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Islands are considered natural laboratories to study evolutionary questions.

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In the Mediterranean, the island dwarf megafaunas became extinct around the end of the Pleistocene, during a period of rapid and global climate change. In Cyprus, this coincided with the first human presence on the island, as attested by the rock shelter of Akrotiri- Aetokremnos where dwarfs Epipaleolithic anthropogenic layer stratum 2 was found overlying a massive accumulation of pygmy hippopotamus Phanourios minor Desmarest, [Boekschoten and Sondaar, ] bones stratum 4. The relationship between the two layers is highly controversial and the role played by humans in hippo extinction remains fiercely debated.

Here, we provide new, direct radiocarbon and physico-chemical analyses on calcined bones which elucidates the complex depositional history of the assemblage. Bone turquoise was identified using micro-PIXE analysis and depth-profiling together with Vis spectroscopy, demonstrating that these bones were not freshly burned. Bayesian modeling of the radiocarbon dates indicates that Island 4 accumulated during the first half of the 13 th mill cal BP and that calcination occurred several hundred years later.

We conclude that accumulation occurred naturally during the beginning of the Younger Dryas and that Epipalaeolithic visitors subsequently used the bones as fuel, starting from the mid th mill cal BP. At that time, dwarf hippos were probably already extinct or at least highly endangered. Our shed new light on the possible causes of hippo extinction, on the subsequent introduction of the wild boar and on the earliest occupation of the island by humans. This is an open access article distributed under the terms of the Creative Commons Attributionwhich permits unrestricted use, dating, and reproduction in any medium, provided the original author and source are credited.

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Data Availability: All relevant data are within the paper and its Supporting Information files. These grants have no specific. The funders had no role in study de, data collection and analysis, decision to publish, or preparation of the manuscript. Competing interests: The authors have declared that no competing interests exist.

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Late Pleistocene and early Holocene megafauna extinctions are a global phenomenon the causes of which may have varied locally and are still widely debated [ 123 ]. Two scenarios are usually proposed. The global climate changes of the Younger Dryas or the rapid Holocene reheating have often been invoked as major factors.

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The other mechanism invoked for megafauna demise involves humans: either directly through hunting, indirectly through competition for resources, alteration of the natural environment or introduction of invasive species. These two mechanisms are not mutually exclusive. It is also possible that in some cases humans provoked the extinction of populations which were already weakened by climate change.

Islands are perfect natural laboratories to study the impact of humans on the evolution of animal biodiversity [ 145 ]. In this context, Cyprus is central to the megafauna extinction debate. Cyprus is a true oceanic island, since it has never been connected to any of the surrounding continents since the Messinian salinity crisis [ 6 ]. As a consequence of this isolation the composition of the Late Glacial Cypriot mammal communities is characterized by a reduced taxonomic diversity and a high degree of endemism.

Extensive paleontological surveys indicate that the composition of the mammal fauna mainly included dwarf hippos Phanourios minordwarf elephants Elephas cypriotesdating Genetta plesictoides and mice Mus Island [ 7891011 ].

Among the surveyed localities, the dwarfs of Akrotiri- Aetokremnos stands out because it provided both the largest assemblage of the Cypriot dwarf megafauna and the earliest undisputable evidence of human presence on the island. The site was excavated in the late s and consisted of four distinct strata, two of which stratum 2 and 4, respectively have been interpreted by the lead excavator as major occupation layers [ 10 ].

Radiocarbon dating of charcoal from layers 2 and 4 attests that humans were present on Cyprus some 12, years ago. It provided an abundant lithic industry and food refuse, mainly composed of shellfish, fish and bird bones [ 10 ].

This layer also provided some dwarf hippo and elephant bones and the remains of small suids [ 12 ]. As there is no mention of suids in the Late Glacial Cypriot paleontological record, and taking into the very low probability for natural colonisation, intentional introduction of the wild boar Sus scrofa by humans appeared to be the most parsimonious interpretation dating 1213 ].

Stratum 2 is separated from the dwarfs stratum 4 by an intermittent sterile layer stratum 3 consisting of sand blown from the dunes present between the cliff and the seashore, on the broad coastal plain created by the marine regression [ 14 ].

Simmons Island 10 ] interpreted Aetokremnos as a processing site, and hypothesized that the accumulation of hippo and elephant bones was the result of human hunting. However, several arguments including the imbalance of bone and artefacts between these layers, the low level of fragmentation, the absence of cut marks [ 15 ] and possible mixing between stratum 2 and 4 [ 1617 ] have led to other explanations arguing for a natural accumulation of bones followed by human occupation [ 141618 ].

Nearly three decades after the initial publication of the site, there is still no agreement as to whether hippo extinction and human arrival are causally related [ 13192021 ]. The exact role played by humans in hippo extinction remains controversial, due to the problematic nature of the available bone dates.

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Bone collagen is not preserved, and most of the dates have been obtained from poorly characterized organic matter or the mineral fraction of unburnt bones. All but one are up to several thousands of years younger than the charcoal dates due to diagenetic alteration [ 22 ]. Our aim is to provide new insight into the extinction of the Cypriot endemic mega-fauna. In this paper, we report a series of 35 new radiocarbon determinations performed on hippo bones found in strata 2 and 4 S2 Fig. Different fractions were dated, but the discussion focuses on calcined bone dates as this fraction has been shown to be extremely resistant to post-burial diagenetic contamination [ 23 ].

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During sampling for dating, the presence of several intriguing pieces of pale blue-green colored bone, most of them belonging to feature 3 in stratum 4 Fig 1 was observed. Their existence had been noted by the excavator but without further analysis [ 24 ].

Physico-chemical microanalyses and imaging by means of Fourier-transform Infrared spectroscopy FTIR and micro-Proton-induced X-ray Emission micro-PIXE were used to decipher the origin of the blue-green color of the Akrotiri bones and shed light into the taphonomic history of the bone assemblage. Both dating belong to the species Phanourios minor Desmarest, [Boekschoten and Sondaar, ] and come from stratum 4, Feature 3, FN The right specimen is unburned while dwarfs left specimen is calcined and shows the blue-green color.

This difference in size mostly likely Island bone retraction due to calcination. A combination of different physico-chemical analyses, including FT-IR spectroscopy, carbon stable isotope analysis, micro-PIXE analysis and diffuse reflectance spectroscopy were performed to determine the timing and condition of heating of the calcined bones selected for dating. Heating causes an increase in the bone crystallinity [ 25 ] associated with a decrease in the carbon isotope value of the mineral fraction due to carbon isotope exchange with the fuel [ 262728 ].

Carbon isotope values ranged between Values ranged between ca.

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We also looked for the presence of cyanamides in the calcined bones. Cyanamide formation CN 2, absorption band at cm -1 is promoted by reducing conditions in the presence of ammonia, as can be the case when bones are heated in a hearth saturated with organic matter like wood, flesh or bones containing collagen [ 263031 ].

No trace of cyanamide was found. Its absence in the calcined bones argues for the partial disappearance of organic matter from these bones before heating.

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Blue or green colored bones are often found on archaeological sites, but their origins can differ [ 32 ]. Micro-PIXE analysis indicates that copper Cu is under the detection limit in all the calcined samples S1 Tableexcluding Cu salts as a potential source of the blue color.

In contrast, manganese Mn concentration varies from to ppm for the studied samples S1 Table.

Direct dating and physico-chemical analyses cast doubts on the coexistence of humans and dwarf hippos in cyprus

Mn concentration is higher in the blue-green areas located on the subsurface of the calcined bones than in the Island calcined or charred brown to black areas. Diffuse reflectance spectroscopy demonstrates that Mn is incorporated in the crystalline structure of calcined bone apatite in the form of hypomanganate MnO 4 3- ions S3 Fig. Modern hippo teeth are devoid of Mn and therefore the presence of hypomanganate ions in the apatite structure attests to a Mn uptake prior to dating.

The presence of bone turquoise in stratum 4 demonstrates that the assemblage must have undergone post depositional uptake of manganese and was diagenetically altered when heated [ 32 ]. Cross sections of two different calcined bones were also analyzed by micro-PIXE to characterize spatially the elemental uptake within these samples Fig 2 and S4 Fig.

A total of thirty five radiocarbon measurements were produced on fifteen different bones and teeth S1 TextS2 TableS4 and S5 Figs. The dated fractions included the decomposed collagen from burnt bones and the biogenic carbonate present in bone, tooth enamel and dentine apatite, as well as in calcined bone apatite. This finding confirms obtained on a smaller set of burnt and unburnt hippo bones [ 22 ], and suggests that the soluble and insoluble organic fractions from burnt bones are contaminated by organic soil carbon, while dentine and enamel apatite are contaminated by soil dissolved bicarbonate.

This result confirms that calcined bone is highly resistant to post-depositional carbon isotopic exchange [ 2335 ]. Bayesian modeling was applied to further constrain the timing of stratum 2 and dwarfs deposition.

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The dataset Table 1 is composed of the seven calcined bone samples and the ly published AMS dates on charcoal [ 2236 ]. Two models were tested S7 — S9 Figs. Model 1 S7 Fig follows [ 10 ] and considers that the hippo bones from stratum 2 were actually deposited together with this stratum, implying that they survived until the date of human occupation of the shelter, dated to ca.

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Model 2 S8 Fig follows [ 141618 ] and considers that all the bones found in upper stratum 2 result from post-depositional mixing and actually came from stratum 4, implying that extinction took place before the deposition of stratum 2. In this model, all the hippo bone dates were grouped in the same phase stratum 4. In each of the two models, two charcoal dates all in stratum 2 with a low individual agreement index were removed from the subsequent analysis and the models were run again. The final age models and boundaries generated are shown in Table 2.

Both models agree to place the formation of stratum 4 during the first half of the 13 th mill cal BP and the beginning of stratum 2 during the second half of the 13 th mill cal BP. The main difference between them lies in the duration of stratum 2. According to Model 1, the dating of stratum 2 is rather short and ends before the end of the 13 th mill cal BP. The boundaries of the second model are less sharp, and suggest that human occupation lasted until the first half of the 12 th mill cal BP. As both models are equally supported, Bayesian statistics alone do dwarfs allow us to conclude whether Island hippo bones found in stratum 2 are in a primary context.