ORIGINAL RESEARCH published: 09 September 2021 doi: 10.3389/fevo.2021.733062 Night Capture of Roosting Cave Birds by Neanderthals: An Actualistic Approach Guillermo Blanco 1* , Antonio Sánchez-Marco 2 and Juan José Negro 3 1 Department of Evolutionary Ecology, Museo Nacional de Ciencias Naturales, CSIC, Madrid, Spain, 2 Area of Neogene and Quaternary Faunas, Institut Català de Paleontologia Miquel Crusafont, Barcelona, Spain, 3 Department of Evolutionary Ecology, Estación Biológica de Doñana, CSIC, Seville, Spain Evidence is accumulating on the regular and systematic Neanderthal exploitation of birds. However, the motivations, mechanisms, and circumstances underlying this behavior remains little explored despite their potential implications on Neanderthal Edited by: Pasquale Raia, ecology and capabilities. Fossil remains of choughs (Pyrrhocorax, Corvidae) are among University of Naples Federico II, Italy the most abundant in cave sites with Mousterian technology. We reviewed the Reviewed by: evidence showing that Neanderthals processed choughs for food, and confirmed Maciej Tomasz Krajcarz, that it occurred frequently over a widespread spatial and temporal scale. This lead Institute of Geological Sciences (PAN), Poland us to propose the hypothesis that the cave-like refuge is the keystone resource Deepa Agnihotri, connecting Neanderthals and choughs captured at night in rocky shelters eventually Birbal Sahni Institute of Palaeobotany, India used by both species. By adopting an actualistic approach, we documented the Costantino Buzi, patterns of refuge use and population dynamics of communally roosting choughs, University of Tübingen, Germany the strategies and technology currently used to capture them, and their behavioral *Correspondence: response against experimental human predators at night. Actualistic experiments Guillermo Blanco g.blanco@csic.es showed that large numbers of choughs can be captured without highly sophisticated tools at night regularly and periodically, due to their occupation year-round during Specialty section: long-term periods of the same nocturnal shelters, the constant turnover of individuals, This article was submitted to Paleoecology, and their high site tenacity at these roost-sites even after recurrent disturbance and a section of the journal predation. Captures even with bare hands are further facilitated because choughs tend Frontiers in Ecology and Evolution to flee confused into the cavity in darkness when dazzled and cornered by human Received: 29 June 2021 Accepted: 13 August 2021 (experimental) predators. Given the extreme difficulty of daylight chough capturing Published: 09 September 2021 in open country, nocturnal hunting with the help of fire in the roosting caves and Citation: consumption in situ are proposed as the most plausible explanations for the strong Blanco G, Sánchez-Marco A and association of choughs and Neanderthals in fossil assemblages. Night hunting of birds Negro JJ (2021) Night Capture of Roosting Cave Birds by has implications for the social, anatomical, technological, and cognitive capacities of Neanderthals: An Actualistic Neanderthals. Approach. Front. Ecol. Evol. 9:733062. Keywords: caves, choughs, fire-related technology, hunting tactics, micronutrients, Mousterian sites, doi: 10.3389/fevo.2021.733062 Pyrrhocorax, troglodyte habits Frontiers in Ecology and Evolution | www.frontiersin.org 1 September 2021 | Volume 9 | Article 733062 Blanco et al. Nocturnal Bird Hunting by Neanderthals INTRODUCTION assigning unprecedented cognitive abilities to Neanderthals, thus sustaining the ongoing debate and opening new research Neanderthal cognitive and physical capacities remain a hotly avenues in human evolution. Even though this hypothesis is debated topic in human evolution. Social networking, including gaining momentum, the understanding of bird exploitation verbal communication, planning, anticipation, and coordination and its eco-evolutionary implications are constrained by partial of labor division for obtaining food are linked to modern and unbalanced databases regarding birds as compared with cognitive abilities with broad eco-evolutionary implications other prey groups in sites with Neanderthal occupation. These (Villa and Roebroeks, 2014; Botha, 2020; Breyl, 2020; Lombard information sources rarely include comprehensive qualitative and Högberg, 2021; Wadley, 2021). Among socially coordinated and quantitative data on avian prey, much less on the relative activities, hunting of large terrestrial game has been argued to importance of this over other food types, on the potential provide pulses of food covering most energetic and nutritional factors governing the occurrence of particular bird species, or demands of Neanderthals (Richards et al., 2000; Bocherens on the preferential target of some species over others. Therefore, et al., 2005). Yet dietary reconstructions are challenging from information and circumstantial evidence about bird catching and an ecological perspective, especially when faced the sources and the exploitation of avian populations could shed light on the methods used to obtain meat by distinguishing predation from ecology and cognitive abilities of Neanderthals. scavenging (Marean and Yeun Kim, 1998; Villa et al., 2005). Among birds exploited by hominins, raptors, pigeons, and Smaller prey or plants providing scarcer but more regularly corvids, especially the Pyrrhocorax choughs (Passeriformes, available food and essential nutrients for optimal or specific Corvidae), have been frequently recorded in the Pleistocene metabolic requirements are gaining importance in the study of the Palearctic (Tyrberg, 1998, 2008). Choughs are medium- of Neanderthal trophic ecology, both in their strongholds in sized (200–360 g depending on species and sex), highly social Europe (Hardy and Moncel, 2011; Nabais and Zilhao, 2019) corvids widely distributed at continental scales but with currently and in the easternmost part of Neanderthal distribution in the fragmented and isolated populations throughout the Palearctic Altai mountains of southern Siberia (Salazar-García et al., 2021). (Cramp and Perrins, 1994). Choughs are represented by two Recently, increasing evidence is accumulating on the regular sister species, the red-billed chough (P. pyrrhocorax) (Figure 1A) and systematic Neanderthal exploitation of marine resources and the Alpine chough (P. graculus) (Figure 1D), slightly such as mollusks providing limiting nutrients (e.g., Zilhão differing in appearance and altitude-related habitat use and et al., 2020, and references therein) and flying birds of many distribution, but sharing many aspects of their ecology and species (e.g., Finlayson et al., 2012; Negro et al., 2016, and behavior. Both inhabit open, montane, and rocky inland and references therein). Hunting elusive birds can be cognitively coastal landscapes, locally in sympatry (Cramp and Perrins, challenging, technologically difficult, and energetically costly. 1994). They are singular among Palearctic birds by their However, this type of prey can eventually represent abundant remarkable troglodyte habits. Large caves, cracks, potholes, and and nutritionally valuable resources for versatile omnivorous chasms are used for nesting, resting during the hottest daylight hunter-gatherers (Negro et al., 2016), especially when or hours and inclement weather conditions, and especially for where herbivore mammals were scarce or seasonally available. communally night roosting often congregating hundreds of The frequency, circumstances, methods, and nutritional inputs individuals (Cramp and Perrins, 1994; Blanco and Tella, 1999; associated to bird capture and exploitation have important, albeit Blanco et al., 2009). little explored, implications in Neanderthal physical/anatomical, Chough fossil remains are among the most abundant elements social, technological, and cognitive capacities. in the paleontological avian record, as one or both chough By knowing specific features of the ecology and behavior of a species are present in almost all of the karstic infillings from food species, it is possible to infer capture and exploitation tactics the European Middle and Early Pleistocene (Tyrberg, 1998, by their consumers and then to conduct actualistic experimental 2008). Taking into account that choughs nest and rest in approaches taking extant predators and scavengers as study rocky shelters, finding their bones in fossil deposits has been models (Sala and Arsuaga, 2018). These approaches may also treated in the literature as a consequence that did not need allow the making of comparative inferences about the capacities further explanation in the absence of anthropic cut marks. The of Neanderthals for food procurement by using extant humans as spatiotemporal coexistence of Neanderthals and choughs across smart-hunter referents (Negro et al., 2016). Generalizations about Eurasia would have favored a regular contact between these cave- the foraging and feeding ecology of Neanderthals have proposed dwelling species, and therefore an easy access of Neanderthals bird exploitation owing to a generalist and versatile foraging and other hominins to choughs. In fact, when searched for mode (Blasco and Fernández Peris, 2012; Negro et al., 2016). cut marks, an active processing of wing feather removal for A recent non-mutually exclusive hypothesis states that birds meat consumption, ornamentation, or both, has been recorded were targeted and systematically or opportunistically predated in cave sites with Mousterian lithic tools (e.g., Peresani et al., for not only consumption, but also for feathers, claws, and 2011; Finlayson et al., 2012; Blasco et al., 2016). Therefore, the bones for ornamentation and other symbolic purposes (Fiore extensive occurrence and frequency of chough remains from the et al., 2004; Sánchez Marco and Cacho Quesada, 2010; Peresani Mousterian onward, until the end of the Pleistocene, suggests et al., 2011; Finlayson et al., 2012; Radovčić et al., 2015, 2020; an even stronger association than previously acknowledged. To Fiore et al., 2016; Majkić et al., 2017; Blasco et al., 2019). assess the spatial and temporal extent of Neanderthals and This appealing hypothesis has revolutionary implications by choughs co-occurrence we performed a literature review of Frontiers in Ecology and Evolution | www.frontiersin.org 2 September 2021 | Volume 9 | Article 733062 Blanco et al. Nocturnal Bird Hunting by Neanderthals FIGURE 1 | (A) Red-billed choughs. (B) Map showing the current pooled distribution range of red-billed and Alpine choughs (red area, according to BirdLife International and Handbook of the Birds of the World, 2019; freely available at http://datazone.birdlife.org/species/requestdis), and estimated range of Neanderthals (green barred area; modified from Ryulong, 2016; freely available at https://www.ancient.eu/image/5958/geographical-range-of-neanderthals/). (C) Sites with evidence of both Neanderthal occupation and presence of chough skeletal elements. The presences of red-billed choughs, Alpine choughs or both species in the sites are represented by red, yellow, or both-colors circular markers. Markers with blue borders represent sites with presence of processed chough fossils remains, while circles with black borders represent sites where processing marks were not searched for or not recorded. References of the sites:1–3: Gorham, Vanguard, Ibex caves; 4: Cova Negra; 5: Bolomor; 6: Arbreda; 7: Pié Lombard; 8: Fumane; 9: Grotte de Castelcivita; 10: Figueira Brava; 11: Beneito; 12: El Castillo; 13: Labeko koba; 14: Romaní; 15: Gegant; 16: Coll Verdaguer; 17: Combe Grenal; 18: La Baume de Gigny; 19: Sesselfelsgrotte; 20: Vindija; 21: Grotta del Broion; 22: Valle Radice; 23: Grotta Guattari; 24: Grotta di Sant Agostino; 25: Temnata; 26: Bacho Kiro; 27: Mezmaiskaya; 28: Kebara. Sources are shown in Table 1 and Supplementary Table 1. (D) Alpine choughs. Maps were generated with QGIS software and modified with Microsoft PowerPoint 2010 (Microsoft Corporation, Redmond, WA, United States, https://www.microsoft.com/pt-pt/microsoft-365/previous-versions/office-2010) under CSIC Organizational License. Photo credits: A (G. Blanco), D (J.J. Negro). published information on sites where these species were present. 40◦ east, and between 30◦ and 40◦ north latitude (Figure 1C). In the case of the choughs, the evidence was fossil. Neanderthals Processing marks on chough remains were confirmed in all presence was inferred through fossils or by lithic toolkits from the sites (n = 9) where they were searched for Table 1, while in Middle Paleolithic. We paid particular attention to taphonomic other sites (n = 19), evidence of processing was generally not studies determining whether chough remains were modified by searched for or not reported (Figure 1B and Supplementary human action (i.e., presenting evidence of cut or tooth marks, Table 1). Cases are particularly abundant on or close to the as well as burn signs) or accumulated on the site by other coasts of the Iberian Peninsula. Although a majority of the processes. This review indicated that the current distribution of levels where processed choughs were found belong to the choughs greatly overlaps with that estimated for Neanderthals late Middle Paleolithic, when the Neanderthals were about to (Figure 1B). The coincidental presence of Neanderthals and become extinct, some evidence is much older, as in Bolomor choughs at anthropological sites is common and widespread Cave, Iberian Peninsula (Table 1). We cannot rule out that (Figure 1C and Table 1). As of today, there is evidence of Neanderthals that may have used specific lithic industries such consumption of both chough species in sites with Mousterian as the Micoquian in the easternmost end of their distribution technology (Middle Paleolithic) between longitude 10◦ west and (Kolobova et al., 2020), also procured choughs for themselves, Frontiers in Ecology and Evolution | www.frontiersin.org 3 September 2021 | Volume 9 | Article 733062 Blanco et al. Nocturnal Bird Hunting by Neanderthals TABLE 1 | Number of identified specimens (NISP), minimum number of individuals (MNI), and NISP with evidence of anthropogenic processing marks on chough fossil bones at Mousterian sites. Site name (location) Chronology Species NISP (MNI) NISP with marks Interpretation Source Pié Lombard (France) c. 70 ka Pp, Pg, Psp 1091 (73) 26 D, S Romero et al., 2017 Gorham’s Cave (Gibraltar) 50–27.9 ka Pp, Pg, Psp 518 (104) 91 D, C, S Blasco et al., 2016 Vanguard Cave (Gibraltar) 50–40 ka Pp, Pg, Psp 17 (7) 1 D Finlayson et al., 2012 Ibex Cave (Gibraltar) 53.9–34.8 ka Pp 20 (3) 4 D Finlayson et al., 2012 Grotta di Castelcivita (Italy) 47.6–41.1 ka Pp + Pg 16 (7) 2 D Fiore et al., 2020 Fumane (Italy) 47.6–42.2 ka Pp, Pg, Psp 77 (9) 24 D, S Fiore et al., 2016 Arbreda (Spain) c. 40 ka Pp, Pg, Psp 162 (11) 3 D Lloveras et al., 2018 Bolomor (Spain) 350–120 ka Psp 6 (1) 1 D Blasco and Fernández Peris, 2012 Cova Negra (Spain) MI6-MI5 Pp, Pp, Psp 35 (14) 27 D, C Martínez Valle et al., 2016 Pp, Pyrrhocorax pyrrhocorax; Pg, Pyrrhocorax graculus; Psp, Pyrrhocorax sp; D, defleshing; C, cooking; S, symbolic (feathers). as data on chough processing for those populations are currently to choughs in their rocky shelters as the most parsimonious unavailable. None-the-less, the known diet of those far-away explanation sustaining this connection, instead of their capture Neanderthals was broad and therefore similar to that of other during daylight in nesting and foraging sites. By adopting an Neanderthals elsewhere (Salazar-García et al., 2021). actualistic approach, we document the patterns of refuge use Choughs would have been particularly abundant in the and population dynamics of communally roosting choughs, the past, but they should have been especially easy to capture or strategies and technology currently used to capture them, and targeted preferentially by Neanderthals to explain this remarkable their behavioral response against experimental human predators association. However, an easy capture conflicts with the at night. Our main aim is to evaluate the eco-evolutionary distrustful character and great intelligence of corvids (Marzluff implications of chough exploitation, by considering the generally and Angell, 2007). Unlike scavenger species whose capture would overlooked potential nocturnal hunting activity of Neanderthals. be predictable at large animal carcasses exploited by Neanderthals Specifically, we aimed to deep on (1) Neanderthals’ cognitive (Finlayson and Finlayson, 2016), choughs perform long daily, capabilities to weave a night ambush toward elusive birds; (2) seasonal, and altitudinal movements (Cramp and Perrins, 1994; social abilities to arrange and achieve massive bird captures Morinha et al., 2017b) to feed on invertebrates, seeds, and fruits, in darkness; (3) fire-related technology associated to enlighten but never on carrion (Soler and Soler, 1993; Blanco et al., 1994; themselves, and dazzle, harass, corral, and grab flying prey; Sánchez-Alonso et al., 1996; Laiolo and Rolando, 1999), which (4) anatomical features related with an improved vision to makes the daylight location of foraging flocks very unpredictable locate and track roosting flocks, and cautiously approach and (Blanco et al., 1998; Morinha et al., 2017a). Choughs are also access the caves under low light and dark conditions, as well known by their strong and acrobatic flight that makes them as climbing abilities previously overlooked; and (5) nutritional difficult targets for most diurnal predators (Cramp and Perrins, rewards associated to a chough meal. 1994; Cuevas and Blanco, 2009), including modern humans with relatively rudimentary hunting tools, as indicated by the chough elusive escape behavior and long flushing distance (Jiménez et al., MATERIALS AND METHODS 2013). However, choughs can be very vulnerable against human predators in their night shelters (Ibáñez, 1986; Zúñiga, 1989; Night Shelters and Capture of Choughs Blanco et al., 2019). Monitoring of population size and trends of choughs and other The motivations, mechanisms, and circumstances underlying corvids often includes the simultaneous counts of individuals chough exploitation remain unresolved despite the potential in shelters used for communally roosting over large geographic implications on Neanderthal ecology and capabilities. Caves areas. With this aim, it is necessary to locate previously the active represent an essential resource tightly linked to human evolution. roosts each season, by monitoring foraging flocks and the flights Suitable refuges would have been scarce and difficult to locate to and from these sites at sunset and sunrise, respectively (Blanco and defend against conspecific competitors and carnivore et al., 2019). These activities were conducted during the last predators, especially for hominins venturing into unknown three decades in several regions of Spain, which allowed us to regions. Choughs use caves and a variety of other large indoor determine the size of communally roosting flocks and to locate rocky shelters for night roosting throughout the year (Blanco and characterize roosting sites over a variety of habitats. Here, et al., 1993; Cramp and Perrins, 1994), which implies that we focused on the more widely distributed and abundant red- refuge and abundant food for Neanderthals would converge in billed chough, which also shows currently less restricted habitat these places. Therefore, cave-like refuge represents a keystone requirements than the Alpine chough in Iberia, although both resource connecting Neanderthals and choughs captured at night species can form mixed flocks and share roosting sites (Cramp in rocky shelters eventually used by both species. This hypothesis and Perrins, 1994). The daily, seasonal, and inter-annual use posits the nocturnal hunting activity of Neanderthals directed of communal roosts was assessed by frequent monitoring of Frontiers in Ecology and Evolution | www.frontiersin.org 4 September 2021 | Volume 9 | Article 733062 Blanco et al. Nocturnal Bird Hunting by Neanderthals multiple sites across the years, which confirmed that communal as well as smaller cavities concentrated in particular sectors of roosts were generally used throughout the year with maximum cliffs (see examples in Supplementary Figures 1A–C). These sites numbers of individuals during winter (Blanco et al., 1993, 2019; showed entrances of variable size (from about 1 to >20 m width Morinha et al., 2017b). Therefore, we considered winter counts and up to 30 m high or deep), shape (circular, elliptic, elongated, (January) to determine roosting flock sizes in the monitored irregular), and accessibility for humans (from good accessibility sites. The nature and characteristics of each roosting site were on foot or relatively easy climbing to inaccessible without using recorded and categorized as (i) large natural cavities in rocking climbing gear). The entrances (single or multiple) of these cavities terrain, and (ii) human-made cavities and structures that mimic invariably connect with dark and deep indoor shelters completely the indoor conditions of natural ones. To evaluate roosting site closed (caves) or open in its upper part, both partially (cracks in tenacity, we considered the number of years that each particular the ground or cliffs) and totally (chasms). The dimensions of a site was used by choughs during the period 1988–2020. Given sample of accessible sites ranged from a combination of relatively that the monitoring period was different for each particular site narrow spaces with an elongated but variable conformation and depending on the date of first occupation or localization, we height, to large spaces of several hundred square meters in considered those sites monitored for at least 5 years. area and up to >40 m in height and depth. The remainder The localization of communal roosting sites allowed us to communal roosts were located in anthropogenic structures, attempt capturing choughs to individually mark and study including caves, tunnels, quarries, and wells generated by mining them in a sample of these sites (Blanco and Tella, 1999; activities, abandoned farmhouses, and wells in agricultural areas, Morinha et al., 2017b). The apparently best way to proceed to and historical buildings, bridges, and other artifacts in urbanized capture as many choughs as possible was previously planned areas (see examples in Figure 2A, Supplementary Figure 1D). according to the access, dimensions, structure, and escape The entrances and indoor spaces of these anthropogenic sites exits in each site. We recorded the type and characteristics used as shelters by choughs are easily accessible for humans, of each roosting site where the captures were conducted, the except when located in large infrastructures such as bridges or number of persons involved, the strategy and tools used, the the retaining walls of reservoir dams. behavior of choughs toward contemporary nocturnal human predators (as a proxy of prehistoric cave-dwelling humans), and Roosting Flock Size, Site Tenacity, and the number of individuals captured in each event. Choughs Individual Turnover were captured and handled by authorized personnel. Handling Flock size of communally roosting choughs in January ranged time was minimized to reduce stress and injury during between 3 and 737 individuals (mean ± SD = 76 ± 91, capture/sampling. After manipulation choughs were released in median = 48, n = 542 counts from 93 sites from 1990 to 2020). good state where captured. Among winter roosting sites monitored for at least 5 years We acknowledged that a proportion of choughs was (range: 5–32), most (98.3%, n = 60) were used recurrently individually marked with plastic rings with unique alpha- (mean ± SD = 8.6 ± 5.1 years, range = 1–25). numeric codes to assess the replacement rate of identifiable The number of choughs that used the same communal roosts individuals in communal roosts. Thus, individual turnover in in three sampled sites varied on average by 26.2% ± 15.0 between the roosts was used as a form to evaluate whether choughs consecutive days (range = 7.7–43.4%). These variations were could be viewed as a renewable resource for human predators. confirmed by the daily turnover of individuals, evaluated through Thus, we monitored the flock size and the presence of ringed the individual identification of ringed choughs. Overall, 33 (58%), choughs identified with spotting scopes over consecutive days in 12 (21%), and 12 (21%) of the choughs identified by their rings communal roosts. In addition, we evaluated the impact on flock in the three sites (n = 57) were observed in one, two, or three dynamics and site desertion of recurrent year-round captures consecutive days in the same roosts. On the few occasions when in particular roosting sites across the years, and the turnover we captured and banded all individuals in a particular site, we of individually marked choughs in these places by means of confirmed this partial daily turnover by determining the presence multiple captures. In a few cases, we were able to capture and ring of a proportion of unmarked individuals entering the same site all individuals present in a particular roosting site and in each the following evening. nocturnal capture event, which allowed us to further evaluate the site-tenacity of flocks and the daily turnover of a proportion of individuals by monitoring the number and identity of individuals Chough Behavior Against Nocturnal using the roosts the following days. Human Predators and Capture Bags Chough captures for research purposes were mostly conducted in roosting sites whose entrances were accessible on foot. These RESULTS sites were accessed through a silent night-time approach with the help of the minimum necessary artificial light 1 to 3 h after dark, Characterization of Roosting Sites or less frequently before sunrise. Chough behavior in the face of By tracking chough flocks, a total of 185 communal roosting sites such a nocturnal threat generally varies depending on the capture were located. A proportion (33%) of these sites was large cavities sequence. At first, some choughs try and manage to escape generated by diverse geological processes in variable rocky and from the human “predators,” especially the most alert individuals sedimentary substrates, including caves, crevices, and chasms, perching closest to the cavity exits. After this initial reaction, the Frontiers in Ecology and Evolution | www.frontiersin.org 5 September 2021 | Volume 9 | Article 733062 Blanco et al. Nocturnal Bird Hunting by Neanderthals FIGURE 2 | (A) Example of a communal roost of red-billed choughs in a well (Cuenca province, Spain); (B) Details of the position of choughs after cornered them by human (experimental) predators, and (C) their capture by hand and (D) with the help of a ladder in communal roosts located in buildings in Aragón (Spain). (E) A red-billed chough after marked with rings for individual identification. Photo credits: A (J. A. Cuevas), B (G. Blanco), C,D (J. M. García), E (Ó. Frías). most frequent chough attitude when lit with flashlights was to flee were carried out at most of the sites (mean ± SD = 79 ± 114 to the highest positions or into the deeper and often progressively individuals captured per particular site, n = 70, across the years; narrower and darker parts of the cavity acting as a cul-de-sac, thus range = 3–522) without roosting flock desertion in any site. This facilitating the capture of most individuals (Figure 2B). On the was further supported by the large proportion of individuals few occasions that captures were carried out in vertical cavities recaptured in several occasions, as confirmed by the ring codes like wells (Figure 2A) and chasms (Supplementary Figure 1C), (Figure 2E). In addition, breeding choughs were captured by the behavior of choughs was invariably to take refuge toward using the same procedures in their nesting sites, generally one or the bottom. This allowed capturing most or all individuals by two members of the mated pair, while developing nestlings were accessing them with climbing gear. captured during daylight in their nests (accessed by ladders and The number of persons involved was variable (generally a climbing gear) when feathered but before fledgling on predictable team of 4–5 persons, range: 2–10) depending on the size of the dates (population peak from mid to late May) each year. roosting flock. At relatively small and narrow roosting sites, the Depending on geographic area and season, other bird species captures were conducted at the cavity exits by people equipped were opportunistically caught in much lower numbers during the with large butterfly hand-nets and headlamps, so that the choughs night-time captures of choughs, including mostly kestrels (Falco could be dazzled and intercepted without damage when they tried tinnunculus and Falco naumanni), feral Rock dove (Columba to escape to the outside. On many (not quantified) occasions livia), Barn owl (Tyto alba), Red start (Phoenicurus ochruros), and the dazzled choughs were captured by bare hand in flight a variety of other birds. (Figure 2C), on the ground, and on the indoor walls with the help of hand nets and ladders (Figure 2D). Large roost entrances were sometimes partially covered with nets to maximize the DISCUSSION number of catches. By using all these procedures, 5,525 full-grown choughs were Unraveling how and how often the remains of each bird captured in 296 events (mean ± SD = 19 ± 29 individuals species reached the fossil deposits is paramount to understand per event, range = 1–258) at 70 different communal roosting its abundance, distribution, behavior, paleoenvironmental sites, and released there after data collection. Overall, choughs conditions, and predator-prey relationships in the paleocenosis. were captured in large crevices in cliffs (n = 206 individuals), With regard to archaeological sites, addressing these questions mining caves and quarries (n = 171), traditional agricultural wells can also provide insight on human ecology, behavior, and (n = 179), chasms (n = 34), an old trench for an anti-aircraft gun evolution. During the Pleistocene, choughs were distributed (n = 101), historic buildings (n = 186), and a variety of abandoned throughout Europe, sharing caves and rocky shelters with and in-use farm houses (n = 1,969), livestock corrals (n = 2,520), different Homo species. Choughs and Neanderthals largely and industrial warehouses (n = 159). Several capturing events overlapped in their geographical distributions during this period, Frontiers in Ecology and Evolution | www.frontiersin.org 6 September 2021 | Volume 9 | Article 733062 Blanco et al. Nocturnal Bird Hunting by Neanderthals from western Europe to at least the Altai mountains in the temporal range. This supports a targeted and extensive chough East, and their ranges were likely further shared during the exploitation rather than incidental predation or scavenging, Pleistocene when choughs were more widely distributed in and hunting by just a few specialist Neanderthals. Evidence central and eastern Europe according to the fossil record, while of chough exploitation commenced to accumulate in the last in the Holocene the range of choughs became notably restricted, decade, even though cut marks are not necessarily associated to particularly for the Alpine chough (Tyrberg, 1998, 2008; Sánchez the consumption of this kind of relatively small prey. Therefore, Marco, 2004). Our review confirms that chough fossil remains we should expect analyses of fossils excavated in the past, or are among the most abundant in cave sites with Neandertal those from ongoing or future studies will provide a more detailed presence where avifaunal remains have been recorded and picture of the spatial and temporal extent of the Neanderthal- quantified. It may be of great interest to explore in the future chough utilitarian association. the existence of this pattern of chough consumption in caves Overall, the motivations, mechanisms, and circumstances with ante- and post-Mousterian transition lithic industries underlying the widespread and frequent Neanderthal (Micoquian and Szeletian) (Kolobova et al., 2020). exploitation of choughs and other birds (especially rock In this study, we aimed to attempt understanding how doves) have remained unresolved despite their broad eco- and why Neanderthals exploited choughs, not to review the evolutionary implications. Same as contemporary humans paleontological record including these species, nor to posit currently do for research, Neanderthals could aurally detect hypothesis about the accumulation of chough remains due to and visually follow chough flocks to their shelters to establish other, generally unknown, predators. Of course, there are many temporary or permanent settlements, and to take advantage sites where choughs fossil remains have been found not associated of an abundant and easy-to-use trophic resource consumed to cave occupation by Neanderthals (reviewed by Tyrberg, 1998, in situ. At present, dozens to hundreds of choughs can gather 2008; Finlayson et al., 2012), and others with Neanderthal at night shelters year-round. At these sites, variable numbers lithic industries where chough consumption was suspected but of dazzled and cornered choughs (up to 250 individuals) can anthropogenic processing marks on fossil bones were not been be captured by hand nets and bare hand, both in rocky sites as searched or recorded (Supplementary Table 1). Even though caves, crevices, and chasms, as well as in human-made cavities some chough skeletal remains may correspond to individuals and buildings mimicking the conditions of caves. As an example, dying naturally in the caves, or be the results of capture by other one of us (GB) and his collaborators in their twenties were able predators (e.g., Laroulandie, 2010), to our knowledge, there is to catch about ten choughs each in repeated capture events no evidence of particular predator species accumulating chough conducted with bare hands and just the help of headlamps remains in Neanderthal sites or current deposits. This may be due and bags by free climbing into roosting crevices and caves, to the difficulty in capturing choughs during the day by daytime although assuming the risk of dangerous falls. Choughs can be predators that could potentially accumulate remains in the caves. captured regularly and periodically because their occupation In fact, potential prey accumulators in caves could be restricted to year-round during long-term periods of the same night shelters, medium-sized carnivore mammals such as canids and mustelids the constant turnover of individuals, and their high site tenacity mostly acting at night. Diurnal raptors able to capture choughs of roosting and nesting sites even after disturbance and recurrent (e.g., Aquila chrysaetos, Aquila fasciata), currently do it rarely predation (Zúñiga, 1989; Blanco et al., 1996; Banda and Blanco, (mostly upon juveniles) when compared to other species of birds 2009, 2014; Laiolo et al., 2009; Morinha et al., 2017b). The easier to capture (Ontiveros, 2016; Arroyo, 2017). These eagles use of flashlights facilitates the capture providing artificial do not accumulate food remains in nests and rarely beneath illumination and by dazzling choughs. Captures by hand are perches, as demonstrated by the need of repeated snapshot further enhanced by the behavior of choughs in the presence samplings in these sites to collect enough of these generally scarce of experimental human predators when they enter the roosts, food remains for dietary studies (Ontiveros, 2016; Arroyo, 2017) since they tend to flee confused into the cavity in darkness. before they disappear due to scavengers. These eagles do not Therefore, the relative ease of nocturnal capture of chough access the interior of caves used by choughs as roosting sites, flocks by hominin predators without great technical means although their prey remains could be passively washed there or is demonstrated by comparison with modern humans used transported secondarily by scavengers (Laroulandie, 2010). In as a proxy. Unlike against other predators, choughs would be addition, nocturnal predators such as large owls and carnivore especially vulnerable to Neanderthals due to their unique use mammals cannot hunt in the complete darkness of deep caves of artificial lighting by means of fire in the complete darkness at night, further hampered by the inaccessible positions that of caves at night. choughs use to sleep inside the roosting sites. Therefore, it According to the hypothesis of a cave connection between seems unlikely that the accumulation of chough remains in sites choughs and Neanderthals, other cliff-nesting species are where human-made cut marks has been found was mostly due expected to occur also frequently in Neanderthal sites. However, to other predators such as owls and carnivore mammals. In the fossil remains of choughs far exceed those of other rock- fact, predators smaller than Neanderthals would probably leave dwelling species such as swallows, swifts, and raptors (Tyrberg, more recognizable and frequent marks than the Neanderthals 1998, 2008; Sánchez Marco, 2004). In support of a targeted themselves (Laroulandie, 2010; Lloveras et al., 2020). Instead, seeking for choughs, other similarly sized and cliff-nesting there is extensive evidence that Neanderthal people processed corvids roosting on trees, as well as tree-nesting species also choughs for food frequently over a widespread spatial and roosting on trees (genus Corvus, Pica, Cyanopica), should be Frontiers in Ecology and Evolution | www.frontiersin.org 7 September 2021 | Volume 9 | Article 733062 Blanco et al. Nocturnal Bird Hunting by Neanderthals much less frequent in the Mousterian sites, which is actually in birds (Tella et al., 2004), and these molecules are essential true (Tyrberg, 1998, 2008; Sánchez Marco, 2004) despite their micronutrients playing roles in different physiological processes scavenging and mostly colonial habits would make them frequent including vision and immunological function (Álvarez et al., prey (Finlayson and Finlayson, 2016). Choughs often form 2014; Milani et al., 2017). mixed foraging flocks with other corvid species (Cramp and Translating the above knowledge to a possible regular capture Perrins, 1994; Cuevas and Blanco, 2009; Blanco et al., 2019) of choughs by Neanderthals has multiple implications on their comparatively much less consumed by Neanderthals, which ecology, behavior, and capabilities. Given the extreme difficulty supports a differential capture of choughs in roosting sites (never of daylight capturing choughs in open country without highly shared with other corvids) rather than in open country. In sophisticated tools, nocturnal hunting with the help of fire in turn, a parallel case of bird consumption by Neanderthals is the roosting caves is the only plausible explanation for the offered by the rock dove. This pigeon is associated to rocky strong association of processed choughs and Neanderthals in outcrops for nesting and roosting, and it has been suggested fossil assemblages. The hunt resulting in chough death for that it was regularly consumed by Neanderthals according consumption is doubtless easier than their current capturing to processing marks in fossil bones (Blasco et al., 2014). alive without damage for research purposes. This could be Choughs and rock doves, share not only the troglodyte nesting achieved by throwing stones or by the documented use of and communal roosting habit and sites but a similar body long wooden sticks and stone-tipped spears (Aranguren et al., mass. A single individual of any of these two species would 2018; Hoffecker, 2018). Dazzling and bewilderment could be make an adequate meal for a hominin, and in fact several promoted by the light of torches or even through controlled individuals of both species may be captured simultaneously fires with parapets of branches at the entrance to the cavities, at roost sites. In addition, pigeons are appreciated as food both also producing heat, noise and smoke increasing confusion worldwide, while choughs are highly palatable according to in the choughs. In fact, Neanderthals mastered the use of personal appreciations of hunters consuming them in the past in fire all along their existence as a species from about 400– Spain and nowadays in Morocco. 300,000 years ago (Roebroeks and Villa, 2011; Sanz et al., 2020; As it occurs with rock doves, choughs presenting an MacDonald et al., 2021), and the use of constructions inside overlapping distribution range with the Neanderthals would of long caves in total absence of natural light also testifies have been a suitable food resource exploited regularly or as an of the use of fire for illumination (Jaubert et al., 2016). This occasional dietary backup. Perhaps an adult Neanderthal would would support Neanderthal use of fire for hunting and, to our need at least 2–3 choughs for satiation, but choughs together knowledge, this is the first documented suggestion of social with rock doves could be harvested en masse at night in the hunting of birds at night with the help of fire technology. roosting sites. Neanderthal group size has been estimated to This necessarily implies prior organization for silent night-time be about 10–20 adults and their children (De Groote, 2018). approach to the caves, and episodic-like memory linked to Capturing 40–60 choughs in a single hunting bout by just a social coordination for previously planned nocturnal hunting, few skilled hunters in a roost site could be entirely possible which suggests cognitive capabilities for anticipation and labor according to our actualistic experiments, which suggest a valuable division involving the use of hunting kits. Handling a torch, resource on which the whole group could feed regularly. In a spear, or launching projectiles at dark by single individuals addition, choughs are relatively territorial at breeding, especially requires great working attention (Wynn and Coolidge, 2012). the red-billed, with just one couple per cave or a few in very In this particular case, the use of different tools seems more large cavities (Blanco et al., 1997, 1998). Therefore, as currently, likely to be successful if managed by individuals coordinating choughs could be only harvested regularly and in good numbers tasks than by hunting pack members using the available at night when they gather in large flocks in roosting caves. toolkit without prior planning. In addition, the apparently Breeding pairs could also be regularly captured at night in their repeated chough hunting and consumption events in the same nesting sites used for roosting year-round, while nestlings could caves, as assessed by stratigraphy, has been particularly well be seasonally harvested each spring by predating accessible nests documented in Gorham’s Cave along a minimum 20,000– at daylight. Current nocturnal bycatches in the chough roosts 30,000 years (Blasco et al., 2016). This would indicate the regular of other bird species suggest a similar process to explain their or seasonal exploitation of a renewable resource, whose recurrent relatively high frequency at Mousterian sites (Tyrberg, 1998, use is incompatible with the shared long-term occupation of 2008; Sánchez Marco, 2004; Finlayson et al., 2012). Some of the roosting caves of choughs by Neanderthals, but with an these species, including the colonial lesser kestrel (Negro et al., intermittent use by each species. This agrees with the regular, 2020), could be encountered at sites shared with choughs as seasonal occupation by short periods documented in many caves nowadays (Blanco and Tella, 1997) and perhaps also hunted associated to Neanderthal mobility (Carrion-Marco et al., 2019; there by Neanderthals. In fact, kestrels of both species proved Leierer et al., 2019). A temporal exclusion of choughs from especially clumsy and easy to capture by us at night in these their roosting sites, together with the likely long-term memory sites. The consumption of birds, even if occasional, may have of their hominin predator, could potentially lead to a hunting been not necessarily driven only because of their net caloric tradition and sustainable exploitation strategy compatible with content, but for the acquisition of micronutrients (Watts, 2020). some degree of autonoesis (sensu Tulving, 2002), a salient In particular, the red-billed chough has been reported showing feature of human condition rarely attributed to Neanderthals the highest content of circulating carotenoids recorded so far (Wynn and Coolidge, 2012). Frontiers in Ecology and Evolution | www.frontiersin.org 8 September 2021 | Volume 9 | Article 733062 Blanco et al. Nocturnal Bird Hunting by Neanderthals Neanderthals were well-endowed technologically and also DATA AVAILABILITY STATEMENT anatomically for night captures in a cave environment. First, compared with anatomical modern humans (AMH), they had The original contributions presented in the study are included features such as an improved vision in dim light (Taylor in the article/ Supplementary Material, further inquiries can be and Reimchen, 2016) that may have helped them to locate directed to the corresponding author. and track birds, and to hunt under low light and darkness conditions, including associated cranial morphology and eye size (Pearce et al., 2013). Second, Neanderthals had shorter ETHICS STATEMENT lower limbs compared to AMH. A study on the locomotor abilities of hominins (Higgins and Ruff, 2011), suggests that Ethical review and approval was not required for the animal Neanderthals were possibly better climbers in rough terrain and study because bird captures for ringing do not requires ethical inside caves than AMH. approval in Spain. The procurement of choughs by cave people does not end with the extinction of the Neanderthals. In the Upper Paleolithic, AMH also processed choughs. For instance, Laroulandie (2010) AUTHOR CONTRIBUTIONS reported the finding of 1,337 chough remains at the Upper Magdalenian site of La Vache, in France, 245 of which presented GB and JN conceived and designed the study. GB conducted cut marks. This and similar findings in other places led Finlayson the fieldwork and wrote the first draft of the manuscript. AS-M, and Finlayson (2016) to suggest that the practice of capturing JN, and GB reviewed and organized the data. All authors choughs, and particularly when the aim was to collect their participated in improving the manuscript and gave final approval feathers, may have been transmitted from Neanderthals to for publication. modern humans. The association of shelter and food in the form of choughs could have led to abstract thinking associated with this species that would reinforce the use of its feathers, and FUNDING also talons (especially the posterior digit D-I claw, showing a This study was partially funded by projects from the Junta size and shape close to a medium-sized raptor) and other parts de Comunidades de Castilla-La Mancha (PPIC10-0094-3036), (e.g., red tarsus and red or yellow beaks) as adornments. As the Spanish Ministry of the Environment (082/2002), and an alternative hypothesis, cut marks on tibiotarsus (which lack the Ministry of Science and Education (BOS2003-05066 and flesh) apparently for peeling and fracturing (Fiore et al., 2016; CGL2015-66381-P). AS-M was supported by the projects Martínez Valle et al., 2016) could be related to the consumption of CGL2016-76431-P and CGL2017-82654-P (AEI/FEDER, EU). carotenoids deposited under the tarsal scales. Therefore, although Neanderthals could have used chough feathers for symbolic purposes, their capture do not necessarily imply a focused ACKNOWLEDGMENTS searching for feathers, but for flesh and micronutrients. This is supported by the fact that the long molting period in this Conversations with Clive Finlayson and Carolina Lakunza, and species (May-November) implies that molted flight feathers in comments by Ruth Blasco, helped us to focus the study and good state accumulate in large quantities in the floor of roosting improve the manuscript. We thank all persons supporting the sites promoted by their indoor conditions and the often large fieldwork and involved in the chough captures across the years. numbers of choughs using them repeatedly. In turn, this implies We thank Jesús A. Cuevas, José M. García, and Óscar Frías for that molted feathers could be easily collected during daylight in providing pictures illustrating the study, and Pablo Salinas for the caves, while the presence and number of these and other help in the elaboration of maps. remains such as feces represent unequivocal signs of the presence and approximate quantity of roosting individuals for future meals. Whatever the actual relevance and motivations of chough SUPPLEMENTARY MATERIAL exploitation, our study sustains the ongoing debate on social, anatomical, technological and cognitive abilities associated to The Supplementary Material for this article can be found Neanderthal bird –nocturnal– hunting, thus contributing to open online at: https://www.frontiersin.org/articles/10.3389/fevo.2021. new research avenues in human ecology and evolution. 733062/full#supplementary-material REFERENCES Arroyo, B. (2017). “Águila real – Aquila chrysaetos,” in Enciclopedia Virtual de los Vertebrados Españoles, eds A. 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