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Figure 2
Energy expenditure of scavengers. The results of the experiments are shown in relation to the size of the hominin groups. Three experiments were performed for each scenario by varying the densities of predators from low density (red line) to medium density (blue line) to high density (green line). The limits of the boxes correspond to the first and third quartiles; the median is shown by a horizontal line. The whiskers mark the maximum and minimum without outliers and extreme values. Outliers and extreme values are indicated with a white dot and an asterisk, respectively.
Discussion
Scavenging is a fundamental factor in the structure of carnivorous communities in terrestrial ecosystems37. Moreover, the role of scavenging in the evolution and expansion of early hominins is a frequently debated and controversial issue19,20,22. The simulation experiments suggest that passive scavenging could be a very successful strategy for late-early Pleistocene hominins in Europe, even in competition with giant hyenas. Only when hominins foraged in very small groups, the ecosystem productivity was low, and the population densities of Megantereon and Homotherium were low or moderate, giant hyenas displaced the hominins. However, our simulations considered scavenging a unique procurement strategy for hominins, and this is an entirely unrealistic assumption. The hominins may be assumed to exhibit flexible omnivorous behaviour and are capable of adopting their diet by exploiting different plant and animal resources, including carrion, according to their availability6,8,38,39.
A requisite for the coexistence of two large scavengers, hyenas and hominins, is the availability of sufficient carcasses containing large amounts of edible resources. It has been suggested that these resources existed in Early Pleistocene Europe, owing to the presence of two sabre-tooths, especially Megantereon29,35. The estimates of the number of edible resources on the carcasses of large ungulates abandoned by the two sabre-toothed species support the interpretation of sabre-tooths as significant carrion providers. If Megantereon killed one prey every week, based on a conservative estimate, only one-third of the edible energy in the carcass would be consumed before killing a new prey (Table 2). This estimate supports the claims linking the extinction of the giant hyena in Europe to the extinction of Megantereon29,30. Interestingly, although this argument is usually applied only to Megantereon, our estimations suggest that Homotherium also produces carcasses with similar amounts of edible resources. In contrast, the resources contained in the carcasses of prey killed by the European jaguar would be markedly lower (Table 2) and similar to the average caloric content of the carcasses abandoned by recent large predators40. However, it should be acknowledged that the role of Homotherium as a producer of carcasses with high nutrient content relies on the assumption that it was a solitary species. If Homotherium was a social felid, as sometimes suggested41, a pack would be able to consume a large proportion of the carcass before abandoning it. Indeed, according to the estimates in Table 2, a pack of five Homotherium individuals would require approximately 45,000 kcal/day and consume the entire carcass of a 400 kg ungulate every 3–4 days. In such cases, only some portions, such as the brain and bone marrow, remain in the carcass because of the sabre-tooth’s inability to break bones41.
Our simulations modelled Pachycrocuta brevirostris as a solitary passive scavenger; however, this decision may be controversial because it has been proposed that P. brevirostris occupied a niche similar to that of extant spotted hyenas (Crocuta crocuta), which are highly active hunters and kleptoparasites29. However, the taphonomic study of the bone assemblage preserved at Venta Micena27,30,42 together with the morphofunctional analyses of the mandibles and teeth of Pachycrocuta from several European localities30, strongly suggests that the giant hyena was a dedicated strict scavenger or specialised kleptoparasite that stole the prey of sabre-tooths and other large carnivores. A possible argument against considering Pachycrocuta a passive scavenger30 is that carrion eaters must range over large areas in search of food, a task to which the large and non-cursorial giant hyena is not especially adapted. Based on this argument, giant hyenas did not prospect the environment in search of carrion but pursued other predators and stole their preys30. Thus, giant hyenas were kleptoparasites rather than passive scavengers. In this regard, their behaviour would be similar to that of recent spotted hyenas, as suggested by Turner and Antón29. Nevertheless, the simulation experiments suggest that if the carrion is sufficiently abundant, high mobility is not required for a passive scavenger. The walking speed of P. brevirostris was set at 5 km/h (the same as that of the hominins), and it was assigned a high energy expenditure during movement. Moreover, if giant hyenas were kleptoparasites, they would have frequent primary access to carcasses, and the bone accumulation generated by giant hyenas would be difficult to differentiate from that generated by hunting carnivores.
The social behaviour of giant hyenas is another potentially controversial topic. Turner and Antón29 suggested that giant hyenas were social, which allowed them to confront large predators and steal their prey. In contrast, the Venta Micena assemblage showed that the giant hyenas selectively transported certain parts of the carcass to their dens42. This behaviour supports the interpretation of solitary social behaviour because recent spotted hyenas transport all anatomical elements of the carcass to their den when scavenging in groups, but only selected parts when scavenging alone42. Moreover, the social behaviour of recent spotted hyenas is related to the expansion of the frontal region of the brain, a trait recently acquired in the Crocuta lineage43. Therefore, sociality may be a unique and recent acquisition in spotted hyenas.
Scavenging is a widespread behaviour among medium-sized carnivores in recent terrestrial ecosystems40, which is also practised by contemporary hunter-gatherers. Hadza obtained 20% of their meat through confrontational scavenging17,23. However, the consumption of carrion represents a “windfall” resource for Hadza foragers and not a regular activity due to some shortcomings, such as seasonal variations in encounter rates and the size and completeness of carcasses44. Wild chimpanzees also scavenge, but rarely. Anecdotal evidence of scavenging by chimpanzees has been reported from Gombe, Mahale, Taï, and Ngogo21,45. Confronting large carnivores is risky, but chimpanzees reduce this risk by increasing the number of participants and shouting and throwing stones to intimidate leopards. Scavenging, even passive scavenging, is risky. Indeed, the “fatal attraction” hypothesis46 proposes that carcass sites amplify the suppression effect of large carnivores on medium-sized carnivores. Despite being a widespread behaviour, scavenging has only been presented as a successful strategy for early hominins in the short term33. In contrast, the simulations show that scavenging could be an efficient and adaptive behaviour for the Epivillafranchian under certain conditions.
The results of the simulation experiments highlight the importance of group size for the viability of scavenging when competition is considered. Indeed, it can be argued that defending or stealing a carcass from other scavengers, as simulated in our experiments, does not differ from stealing a carcass from a predator. Interestingly, our results showed that when the group size of hominins was not sufficient to chase away their competitors, the hominins survived until the end of the simulation only when carcasses were abundant because of the high density of predators in a highly productive ecosystem (Fig. 1). This suggests that a fully passive scavenging strategy without direct confrontation with competitors would be energetically inefficient as a regular strategy (Fig. 2), although it could still be viable on an opportunistic basis. Hominins foraging alone or in very small groups could not rely on the active search for carrion as the main food resource, although they could feed on an abandoned carcass, which was found as a stroke of luck when foraging on other resources, until competitors appeared. In contrast, roaming around the landscape in search of carcasses would be an efficient behaviour for a group of hominins that was large enough to chase away other scavengers. Another important issue demonstrated in the experiments was the existence of an optimal group size for the foraging band (13 individuals in our simulations). The energetic cost of the scavenging activity increases with group size when the group is larger than the minimum size necessary to chase away all competitors and predators. This is because a group that is too large is not satiated by a single carcass and should expend energy in search of additional resources. Thus, the less productive the ecosystem and the scarcer the carcasses, the more energy-intensive this strategy is for a large group. However, it is important to note that the results of our simulations should not be interpreted as estimates of the viable population density of hominins or the optimum group size. The values obtained for these response variables are dependent on the values arbitrarily assigned to parameters such as the group size necessary to chase away giant hyenas and predators or the carrion waste rate. The results suggest the existence of an optimum group size but do not provide an estimate of it. In the real world, this optimum would be determined by the strength necessary to chase away competitors and by the size and nutrient content of the carcasses. The positive effect of foraging in a group with size close to the optimum is larger, and the encounter rate with competitors and predators is higher. Thus, foraging in a group of size close to the optimum is more beneficial in highly productive ecosystems, where the density of carnivores and the encounter rate are higher.
Moreover, scavenging large carcasses in competition with other carrion eaters may have led hominins to coordinate their movements, group cohesion, defence, cooperation, and communication. A relationship between scavenging and language emergence was proposed47. It has been suggested that cooperative behaviour also allowed rapid processing and disarticulation of large carcasses with stone tools to minimise the time spent at the kill site and reduce the encounter rate with carnivores19,48, but this behaviour was not included in our simulations. Direct competition between scavengers, in our case Homo and Pachycrocuta brevirostris, could favour grouping. A certain number of hominins banding together, even brandishing sticks or stones, and shouting could chase out larger predators from their preys17,49. Indeed, archaeological evidence from Fuente Nueva-350 and Dmanisi51 suggests that cobbles and limestone blocks could be used as throwing stones to drive away predators and competitors, reducing the risk of the confrontation52. The results showed that maintaining an optimum group size can be an important factor for success in the competition for carrion in the form of interference competition53. Therefore, an optimum group size protects against predation 45 and improves scavenging efficiency.
SCAVCOMP-ABM54 simulated the trophic behaviour of hominins without using a central place-foraging model55,56,57,58. This is an important difference from other computer simulations of hominin foraging strategies, including simulations of scavenging activities59,60. In the HOMINIDS (Hungry Omnivores Moving, Interacting, and Nesting in Independent Decision-making Simulations) model59, hominin agents leave their nests in the morning and roam individually to search for food. If an agent finds an abandoned carcass, it feeds on it; however, if there are other scavengers on the spot, the hominin calls for help and waits until more hominins arrive to chase away competitors and feed on the spot. Szilágyi et al.60 developed an ELBA model and simulated confrontational scavenging to test a hypothesis regarding the emergence of language. Since carnivores are not included in the ELBA model60, it closely simulates passive scavenging rather than confrontational scavenging. In the ELBA model, hominins forage during the day and return to a campsite at night, where they share food and information regarding the location of the carcasses. Moreover, in the ELBA model, group size had no influence on the ability of hominins to access a carcass but did influence their capability to transport the carcass to the campsite. In contrast, in SCAVCOMP-ABM54, hominins live in small bands that move from one resource patch to another and remain in the patch until the resources (carrion) are depleted; this type of mobility is better described as an optimal patch-use strategy61. Similarly, a strategy without a central place or reference site and provisioning in a fission–fusion social model is common among non-human primates, such as chimpanzees and baboons62,63,64,65. Although a central place strategy is usually assumed for coeval hominin populations in Africa56, assuming a different behaviour for the European hominins during the Epivillafranchian does not conflict with the archaeological records. Most early Pleistocene sites from Iberia are interpreted as marginal occupations by hominins, as Fuente Nueva-332,39 Barranco León D2, Vallparadís EVT766,67, or Barranc de la Boella sites68,69, or as low intensity occupations as Sima del Elefante TE970. Most of these sites are open-air localities usually associated with floodplains or riparian environments and are interpreted as foraging sites. Only the Atapuerca TD6.2 assemblage has been interpreted as a home base intensively occupied by hominins over long periods of time71,72 and might thus be evidence of a central place foraging strategy. However, TD6.2, which has been dated to approximately 0.8 Ma73, has a faunal assemblage characterised by the absence of both P. brevirostris and Megantereon and the presence of Crocuta crocuta74. Thus, Atapuerca TD6.2, which corresponds to the time after the extinction of Megantereon and the replacement of Pachycrocuta brevirostris by C. crocuta, is younger than that considered here and with an entirely different ecological scenario.
The quantitative estimates of carrion production support that sabre-toothed felids created a niche for scavengers by abandoning carcasses with a high nutrient content. In this scenario, scavenging was a reliable food procurement strategy for early hominins in southern Europe, as they foraged in groups strong enough to chase giant hyenas away from the carcasses. This suggests that the differentiation between passive scavenging and kleptoparasitism is limited in the presence of a strong competitor. However, group size had to be moderate in order to maximize the energetic efficiency of the activity. Scavenging does not require advanced technology only group cohesion and cooperation and was likely an important source of meat and fat for Homo sp. in Europe, especially in winter when plant resources were scarce.
Energy expenditure of scavengers. The results of the experiments are shown in relation to the size of the hominin groups. Three experiments were performed for each scenario by varying the densities of predators from low density (red line) to medium density (blue line) to high density (green line). The limits of the boxes correspond to the first and third quartiles; the median is shown by a horizontal line. The whiskers mark the maximum and minimum without outliers and extreme values. Outliers and extreme values are indicated with a white dot and an asterisk, respectively.
Discussion
Scavenging is a fundamental factor in the structure of carnivorous communities in terrestrial ecosystems37. Moreover, the role of scavenging in the evolution and expansion of early hominins is a frequently debated and controversial issue19,20,22. The simulation experiments suggest that passive scavenging could be a very successful strategy for late-early Pleistocene hominins in Europe, even in competition with giant hyenas. Only when hominins foraged in very small groups, the ecosystem productivity was low, and the population densities of Megantereon and Homotherium were low or moderate, giant hyenas displaced the hominins. However, our simulations considered scavenging a unique procurement strategy for hominins, and this is an entirely unrealistic assumption. The hominins may be assumed to exhibit flexible omnivorous behaviour and are capable of adopting their diet by exploiting different plant and animal resources, including carrion, according to their availability6,8,38,39.
A requisite for the coexistence of two large scavengers, hyenas and hominins, is the availability of sufficient carcasses containing large amounts of edible resources. It has been suggested that these resources existed in Early Pleistocene Europe, owing to the presence of two sabre-tooths, especially Megantereon29,35. The estimates of the number of edible resources on the carcasses of large ungulates abandoned by the two sabre-toothed species support the interpretation of sabre-tooths as significant carrion providers. If Megantereon killed one prey every week, based on a conservative estimate, only one-third of the edible energy in the carcass would be consumed before killing a new prey (Table 2). This estimate supports the claims linking the extinction of the giant hyena in Europe to the extinction of Megantereon29,30. Interestingly, although this argument is usually applied only to Megantereon, our estimations suggest that Homotherium also produces carcasses with similar amounts of edible resources. In contrast, the resources contained in the carcasses of prey killed by the European jaguar would be markedly lower (Table 2) and similar to the average caloric content of the carcasses abandoned by recent large predators40. However, it should be acknowledged that the role of Homotherium as a producer of carcasses with high nutrient content relies on the assumption that it was a solitary species. If Homotherium was a social felid, as sometimes suggested41, a pack would be able to consume a large proportion of the carcass before abandoning it. Indeed, according to the estimates in Table 2, a pack of five Homotherium individuals would require approximately 45,000 kcal/day and consume the entire carcass of a 400 kg ungulate every 3–4 days. In such cases, only some portions, such as the brain and bone marrow, remain in the carcass because of the sabre-tooth’s inability to break bones41.
Our simulations modelled Pachycrocuta brevirostris as a solitary passive scavenger; however, this decision may be controversial because it has been proposed that P. brevirostris occupied a niche similar to that of extant spotted hyenas (Crocuta crocuta), which are highly active hunters and kleptoparasites29. However, the taphonomic study of the bone assemblage preserved at Venta Micena27,30,42 together with the morphofunctional analyses of the mandibles and teeth of Pachycrocuta from several European localities30, strongly suggests that the giant hyena was a dedicated strict scavenger or specialised kleptoparasite that stole the prey of sabre-tooths and other large carnivores. A possible argument against considering Pachycrocuta a passive scavenger30 is that carrion eaters must range over large areas in search of food, a task to which the large and non-cursorial giant hyena is not especially adapted. Based on this argument, giant hyenas did not prospect the environment in search of carrion but pursued other predators and stole their preys30. Thus, giant hyenas were kleptoparasites rather than passive scavengers. In this regard, their behaviour would be similar to that of recent spotted hyenas, as suggested by Turner and Antón29. Nevertheless, the simulation experiments suggest that if the carrion is sufficiently abundant, high mobility is not required for a passive scavenger. The walking speed of P. brevirostris was set at 5 km/h (the same as that of the hominins), and it was assigned a high energy expenditure during movement. Moreover, if giant hyenas were kleptoparasites, they would have frequent primary access to carcasses, and the bone accumulation generated by giant hyenas would be difficult to differentiate from that generated by hunting carnivores.
The social behaviour of giant hyenas is another potentially controversial topic. Turner and Antón29 suggested that giant hyenas were social, which allowed them to confront large predators and steal their prey. In contrast, the Venta Micena assemblage showed that the giant hyenas selectively transported certain parts of the carcass to their dens42. This behaviour supports the interpretation of solitary social behaviour because recent spotted hyenas transport all anatomical elements of the carcass to their den when scavenging in groups, but only selected parts when scavenging alone42. Moreover, the social behaviour of recent spotted hyenas is related to the expansion of the frontal region of the brain, a trait recently acquired in the Crocuta lineage43. Therefore, sociality may be a unique and recent acquisition in spotted hyenas.
Scavenging is a widespread behaviour among medium-sized carnivores in recent terrestrial ecosystems40, which is also practised by contemporary hunter-gatherers. Hadza obtained 20% of their meat through confrontational scavenging17,23. However, the consumption of carrion represents a “windfall” resource for Hadza foragers and not a regular activity due to some shortcomings, such as seasonal variations in encounter rates and the size and completeness of carcasses44. Wild chimpanzees also scavenge, but rarely. Anecdotal evidence of scavenging by chimpanzees has been reported from Gombe, Mahale, Taï, and Ngogo21,45. Confronting large carnivores is risky, but chimpanzees reduce this risk by increasing the number of participants and shouting and throwing stones to intimidate leopards. Scavenging, even passive scavenging, is risky. Indeed, the “fatal attraction” hypothesis46 proposes that carcass sites amplify the suppression effect of large carnivores on medium-sized carnivores. Despite being a widespread behaviour, scavenging has only been presented as a successful strategy for early hominins in the short term33. In contrast, the simulations show that scavenging could be an efficient and adaptive behaviour for the Epivillafranchian under certain conditions.
The results of the simulation experiments highlight the importance of group size for the viability of scavenging when competition is considered. Indeed, it can be argued that defending or stealing a carcass from other scavengers, as simulated in our experiments, does not differ from stealing a carcass from a predator. Interestingly, our results showed that when the group size of hominins was not sufficient to chase away their competitors, the hominins survived until the end of the simulation only when carcasses were abundant because of the high density of predators in a highly productive ecosystem (Fig. 1). This suggests that a fully passive scavenging strategy without direct confrontation with competitors would be energetically inefficient as a regular strategy (Fig. 2), although it could still be viable on an opportunistic basis. Hominins foraging alone or in very small groups could not rely on the active search for carrion as the main food resource, although they could feed on an abandoned carcass, which was found as a stroke of luck when foraging on other resources, until competitors appeared. In contrast, roaming around the landscape in search of carcasses would be an efficient behaviour for a group of hominins that was large enough to chase away other scavengers. Another important issue demonstrated in the experiments was the existence of an optimal group size for the foraging band (13 individuals in our simulations). The energetic cost of the scavenging activity increases with group size when the group is larger than the minimum size necessary to chase away all competitors and predators. This is because a group that is too large is not satiated by a single carcass and should expend energy in search of additional resources. Thus, the less productive the ecosystem and the scarcer the carcasses, the more energy-intensive this strategy is for a large group. However, it is important to note that the results of our simulations should not be interpreted as estimates of the viable population density of hominins or the optimum group size. The values obtained for these response variables are dependent on the values arbitrarily assigned to parameters such as the group size necessary to chase away giant hyenas and predators or the carrion waste rate. The results suggest the existence of an optimum group size but do not provide an estimate of it. In the real world, this optimum would be determined by the strength necessary to chase away competitors and by the size and nutrient content of the carcasses. The positive effect of foraging in a group with size close to the optimum is larger, and the encounter rate with competitors and predators is higher. Thus, foraging in a group of size close to the optimum is more beneficial in highly productive ecosystems, where the density of carnivores and the encounter rate are higher.
Moreover, scavenging large carcasses in competition with other carrion eaters may have led hominins to coordinate their movements, group cohesion, defence, cooperation, and communication. A relationship between scavenging and language emergence was proposed47. It has been suggested that cooperative behaviour also allowed rapid processing and disarticulation of large carcasses with stone tools to minimise the time spent at the kill site and reduce the encounter rate with carnivores19,48, but this behaviour was not included in our simulations. Direct competition between scavengers, in our case Homo and Pachycrocuta brevirostris, could favour grouping. A certain number of hominins banding together, even brandishing sticks or stones, and shouting could chase out larger predators from their preys17,49. Indeed, archaeological evidence from Fuente Nueva-350 and Dmanisi51 suggests that cobbles and limestone blocks could be used as throwing stones to drive away predators and competitors, reducing the risk of the confrontation52. The results showed that maintaining an optimum group size can be an important factor for success in the competition for carrion in the form of interference competition53. Therefore, an optimum group size protects against predation 45 and improves scavenging efficiency.
SCAVCOMP-ABM54 simulated the trophic behaviour of hominins without using a central place-foraging model55,56,57,58. This is an important difference from other computer simulations of hominin foraging strategies, including simulations of scavenging activities59,60. In the HOMINIDS (Hungry Omnivores Moving, Interacting, and Nesting in Independent Decision-making Simulations) model59, hominin agents leave their nests in the morning and roam individually to search for food. If an agent finds an abandoned carcass, it feeds on it; however, if there are other scavengers on the spot, the hominin calls for help and waits until more hominins arrive to chase away competitors and feed on the spot. Szilágyi et al.60 developed an ELBA model and simulated confrontational scavenging to test a hypothesis regarding the emergence of language. Since carnivores are not included in the ELBA model60, it closely simulates passive scavenging rather than confrontational scavenging. In the ELBA model, hominins forage during the day and return to a campsite at night, where they share food and information regarding the location of the carcasses. Moreover, in the ELBA model, group size had no influence on the ability of hominins to access a carcass but did influence their capability to transport the carcass to the campsite. In contrast, in SCAVCOMP-ABM54, hominins live in small bands that move from one resource patch to another and remain in the patch until the resources (carrion) are depleted; this type of mobility is better described as an optimal patch-use strategy61. Similarly, a strategy without a central place or reference site and provisioning in a fission–fusion social model is common among non-human primates, such as chimpanzees and baboons62,63,64,65. Although a central place strategy is usually assumed for coeval hominin populations in Africa56, assuming a different behaviour for the European hominins during the Epivillafranchian does not conflict with the archaeological records. Most early Pleistocene sites from Iberia are interpreted as marginal occupations by hominins, as Fuente Nueva-332,39 Barranco León D2, Vallparadís EVT766,67, or Barranc de la Boella sites68,69, or as low intensity occupations as Sima del Elefante TE970. Most of these sites are open-air localities usually associated with floodplains or riparian environments and are interpreted as foraging sites. Only the Atapuerca TD6.2 assemblage has been interpreted as a home base intensively occupied by hominins over long periods of time71,72 and might thus be evidence of a central place foraging strategy. However, TD6.2, which has been dated to approximately 0.8 Ma73, has a faunal assemblage characterised by the absence of both P. brevirostris and Megantereon and the presence of Crocuta crocuta74. Thus, Atapuerca TD6.2, which corresponds to the time after the extinction of Megantereon and the replacement of Pachycrocuta brevirostris by C. crocuta, is younger than that considered here and with an entirely different ecological scenario.
The quantitative estimates of carrion production support that sabre-toothed felids created a niche for scavengers by abandoning carcasses with a high nutrient content. In this scenario, scavenging was a reliable food procurement strategy for early hominins in southern Europe, as they foraged in groups strong enough to chase giant hyenas away from the carcasses. This suggests that the differentiation between passive scavenging and kleptoparasitism is limited in the presence of a strong competitor. However, group size had to be moderate in order to maximize the energetic efficiency of the activity. Scavenging does not require advanced technology only group cohesion and cooperation and was likely an important source of meat and fat for Homo sp. in Europe, especially in winter when plant resources were scarce.
