Iberian Neanderthals in forests and savannahs

This article aims to delve into the reality of glacial refuges of forests and tree species (including conifers, mesothermophilous angiosperms and xerothermic scrub) during the cold dry phases of the Iberian Pleistocene in which there is evidence of occupation of Middle Palaeolithic people. The research framework focuses on the eastern sector of the Iberian Peninsula due to the physiographic, palaeobotanical and archaeological peculiarities, substantiated by recent studies. We contend that some Neanderthal occupations developed in the context of high geobiological complexity, high biological diversity and highly structured forest ecosystems. We highlight the importance of glacial refuges as local anomalies that, however, would be contingent on vegetational development, and on the survival of Palaeolithic groups in areas with a broad diversity of natural resources.

Recent investigations have further diversified the landscape of occupation, by showing that Neanderthal populations survived for hundreds of millennia under relatively closedforest habitat conditions which were not substantially stressed by climate during cold stadials. Three of these critical sites are the Iberian caves of Bolomor (Ochando et al., 2019), Teixoneres (Ochando et al., 2020a) and Toll (Ochando et al., 2020b). Some independent studies support these data based on genetic and anatomical information deducing that Neanderthals were accomplished sprinters, ambushing and hunting prey over short distances (Stewart, 2005;Finlayson and Carrión, 2006;Rosas, 2016;Stewart et al., 2019).
In this paper, we review palaeopalynological data for the Iberian Peninsula supporting the perspective of forested habitats for Neanderthal humans during glacial stadials. For practical purposes, we have adopted a wide temporal range reviewing the time span between Marine Isotope Stage (MIS) 12 to the Last Glacial Maximum MIS 2. We need to be aware that the taxonomic boundaries of Homo neanderthalensis are diffuse. The oldest confirmed Neanderthals are found in the Iberian Peninsula, dated to at least 430 000 years ago (Atapuerca Sima de los Huesos; Bischoff et al., 2007;Meyer et al., 2016). While their taxonomic connection with H. heidelbergensis is still open to debate (Roksandic et al., 2018;Bermúdez de Castro et al., 2019;Carrión and Walker, 2019;Rosas et al., 2019), it does not affect the results of the present work, as Heidelbergs represent Neanderthals or at least an early part of the Neanderthal lineage.
With respect to their demise, it must be kept in mind that Neanderthals merged genetically with other archaic hominins that inhabited western Eurasia during the end of the last glacial stage (Krause et al., 2010;Wall et al., 2013;Bermúdez de Castro et al., 2016;Kuhlwilm et al., 2016;Lalueza-Fox, 2017;Slon et al., 2018;Finlayson, 2019). The exact age of the last Neanderthal population is therefore far from clear, although it probably reached the end of MIS 3 in southern Iberia (Zilhão et al., 2017;Carrión et al., 2019c;Finlayson, 2019), while in the north of Iberia they disappeared as early as ca. 48-45 cal BP (Marín- Arroyo et al., 2018). It must also be recognized that the connections between human species taxonomy and lithic technology are not straightforward (Finlayson, 2019;Greenbaum et al., 2019;Haws et al., 2020). While the Mousterian is most likely an exclusively Neanderthal industry in Western Europe (but not in Western Asia) and the post-Aurignacian Upper Palaeolithic seems clearly attributable to Homo sapiens (Finlayson, 2019), it is still not clear who manufactured industries such as the Szeletian, Uluzzian, Chatelperronian,  García-Antón (1989, 1992; García-Antón and Sainz-Ollero (1991) Carrión (1991Carrión ( , 1992aCarrión ( , 1994; Carrión and Munuera (1997)  López- García (1982García ( , 1986 (Continued ) sediments and fossil dung samples (Carrión et al., , 2009Prieto and Carrión, 1999;Navarro et al., 2000Navarro et al., , 2001Navarro et al., , 2002Carrión, 2002a). Several strictly insect-pollinated taxa such as Maytenus, Periploca, Withania, Calicotome and Lycium are noticeably under-represented (Carrión, 2002a;Carrión et al., 2003a). This means that, in dealing with cave sites, relatively high pollen percentages of arboreal taxa excluding pines, and zoophilous scrub species of the xerothermic belt may indicate high local cover of the species involved. This must be kept in mind here. In either case, pollen spectra are not particularly well suited to the spatial inference in the palaeoecosystem (Carrión, 2002a), so it seems practical to give the palaeofloristic contingent more weight than palaeoecological models based on pollen rain models from open depositional environments. Archaeological palynology is thus the fundamental evidence supporting the corollary of this work.

Mixed forests in valleys of Eastern (Mediterranean) Iberia
Ochando et al. (2019) (Fig. 4). With a few exceptions probably associated with cold spells, the xeroheliophytic cover with Artemisia, Amaranthaceae, Erica and Poaceae is relatively minor. Occurrences of some palynological types such as Ceratonia, Castanea, Rhododendron and Celtis are of note because they correspond to species that do not grow in the region at present. Bolomor was characterized by a more forested habitat than has been reported from other sites during Pleistocene stadials (Carrión et al., 2003a(Carrión et al., , 2013González-Sampériz et al., 2010). The human groups who inhabited Bolomor processed and consumed a diversity of animal species (ungulates, lagomorphs, tortoises, birds). Through the taphonomic study of faunal specimens, it was possible to demonstrate a broadspectrum diet in the site (Sanchis- Serra and Fernández-Peris, 2008;Blasco and Fernández Peris, 2012a,b;Blasco et al., 2013). To this, we can add a broad spectrum of edible plants such as hazelnut (Corylus avellana), chestnut (Castanea sativa), Mediterranean hackberry (Celtis australis), strawberry tree (Arbutus unedo), carob tree (Ceratonia siliqua), holly oak (Quercus ilex), olive (Olea europaea), elderberry (Sambucus nigra) and probably wild Rosaceae such as several species of Prunus, Rubus, Rosa and Sorbus (Ochando et al., 2019).
The Neanderthals of Bolomor must have possessed highly adaptive subsistence strategies in forested environments (Blasco et al., 2011(Blasco et al., , 2013. The low elevation of the site within an intramountainous valley, its proximity to marine resources and the large Pleistocene coastal platforms, as well as the availability of fresh water, make Bolomor a glacial refugium resembling the large phytodiversity reservoirs of the Balkans (Bennett et al., 1991;Willis, 1994 Magri et al., 2017). It should be noted that Neanderthals occupied this relatively stable biotope for more than 300 000 years, with that well-known forest resilience capable of cushioning the numerous climatic oscillations of such a long period (Carrión, 2001). The existence of glacial forest refugia in the central eastern region of Iberia had already been inferred from lacustrine and peatbog pollen sequences, such as Navarrés in Valencia (Carrión and Dupré, 1996;Carrión and van Geel, 1999). The rapidity of the late MIS 3 colonization of steppe pinelands by Mediterranean mixed forests in this valley pointed to the proximity of Mediterranean forests in the nearby mountain ranges (Figs. 5 and 6). The pollen record of the Palaeolithic Cova Beneito, including during its Mousterian occupation, supports this view by showing late MIS 3 expansions of Juniperus, Oleaceae and Quercus at the expense of open pinelands and grasslands (Carrión, 1992a;Carrión and Munuera, 1997).
Pines, including Mediterranean and high-elevation species, were certainly an abundant component of these levantine woodlands. In line with former anthracological works (Badal, 2001;Esteban et al., 2017), Real et al. (2021, this (Zilhão et al., 2020) and Gibraltar (Ward et al., 2012a,b) is remarkable. In addition, these studies and other fieldwork in the region have provided further evidence of plant foods which would be accessible to Neanderthal and modern humans, as evidenced by carpological remains of Celtis australis and Corema album (Ward et al., 2012a,b;Martínez-Varea et al., 2019;Martínez-Varea, 2020;Zilhão et al., 2020).
Spanning from before MIS 4 up to MIS 1, Toll Cave is an important palaeontological and archaeological site near Teixoneres. Palynological investigations in Toll parallel those at Teixoneres and reinforce the idea that both Neanderthal settlements belonged to an important Quaternary forest refugium (Ochando et al., 2020b). Again, the pollen record is characterized by the prevalence of pines and oaks with an important contribution of Corylus, Juniperus and Castanea, which were continuously accompanied by other trees such as Abies, Taxus, Acer, Betula, Carpinus betulus, Tilia, Celtis, Fraxinus, Juglans, Buxus, Ilex, Populus, Salix and Ulmus, as well as Mediterranean elements such as Pistacia, Myrtus, Calicotome, Cistus, Ephedra fragilis, Ligustrum, Rhamnus and Viburnum (Fig. 8). The heliophytic component (Artemisia, Poaceae, Amaranthaceae, Erica, Ephedra) would still have been relatively unimportant with the exception of in some phases (1.1, 2a.1, 2 c.2, crust 2 c.2-3a) (Fig. 8).
The pollen records of Teixoneres and Toll are particularly interesting in pointing to a high incidence of oak forests in a pleniglacial context and relatively high latitude within the Iberian Peninsula. These sequences must be therefore incorporated into the debates on glacial refugia for temperate trees in the Mediterranean Peninsulas (Bennett et al., 1991;Willis, 1994;Carrión et al., , 2003aTzedakis et al., 2003;Giardini, 2007;Bhagwat and Willis, 2008;Margari et al., 2009;González-Sampériz et al., 2010;Sadori et al., 2016;Magri et al., 2017;Manzano et al., 2017;Sinopoli et al., 2018). The evidence of evergreen Quercus (mainly Quercus ilex) during the Quaternary glacial stages had so far suggested limited cover in northern Iberia (Uzquiano et al., 2016), as a result of stable isotope analyses of herbivore remains during MIS 3 (Jones et al., 2018(Jones et al., , 2019 Based on counts of of woody taxa of palaeobotanical sequences from the Iberian Pleistocene, Teixoneres and Toll rank at the top of a comparative abundance chart (Fig. 9), surpassing in number of trees and shrubs many sites in southern Iberia (Carrión et al., 2013). Apart from possible pollen-preservational biases, this high diversity might be because these caves are located in an ecotone between the Eurosiberian and Mediterranean regions.
The There is a lack of substantial vegetation and floristic changes between Pleistocene stadials and interstadials in a refugium context such as derived from palaeoecological data of Gorham's Cave . In comparison, in the most continental site of Navarrés, climatic changes do affect the structure and composition of vegetation (Carrión and van Geel, 1999). Inspired by Finlayson and Carrión (2007) whole Upper Pleistocene and most of the Holocene, and it is in one of the most continental locations where palynological studies have been carried out within the Iberian Peninsula (Fig. 11). This location, intensively influenced by climatic extremes, undoubtedly affects the composition of the pollen assemblages, which even during interglacials and interstadials show a complex patched vegetation landscape with high incidence of junipers and/or pines, relatively low mesophytic arboreal cover and high proportions of fluctuating xerophytic herbs (mainly Artemisia, Chenopodiaceae/ Amaranthaceae, Asteraceae). Thus, vast steppes and a parkland mosaic do not only exist during cold stages (MIS 6, MIS 4, MIS 2). By contrast, pine, oak and especially juniper savannahs spread during the climate amelioration phases such as MIS 5e, MIS 5c, MIS 5a, some intervals of MIS 3 and the Holocene (González-Sampériz et al., 2010, 2020Aranbarri et al., 2014). The inertial nature of conifer formations, surprisingly led by junipers during MIS 5 (as occurred in mid-Pleistocene inner Iberian palynological sequences) and later by pines, resisting competitive displacement by oaks (both evergreen and semi-deciduous), mesophytes or Mediterranean taxa, demonstrates the intense resilience of vegetation formations in Iberia, which is also seen in inner regions such as the Villarquemado area.
The Atapuerca hominin-bearing sites (42°21′N, 03°31′W; 980 m asl) are located at low elevation in an area with maximum altitude of 1078 m in the Sierra de Atapuerca and are made up of karstified Cretaceous limestones that include galleries and chasms filled with Quaternary sedimentary deposits. The construction of a railway route at the end of the 19th century uncovered some of these sedimentary fillings, such as those that comprise the so-called Trinchera del Ferrocarril and which include Gran Dolina, Galería and Sima del Elefante. They have all provided numerous archaeological and palaeontological remains including hominin fossils belonging to Homo antecessor, H. heidelbergensis and H. neanderthalensis covering from the Lower Pleistocene to the late Middle Pleistocene (e.g. Bermúdez de Castro et al., 1997Arsuaga et al., 1999;Falguères et al., 2013;Meyer et al., 2016;Bógalo et al., 2021).
By using habitat weighting methods on the record of vertebrates, charcoal and pollen, Rodríguez et al. (2011) inferred the past environmental conditions of Atapuerca between ca. 500 and 200 ka (Figs. 12 and 13). Of note is the coexistence of steppic species of vertebrates such as Stenocranius gregaloides and Allocricetus bursae with temperate and thermophilous taxa such as Hystrix refossa and Crocidura. Overall, the herpetofauna suggests a significant local woodland  (García-Antón and Sainz-Ollero, 1991;Burjachs, 2001) (Fig. 12), but the available data support Rodríguez et al.'s (2011) (García-Antón and Sainz-Ollero, 1991) (Fig. 13). For Sima de los Huesos, also in Atapuerca, García and Arsuaga (2011) reviewed the records of carnivores, ungulates and isotopes to construct a palaeoecological model, resolving that the dominant ecosystem was a savannah-like open woodland, in agreement with palynological data obtained from three clay-matrix samples (García-Antón, 1987), showing the abundance of pines together with oaks, Betula and Fagus. The carnivore assemblage (Homotherium, Ursus, Panthera, Felis, Lynx, Vulpes, Canis, Cuon, Meles, Mustela, Martes) was interpreted to represent a consequence of highly productive treelands.
Another important reference pollen sequence is Padul. This comes from a tectonic depression (37°00′21″N, 03°36′43″W) located about 22 km south of Granada, comprising a peaty area of about 2.5 × 3.5 km, at 700 m asl, east of Sierra Nevada. After the pioneering works of Menéndez-Amor and Florschütz (1962Florschütz ( , 1964, the first systematic study was carried out by Florschütz et al. (1971), although there is no secure chronological control here. A subsequent study by Pons and Reille (1988) frames the sequence between isotopic stages 5 and 1. Another study on another core taken in the same area in the 1990s suggests that the deposition of peat begins about 400 000 years ago (Ortiz et al., 2004). The changes in vegetation and climate of the last two glacial-interglacial In general, vegetation changes in Padul are closely related to variations in the elevation of forest species in the bioclimatic vegetation belts in the Sierra Nevada linked to climatic oscillations (Camuera et al., 2019). Additionally, there are orbital-scale vegetation oscillations that point to insolation as the main factor controlling vegetation changes in this record. Under harsher climatic conditions, the Late Pleistocene Carihuela pollen record (Carrión, 1992b;Carrión et al., 1998Carrión et al., 2019c) parallels Padul showing similar dynamics of conifer savannahs and xerophytic grasslands during stadials. However, the longdistance pollen signal for Mediterranean sclerophylls is lower in Carihuela.

Mesothermic savannahs in coastal shelves
The Sima de las Palomas (Torre Pacheco, Murcia, 125 m. a.s.l., 5 km from the Mediterranean coast) includes a Neanderthal and Mousterian occupation dated from ca. 130 to 40 ka (Walker et al., 2004(Walker et al., , 2008. Pollen analyses in an interval implying a time ca. 44-40 ka include a mix of plant taxa with very different ecological affinities (Carrión et al., 2003a. In the context of the current climate of the southern coast of Murcia, with enclaves that do not exceed 200 mm of average annual rainfall, and high evapotranspiration values, the abundance of oaks is striking and, in particular, the presence of species that demand temperate-humid conditions such as hazel (Corylus avellana), ash (Fraxinus), strawberry tree (Arbutus unedo), box (Buxus) or birch (Betula cf. celtiberica) (Fig. 16). It is not easy to determine the exact area of origin of these tree populations, but there is no doubt that the oaks grew in the vicinity, since their pollen percentages range between 15 and 20% and, in a cave context, these cannot be due to long-distance dispersal (Prieto and Carrión, 1999;Navarro et al., 2001Navarro et al., , 2002. A local landscape can be conceived to have been made up of a much more diverse mosaic of plant formations than is currently observed. This would include a prevalence of xerophytic Mediterranean savannahs with pines (Pinus nigra, P. halepensis, P. pinea), oaks (Quercus rotundifolia, Q. coccifera, Q. faginea) and junipers, forest patches of pine and/or oaks with other deciduous trees, and an understorey of Juniperus oxycedrus, Olea europaea, Phillyrea, Chamaerops humilis, Buxus, Rhamnus, Erica arborea, Maytenus europaeus, Smilax aspera and Pistacia, as well as heliophilous formations with Periploca angustifolia, Osyris quadripartita, Asphodelus, Lamiaceae, Asteraceae, Cistaceae, Thymelaea hirsuta, Calicotome intermedia, and other Genisteae and, finally, marshes with chenopods, Lycium and Whitania frutescens. It is probable that many trees behaved like phreatophytes, growing on riverbanks and streams. Because the sequence is within a glacial period, the diversity and abundance of thermophytes can be considered relevant. It should be noted that some species such as Periploca angustifolia and Maytenus senegalensis can hardly bear frost, so it is evident that the local climate was not much colder than it is today.
The situation described for Sima de las Palomas may be extended to the coastal areas from Murcia to Gibraltar and beyond into the Atlantic coasts of Huelva. Similar vegetation records have been described in Perneras Cave, Mazarrón at Murcia province (Carrión et al., 1995), Gorham's  and Vanguard Caves in Gibraltar (Carrión et al., 2018), Mousterian Bajondillo (López-Sáez et al., 2007) and Abrigo del Humo (Ochando et al., 2020c) in Málaga. These records agree in suggesting the existence of a littoral location favourable for the survival of the greatest diversity of environments in the Iberian Peninsula during the last glacial in which the late survival and extinction of the Neanderthals took place Carrión et al., 2018).
Gorham's Cave demands particular attention. The cave is one several located in the basal and south-easternmost level of the Gibraltar Peninsula, on the edge of the current sea level at 36°07′13″N and 05°20′31″W. The excavations, carried out intensively since 1997, have produced a four-level stratigraphy (Finlayson et al., 1999(Finlayson et al., , 2000, with level IV corresponding to a Mousterian occupation, dated between 32 560 and 23 780 a BP. However, there are three older basal dates of 44 090 a BP. Palaeobotanical studies at Gorham's Cave include anthracological and palynological analyses of sediment and coprolites Ward et al., 2012b) Finlayson and Carrión, 2007;Bailey et al., 2008).

Final remarks
The coastal shelves and mountains of southern Iberia where Neanderthals lived were certainly singular in floristic and ecostructural terms. Pine, oak and mixed savannahs may have been the dominant formation. Most interestingly, however, the coexistence of temperate, deciduous trees, cold-adapted pines currently growing in high altitudes, Mediterranean conifers, Mediterranean oaks and scrub, halophytic grasslands, and xerothermic North African matorral with palaeotropical elements represents a unique refugium ecosystem in the sense of a Noah's Ark for plant species. This coexistence is not exclusive to the Pleistocene. However, it reaches the middle Holocene in some mountains such as Sierra de Gádor, Almería, a local reservoir of edaphic water and forest patches in the heart of a semi-desertic region (Carrión et al., 2003b). Hominin refugia may have been preferentially distributed across regions with high levels of geological variability favouring the maintenance of mosaic habitats through time. This would include many coastlines Finlayson et al., 2008) which would have acted as corridors opening past expansion routes for humans (Bailey et al., 2008). The progressive Neanderthal extinction ending in southern Iberia can be depicted within a continental to oceanic gradient, ending in the southernmost extreme (Finlayson, 2008).
Here we also show evidence of woodlands rich in species and depicting a palaeoecosystem with a tremendous structural complexity in which we find Neanderthals and/or their lithics during cold dry stages of the Iberian Pleistocene. It is likely that these forests were maintained by strong edaphic conditions added to the regional climatic humidity. This possibility has analogues in other geographically complex regions. Recently, Barboni et al. (2019), working on the Aramis Member (Awash Valley, Ethiopia), have emphasized the importance of springs for the palaeoecology of hominin-bearing sites. Springs would have favoured structurally complex vegetation representing, at the landscape scale, hydro-refugia favouring increased gathering of animals, allowing migrations during dry periods. Albert et al. (2018) concluded similarly: though their research was on phytoliths and plant macrofossils, plants from fluvial channels, levées and backswamp environments were of particular importance for human evolution in Africa. In the southern European context, glacial refugia may be regarded as biodiversity reservoirs during cold phases (Hampe et al., 2013). In other words, 'local anomalies' nevertheless have great relevance in terms of biological conservation and, with regard to the focus of this paper, multi-centennial and multi-millennial maintenance of hominin populations. Traditionally we have been highly dependent on palaeoenvironmental reconstructions that are actually based on 'average' pollen rain signals, reflecting the vegetation of broad continental environments (marine sequences) or very vast depositional basins (lakes) (e.g. Birks, 1986;see Carrión, 2004 for a discussion). These signals may be too coarse to facilitate reasonable speculation about the influences of plant ecology on the past ecology, biogeography or behaviour of human populations .
In a certain sense, the traditional perspective on the physical environment's influence on ecology and human evolution has been climaticist, in that most studies take as a general guideline the global data on astronomically induced climatic variation (Potts, 1998;Behrensmeyer, 2006). Not surprisingly, traditional deterministic views of vegetation-climate response are not satisfactory in explaining the observed patterns in the pollen diagrams of the Iberian Peninsula (Carrión, 2001;Carrión et al., 2011;González-Sampériz et al., 2020). We should consider a 'glacier refugium' as an entity endowed with spatial peculiarity and physiographical complexity, that is, plant mosaicity. Without a doubt, the Neanderthals of the Iberian Pleistocene were not everywhere. Here we see that some important occupations, otherwise permanent or quasipermanent, suggest human preferences for the forest and tree savannah landscapes, probably because they presented environmental circumstances that favoured survival, including opportunities for hunting, gathering and shelter. The use of plant materials for food and technological items cannot be disregarded (Ward et al., 2012a,b;Hardy, 2018;Zilhão et al., 2020).
However, we should emphasize that Neanderthals adapted and responded properly to climatic changes, and the great diversity of palaeoenvironmental reconstructions show their occurrence from tundra to closed forests (Finlayson and Carrión, 2007). It is then clear that they were characterized by behavioural versatility, phenotypic plasticity and gene polymorphism . Our goal here is to stress that the forested environments have been somewhat neglected among the broad diversity of habitats where Neanderthals subsisted not only during interglacials and interstadials, but also (in refugial stations) during cold and dry stages.
The role of Iberian glacial refugia in the radiation and selection of the Neanderthal lineage is still unknown. Although not as extensive and crucial for human evolution as eastern and southern Africa, the Mediterranean region is a biodiversity hotspot (Spathelf and Waite, 2007) with a high level of endemism, and probably a remnant of a larger and more fragmented territory that functioned like an engineer of plant and animal diversity over the Cenozoic . The Iberian Peninsula exhibits rugged and complex landscapes with a wide diversity of habitats, locally highly sensitive to climate change (Sechrest et al., 2002), and containing large amounts of evolutionary history, ecological interaction and biotic complexity (Bascompte et al., 2006). Perhaps these factors affect diversification by inducing speciation and reducing extinction rates.