Neanderthal foraging in freshwater ecosystems: A reappraisal of the Middle Paleolithic archaeological fish record from continental Western Europe
Introduction
Western Europe constitutes a key area for investigating Neanderthal subsistence practices due to the quantity and quality of sites available for study. The most recent investigations in this region have significantly expanded our knowledge on the chronology (e.g., Richard et al., 2015; Guérin et al., 2017), environmental conditions (e.g., Britton et al., 2011; Moncel et al., 2015; Discamps and Royer, 2017), and subsistence strategies of Neanderthals (e.g., Delagnes and Rendu, 2011; Cortés-Sánchez et al., 2011; 2019; Niven et al., 2012; Daujeard et al., 2012; 2019; Gaudzinski-Windheuser et al., 2018). These data have contributed to establishing a reliable framework for interpreting the profound biological and cultural changes that occurred from Marine Isotopic Stages (MIS) 11–9 to 3 (Moncel et al., 2016). Traditionally, Neanderthals have been considered as big-game hunters (i.e., top-level carnivores; Bocherens, 2009; Gaudzinski-Windheuser and Niven, 2009; Richards and Trinkaus, 2009; Jaouen et al., 2019). However, over the past decade, studies have evidenced a diversified spectrum of subsistence strategies, with a significant contribution of small game (e.g., Blasco and Fernández Peris, 2012; Cochard et al., 2012; Morin et al., 2019). Archaeozoological and archaeobotanical analyses provide evidence of the exploitation of small mammals, birds, shellfish and plants (Laroulandie, 2000; Cortés-Sánchez et al., 2011, 2019; Hardy et al., 2012, 2013; Laroulandie et al., 2016; Estalrrich et al., 2017), yet the role played by aquatic-vertebrate resources in Neanderthal diets has barely been documented, and Neanderthal fishing remains a controversial issue (Le Gall, 1992, 2000; Roselló-Izquierdo and Morales-Muñiz, 2005). Evidence exists that hominins practiced river or lake fishing during the Lower Paleolithic (Braun et al., 2010; Stewart, 1994) and the Middle Paleolithic in Africa, where specialized technologies such as barbed bone points have been developed by ca. 90 000 BP (Brooks et al., 1995; Yellen et al., 1995). However, in Western Europe, there is currently no evidence that the exploitation of aquatic vertebrates was significant before the Upper Paleolithic period, especially the Magdalenian period (Cleyet-Merle, 1990). For most of the Middle Paleolithic, the sea level was lower than it is today, except during MIS 11 and 5e when sea levels were about 6–13 m above present levels (Dutton et al., 2015). For this reason, the vast majority of coastal archaeological sites, where hominins may have left traces of fishing activities, are currently submerged, often at great depths (Cleyet-Merle, 1990). Although a Neanderthal coastal adaptation, including fishing activities, that would have increased their dietary breadth is possible (see Brown et al., 2011; Zilhão et al., 2020), no such evidence has been found for the exploitation of continental freshwater ecosystems. Hence, the study of inland fishing activities, close to rivers or lakes, remains one of the only possibilities for studying Neanderthal fishing.
Middle Paleolithic fish bones are occasionally documented in inland caves close to rivers, often mixed with stone tools and faunal remains. These remains can only be considered as evidence of fishing by humans when other fish predators, in particular cave-dwelling carnivores and raptors, are ruled out as alternative accumulators. At the time of writing, few studies have been published on how to reliably diagnose fish deposits produced by most of these predators and set them apart from those produced by humans. In Europe, most of these papers focus on the Eurasian eagle-owl (Bubo bubo) and the Eurasian otter (Lutra lutra; Nicholson, 1991, 2000; Le Gall, 1999; Russ and Jones, 2011, Guillaud et al., 2017a, 2018).
This paper explores the role that Western European Neanderthals played in accumulating fish remains. The question “were Neanderthals freshwater fishers?” will also aim to determine whether fishing was an opportunistic or a systematic activity for this hominin. The issue has far-reaching consequences since shifts in prey selection by Neanderthals and anatomically modern humans (AMH) are hotly debated issues. Small terrestrial faunas contributed to the Neanderthal diet as a fallback resource and as staples, yet small game became more frequent in the European Upper Paleolithic (UP), and this suggests that a non-overlap of niches between the two hominins might have existed (Stiner, 1994; Patou-Mathis, 2000; Costamagno et al., 2005; Blasco and Fernández-Peris, 2012; Rufá et al., 2016; Balter and Simon, 2009; Hardy et al., 2013; Wiβing et al., 2019). Fish and shellfish also appear in European Middle Paleolithic (MP) sites, but data on the use of aquatic vertebrates by Neanderthals are still scarce and aquatic faunas are rarely taken into account in studies of Neanderthal consumption patterns (Stringer et al., 2008; Cortés-Sánchez et al., 2011). This scarcity may simply reflect a time-mediated taphonomic bias; fish bones are unlikely to be preserved in archaeological archives because their chemical composition makes them much more susceptible to degradation (Szpak, 2011). This would explain why the earliest exploitation of marine mollusks by Neanderthals, dated to 166 ka cal BP (Bajondillo Cave, Málaga, Spain), is in keeping with that documented for AMH at Pinnacle Point in South Africa (Marean et al., 2007; Cortés-Sánchez et al., 2011, 2019), or on the Atlantic coast of North Africa (Campmas et al., 2016; Chakroun et al., 2017). Later MP deposits from Vanguard (ca. 41.8 ka cal BP) and Gorham’s Cave (ca. 30–32 ka cal BP) in Gibraltar document dolphins, seals and fish, in addition to marine mollusks (Stringer et al., 2008). Additional lines of evidence for the exploitation of aquatic resources by Neanderthals include residue analyses on stone tools, tooth use wear, and anthropological studies (Puech and Puech, 1993; Hardy et al., 2013; Trinkaus et al., 2019). Another potential line of inquiry is isotopic analyses. No isotopic studies have yet focused on the consumption of aquatic resources by Neanderthals, perhaps because if these did not make up a significant fraction of their diet, they may not be discernible using current analytical procedures (Patou-Mathis, 2000; Drucker and Bocherens, 2004; Drucker et al., 2005; Stringer et al., 2008). For this reason, the development of sulfur or zinc isotope analyses seems promising for directly assessing fish consumption on Neanderthal bones (Privat et al., 2007; Nehlich et al., 2010; Jaouen et al., 2018).
Evidence of the use of aquatic resources helps to explain why Neanderthals settled in marine and freshwater areas and lends weight to the proposal that fishing was a well-established Neanderthal practice or an occasional, opportunistic activity. To explore this issue, our paper analyzes and reviews a series of MP fish collections from Belgium, France and Spain that span from MIS 11 to MIS 3 by applying a battery of protocols in order to define a methodology for assessing the contribution of fish to the human diet during prehistoric times.
Section snippets
Materials
This study examines ichthyoarchaeological collections from 11 faunal assemblages (Table 1; Fig. 1), totalizing 3159 fish remains (Table 2), and comprises new ichthyoarchaeological analyses from Scladina Cave (Belgium), Abri des Pêcheurs, Baume-Vallée Cave, and Baume Moula-Guercy (France). These analyses are combined with a reassessment of previously published fish assemblages from Caverne Marie-Jeanne and Walou Cave (Belgium), Vaufrey Cave, Abri du Maras and Barasses II Cave (France), Cueva
Scladina Cave (Belgium)
Seventy-four fish remains were studied. These represent less than 2% of the faunal NISP (SOM Table 1, Table 2). European sturgeon (Acipenser sturio) was the dominant species but unfortunately, its remains were discovered in a disturbed zone (Fig. 2). Thus, although the origin of the sturgeon remains in Scladina is likely to be anthropogenic, since individual size estimates range from about 95 to 165 cm and exclude transport by a non-human predator, we cannot be sure of their attribution to the
Discussion
Although it is questionable to compare faunal assemblages retrieved by different research strategies, excavation methods and retrieval techniques, a comparative overview of taphonomic issues can help to reveal non-evident aspects of the behavioral repertoire of a given bone accumulator agent. Our first observation is the generally well-preserved condition of these collections (Fig. 4), which allowed 75.3% of the items (2380 remains) to be identified to at least the family rank. A second feature
Conclusions
For Neanderthals, even the use of aquatic resources was questioned up until a decade ago. The paradigm was that these humans were unable to gather stationary shellfish. In hindsight, the basis for the question as to whether Neanderthal practiced fishing relied on unstated assumptions and speculative grounds referring to debatable ideas about ‘cognitive barriers’ and the like. Indeed, ample evidence testifies to fishing practices by a wide range of terrestrial mammals, from bears to monkeys,
Declaration of competing interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Acknowledgements
This work was supported by a grant from the Agence Nationale de la Recherche under LabEx ANR-10-LABX-0003-BCDiv (direction P.B. and M.H.M.), as part of the program “Investissements d’avenir” n° ANR-11-IDEX-0004-02. E.R.I. and A.M.M. were supported by grants HAR 2014-55722-P and HAR 2017-88325-P from the Spanish Ministerio de Economía y Competitividad, and by grant 19438/PI/14 from the Programa Séneca 2014. The authors would like to thank the Muséum national d’histoire naturelle (Paris, France),
References (166)
- et al.
Climate and environments during marine isotope stage 11 in the central iberian Peninsula: the herpetofaunal assemblage from the acheulean site of áridos-1, Madrid
Quat. Sci. Rev.
(2014) - et al.
A uniquely broad spectrum diet during the middle Pleistocene at bolomor cave (valencia, Spain)
Quat. Int.
(2012) - et al.
Were bears or lions involved in salmon accumulation in the Middle Palaeolithic of the Caucasus? An isotopic investigation in Kudaro 3 cave
Quat. Int.
(2014) - et al.
Paleobiological implications of the isotopic signatures (13C, 15N) of fossil mammal collagen in Scladina Cave (Sclayn, Belgium)
Quat. Res.
(1997) - et al.
Strontium isotope evidence for migration in late Pleistocene Rangifer: implications for Neanderthal hunting strategies at the Middle Palaeolithic site of Jonzac, France
J. Hum. Evol.
(2011) Natural versus cultural salmonid remains: origin of the dallas roadcut bones, columbia river
J. Archaeol. Sci.
(1993)- et al.
Initial insights into Aterian hunter–gatherer settlements on coastal landscapes: the example of Unit 8 of El Mnasra Cave (Témara, Morocco)
Quat. Int.
(2016) - et al.
Consommation osseuse de carnivores : résultats de l’étude de l’exploitation de carcasses de boeuf (Bos taurus) par des loups captifs
Ann. Paleontol.
(2008) - et al.
Evidence of small fast game exploitation in the middle paleolithic of les canelettes, aveyron, France
Quat. Int.
(2012) - et al.
Plant-animal subsistence ratios and macronutriment energy estimations in world-wide hunter-gatherer diets
Am. J. Clin. Nutr.
(2000)
Shellfish collection on the westernmost Mediterranean, Bajondillo cave (∼160-35 cal kyr BP): a case of behavioral convergence?
Quat. Sci. Rev.
Neanderthal subsistence strategies in southeastern France between the plains of the rhone valley and the mid-mountains of the Massif central (MIS 7 to MIS 3)
Quat. Int.
On Neanderthal subsistence strategies and land use: a regional focus on the Rhone Valley area in southeastern France
J. Anthropol. Archaeol.
Shifts in Neandertal mobility, technology and subsistence strategies in western France
J. Archaeol. Sci.
Reconstructing palaeoenvironmental conditions faced by Mousterian hunters during MIS 5 to 3 in southwestern France: a multi-scale approach using data from large and small mammal communities
Quat. Int.
Archaeological implications of a bald eagle nesting site at ferrelo point, san miguel island, California
J. Archaeol. Sci.
Dietary reconstruction of the El Sidrón Neandertal familial group (Spain) in the context of other Neandertal and modern hunter-gatherer groups. A molar microwear texture analysis
J. Hum. Evol.
The complementarity of luminescence dating methods illustrated on the Mousterian sequence of the Roc de Marsal: a series of reindeer-dominated, Quina Mousterian layers dated to MIS 3
Quat. Int.
Impossible Neanderthals? Making string, throwing projectiles and catching small game during marine isotope stage 4 (Abri du Maras, France)
Quat. Sci. Rev.
A revised chronology for the Grotte Vaufrey (Dordogne, France) based on TT-OSL dating of sedimentary quartz
J. Hum. Evol.
Past distributions of the European freshwater eel from archaeological and palaeontological evidence
Quat. Sci. Rev.
L’impact de l’environnement sur l’évolution biologique et culturelle dans les périodes de transition en Préhistoire : paléolithique ancien/moyen et Paléolithique moyen/supérieur
Comptes Rendus Palevol
Who brought the bird remains to the Middle Palaeolithic site of Les Fieux (Southwestern, France)? Direct evidence of a complex taphonomic story
Quat. Int.
MamÍferos del yacimiento del Pleistoceno superior de cueva Millán (Burgos, España)
Estud. Geol.
Owls, Caves and Fossils
What taphonomy can and cannot tell us
Cuad. Geol. Iber.
Small mammal bone accumulations produced by mammalian carnivores
Paleobiology
Fiche hameçons
Les dépôts quaternaires ; inventaire paléontologique et archéologique
Diet and behavior of the Saint-Césaire Neanderthal inferred from biogeochemical data inversion
J. Hum. Evol.
Ichtyofaune
A late neandertal femur from les rochers-de-villeneuve, France
Proc. Natl. Acad. Sci. U. S. A
Neanderthal dietary habits: review of the isotopic evidence
Le régime alimentaire de la Chouette hulotte Strix aluco dans le Sud des Alpes françaises
BIEVRE
Early hominin diet included diverse terrestrial and aquatic animals 1.95 Ma in East Turkana, Kenya
Proc. Natl. Acad. Sci. Unit. States Am.
Dating and context of three middle stone age sites with bone points in the upper semliki valley, zaire
Science
The taphonomy of owl-deposited fish remains and the origin of the Homestead cave ichthyofauna
Journal of Taphonomy
Small-game and marine resource exploitation by Neanderthals: the evidence from gibraltal
Biologie des poissons d’eau douce européens
Some archaeological uses of fish remains
Am. Antiq.
Fish Remains in Archaeology and Paleo-Environmental Studies
The Pleistocene of Rabat (Morocco): mollusks, coastal environments and human behavior
Afr. Archaeol. Rev.
Les Proies des Rapaces (Petits Mammifères et leur Environnement)
A propos de la pêche au Paléolithique supérieur en France : apport des représentations réalistes de Poissons dans l’art mobilier, premiers résultats
Antiquités Nationales
La Préhistoire de la Pêche
Earliest known use of marine resources by Neanderthals
PloS One
Homme ou carnivores ? Protocole d’étude d’ensembles osseux mixtes : l’exemple du gisement moustérien des Pradelles (Marillac-le-Franc, Charente)
Archeofauna
Les poissons d’eau douce à la fin du Paléolithique supérieur en France. Réexamen et étude complémentaire du site de Pont d’Ambon (Bourdeilles, Dordogne)
Les analyses anthracologiques dans la séquence de la grotte Walou
Neanderthal selective hunting of reindeer? The case study of Abri du Maras (south-eastern France)
Archaeological and Anthropological Sciences
Cited by (19)
Coastal and Inland subsistence strategies during the Gravettian in the Cantabrian Region (northern Iberian Peninsula)
2023, Quaternary Science AdvancesLate Neanderthal “menu” from northern to southern Italy: freshwater and terrestrial animal resources
2023, Quaternary Science ReviewsA warm and humid paleoecological context for the Neanderthal mountain settlement at the Navalmaíllo rockshelter (Iberian Central System, Madrid)
2022, Quaternary Science ReviewsCitation Excerpt :According to the different degrees of digestion (mostly light, except on two trout vertebrae from layer F showing a moderate digestion), the predator responsible for the fish accumulation is interpreted as a category 3 predator such as the Eurasian eagle owl (Bubo), ruling out any possible human activity as accumulation agent. Several authors (e.g. Sanchís-Serra, 2000; De cupere et al., 2009; Russ, 2010; Guillaud et al., 2021; Blanco-Lapaz et al., 2021) also argued the Eurasian eagle owl as the agent responsible of fish assemblage accumulation in archaeological contexts. This species is sedentary and currently present in the area, having opportunistic hunting habits nearby rivers (some 2.3 km around its nest according to Penteriani and Delgado, 2008; 2015).
Selection versus opportunism: A view from Neanderthal subsistence strategies
2022, Updating Neanderthals: Understanding Behavioural Complexity in the Late Middle PalaeolithicSmall animal use by Neanderthals
2022, Updating Neanderthals: Understanding Behavioural Complexity in the Late Middle PalaeolithicReconstructing Neanderthal diet: The case for carbohydrates
2022, Journal of Human EvolutionCitation Excerpt :More recently, evidence has emerged suggesting that the Neanderthal diet was broader than this, including growing evidence for exploitation of a wide range of small animal species such as rabbits and tortoises (Speth and Tchernov, 2002; Stiner et al., 2009; Ben-Dor al., 2011; Blasco, and Peris, 2012; Finlayson et al., 2012; Morin et al., 2019; Nabais and Zilhão, 2019). In addition, there is clear evidence that Neanderthals also exploited marine (Zilhão et al., 2010, 2020; Cortés-Sánchez et al., 2019) and freshwater (Van Neer and Wouters, 2009; Guillaud et al., 2020) resources. Plant use by Neanderthals will likely remain elusive with limited evidence that can be linked to deliberate collection for food and other purposes (technology, medicine; Table 6).