivencia, A.; Krause, J.; et al. Stable isotopes reveal patterns of diet and mobility in the last Neandertals and first modern humans in Europe. Sci. Rep. 2019, 9, 4433.
  28. Miras, Y.; Barbier-Pain, D.; Ejarque, A.; Allain, E.; Allué, E.; Marín, J.; Vettese, D.; Hardy, B.; Puaud, S.; Llach, J.M.; et al. Neanderthal plant use and stone tool function investigated through non-pollen palynomorphs analyses and pollen washes in the Abri du Maras, South-East France. J. Archaeol. Sci. Rep. 2020, 33, 102569.
  29. Hardy, K.; Bocherens, H.; Miller, J.B.; Copeland, L. Reconstructing Neanderthal diet: The case for carbohydrates. J. Hum. Evol. 2022, 162, 103105.
  30. Henry, A.G.; Brooks, A.S.; Piperno, D.R. Plant foods and the dietary ecology of Neanderthals and early modern humans. J. Hum. Evol. 2014, 69, 44–54.
  31. Churchill, S.E. Thin on the Ground: Neandertal Biology, Archeology, and Ecology; John Wiley & Sons: Hoboken, NJ, USA, 2014.
  32. Buck, L.T.; Stringer, C.B. Having the stomach for it: A contribution to Neanderthal diets? Quat. Sci. Rev. 2014, 96, 161–167.
  33. Fiorenza, L.; Benazzi, S.; Tausch, J.; Kullmer, O.; Bromage, T.G.; Schrenk, F. Molar macrowear reveals Neanderthal eco-geographic dietary variation. PLoS ONE 2011, 6, e14769.
  34. Droke, J.L.; Schmidt, C.W.; Williams, F.L.; Karriger, W.M.; Smith, F.H.; Becam, G.; de Lumley, M.-A. Regional variability in diet between Northern European and Mediterranean Neandertals: Evidence from dental microwear texture analysis. In Dental Wear in Evolutionary and Biocultural Contexts; Academic Press: Cambridge, MA, USA, 2020; pp. 225–241.
  35. Ben-Dor, M.; Gopher, A.; Barkai, R. Neandertals’ large lower thorax may represent adaptation to high protein diet. Am. J. Phys. Anthropol. 2016, 160, 367–378.
  36. Hardy, B.L.; Moncel, M.-H. Neanderthal use of fish, mammals, birds, starchy plants and wood 125–250,000 years ago. PLoS ONE 2011, 6, e23768.
  37. Fiore, I.; Gala, M.; Romandini, M.; Cocca, E.; Tagliacozzo, A.; Peresani, M. From feathers to food: Reconstructing the complete exploitation of avifaunal resources by Neanderthals at Fumane cave, unit A9. Quat. Int. 2016, 421, 134–153.
  38. Finlayson, S.; Finlayson, G.; Guzman, F.J.G.; Finlayson, C. Neanderthals and the cult of the Sun Bird. Quat. Sci. Rev. 2019, 217, 217–224.
  39. Morin, E.; Meier, J.; El Guennouni, K.; Moigne, A.-M.; Lebreton, L.; Rusch, L.; Valensi, P.; Conolly, J.; Cochard, D. New evidence of broader diets for archaic Homo populations in the northwestern Mediterranean. Sci. Adv. 2019, 5, eaav9106.
  40. Guillaud, E.; Béarez, P.; Daujeard, C.; Defleur, A.R.; Desclaux, E.; Roselló-Izquierdo, E.; Morales-Muñiz, A.; Moncel, M.-H. Neanderthal foraging in freshwater ecosystems: A reappraisal of the Middle Paleolithic archaeological fish record from continental Western Europe. Quat. Sci. Rev. 2021, 252, 106731.
  41. Tanner, A. An embarrassment of riches: The ontological aspect of meat and fat harvesting among subarctic hunters. In Human–Elephant Interactions: From Past to Present; Konidaris, G., Barkai, R., Tourloukis, V., Eds.; Tübingen University Press: Tübingen, Germany, 2021; Available online: https://publikationen.uni-tuebingen.de/xmlui/handle/10900/114229 (accessed on 19 November 2022).
  42. Ben-Dor, M.; Gopher, A.; Hershkovitz, I.; Barkai, R. Man the fat hunter: The demise of Homo erectus and the emergence of a new hominin lineage in the Middle Pleistocene (ca. 400 kyr) Levant. PLoS ONE 2011, 6, e28689.
  43. Navazo Ruiz, M.; Benito-Calvo, A.; Alonso-Alcalde, R.; Alonso, P.; de la Fuente, H.; Santamaría, M.; Santamaría, C.; Álvarez-Vena, A.; Arnold, L.J.; Iriarte-Chiapusso, M.J.; et al. Late Neanderthal subsistence strategies and cultural traditions in the northern Iberia Peninsula: Insights from Prado Vargas, Burgos, Spain. Quat. Sci. Rev. 2021, 254, 106795.
  44. McLeod, H. Plenty of Fish in the Sea? A Comparison of Marine Resource Use in Early Hominins. Ethnograph 2018, 4, 36–55.
  45. Bertacchi, A.; Starkovich, B.M.; Conard, N.J. The Zooarchaeology of Sirgenstein Cave: A Middle and Upper Paleolithic site in the Swabian Jura, SW Germany. J. Paleolit. Archaeol. 2021, 4, 7.
  46. Englard, S.; Seifter, S. The biochemical functions of ascorbic acid. Annu. Rev. Nutr. 1986, 6, 365–406.
  47. Padh, H. Cellular functions of ascorbic acid. Biochem. Cell Biol. 1990, 68, 1166–1173.
  48. Baker, E.M.; Hodges, R.E.; Hood, J.; Sauberlich, H.E.; March, S.C.; Canham, J.E. Metabolism of 14C and 3H-labeled L-ascorbic acid in human scurvy. Am. J. Clin. Nutr. 1971, 24, 444–454.
  49. Burri, B.J.; Jacob, R.A. Human metabolism and the requirement for vitamin C. In Vitamin C in Health and Disease; Packer, L., Fuchs, J., Eds.; Marcel Dekker Inc.: New York, NY, USA, 1997; pp. 341–366.
  50. Olmedo, J.M.; Yiannias, J.A.; Windgassen, E.B.; Gornet, M.K. Scurvy: A disease almost forgotten. Int. J. Dermatol. 2006, 45, 909–913.
  51. Huss-Ashmore, R.; Goodman, A.H.; Armelagos, G.J. Nutritional inference from paleopathology. In Advances in Archaeological Method and Theory; Academic Press: Cambridge, MA, USA, 1982; pp. 395–474. Available online: https://www.jstor.org/stable/20210060 (accessed on 12 January 2023).
  52. Ortner, D.J.; Ericksen, M.F. Bone changes in the human skull probably resulting from scurvy in infancy and childhood. Int. J. Osteoarchaeol. 1997, 7, 212–220.
  53. Eddie, D.M. Examination of Trauma in a Neandertal Ulna. Master’s Thesis, University of Kansas, Lawrence, KS, USA, 2013. Available online: https://kuscholarworks.ku.edu/handle/1808/12956 (accessed on 27 October 2022).
  54. Mednikova, M.B. Bioarcheology of Neanderthal burials from the territory of France and Crimea. Brief Commun. Inst. Archeol. 2015, 238, 243–261.
  55. Fennell, K.J.; Trinkaus, E. Bilateral femoral and tibial periostitis in the La Ferrassie 1 Neanderthal. J. Archaeol. Sci. 1997, 24, 985–995.
  56. Gardner, J.C.; Smith, F.H. The paleopathology of the Krapina Neandertals. Period. Biol. 2006, 108, 471.
  57. Teschler-Nicola, M.; Czerny, C.; Oliva, M.; Schamall, D.; Schultz, M. Pathological alterations and traumas in the human skeletal remains from Mladeč. In Early Modern Humans at the Moravian Gate; Springer: Vienna, Austria, 2006; pp. 473–489.
  58. Garralda, M.D.; Vandermeersch, B. ¿Escorbuto en los neandertales? Posibles casos en Combe-Grenal (Domme, Francia). Veleia 2008, 24–25, 385–395.
  59. Geraci, J.R.; Smith, T.G. Ascorbic acid in the diet of Inuit hunters from Holman, Northwest Territories. Arctic 1979, 32, 135–139.
  60. Rodahl, K. Nutritional requirements in cold climates. J. Nutr. 1954, 53, 575–588.
  61. Fediuk, K. Vitamin C in the Inuit Diet: Past and Present. School of Dietetics & Human Nutrition. Master’s Thesis, McGill University, Montreal, QC, Canada, 2000.
  62. Delanghe, J.R.; Langlois, M.R.; De Buyzere, M.L.; Na, N.; Ouyang, J.; Speeckaert, M.M.; Torck, M.A. Vitamin C deficiency: More than just a nutritional disorder. Genes Nutr. 2011, 6, 341–346.
  63. Clemens, Z.; Tóth, C. Vitamin C and disease: Insights from the evolutionary perspective. J. Evol. Health Jt. Publ. Ancestral Health Soc. Soc. Evol. Med. Health 2013, 1, 13.
  64. Høygaard, A.; Rasmussen, H.W. Vitamin C sources in eskimo food. Nature 1939, 3631, 943.
  65. Mullie, P.; Deliens, T.; Clarys, P. Vitamin C in East-Greenland traditional nutrition: A reanalysis of the Høygaard nutritional data (1936–1937). Int. J. Circumpolar Health 2021, 80, 1951471.
  66. Levine, V.E. The value of meat as an antiscorbutic. Am. J. Dig. Dis. 1941, 8, 454–463.
  67. Stefansson, V. The Dilemma in Vitamins. Science 1939, 89, 484.
  68. Pierson, E.M. The Antiscorbutic Properties of Some Common Food Materials. Ph.D. Thesis, The University of Minnesota, Minneapolis, MN, USA, 1922.
  69. Stringer, C.B.; Finlayson, J.C.; Barton, R.N.E.; Fernández-Jalvo, Y.; Cáceres, I.; Sabin, R.C.; Rhodes, E.J.; Currant, A.P.; Rodríguez-Vidal, J.; Giles-Pacheco, F.; et al. Neanderthal exploitation of marine mammals in Gibraltar. Proc. Natl. Acad. Sci. USA 2008, 105, 14319–14324.
  70. Dembitzer, J.; Barkai, R.; Ben-Dor, M.; Meiri, S. Levantine overkill: 1.5 million years of hunting down the body size distribution. Quat. Sci. Rev. 2022, 276, 107316.
  71. Ben-Dor, M.; Barkai, R. The importance of large prey animals during the Pleistocene and the implications of their extinction on the use of dietary ethnographic analogies. J. Anthropol. Archaeol. 2020, 59, 101192.
  72. Ben-Dor, M.; Sirtoli, R.; Barkai, R. The evolution of the human trophic level during the Pleistocene. Am. J. Phys. Anthropol. 2021, 175, 27–56.
  73. Guil-Guerrero, J.L. Evidence for chronic omega-3 fatty acids and ascorbic acid deficiency in Palaeolithic hominins in Europe at the emergence of cannibalism. Quat. Sci. Rev. 2017, 157, 176–187.
More
© Text is available under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/)
ScholarVision Creations
Feedback