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This megafauna is now completely extinct, with the largest surviving endemic vertebrates less than 10 kg in body mass 2. However, the dynamics of the Malagasy faunal extinction process and the nature of human involvement in driving prehistoric biodiversity loss for example, overkill versus population attrition, possibly through indirect processes such as habitat degradation or natural climatic change remain poorly understood due to limited data on human-faunal interactions and the duration of temporal overlap between humans and now-extinct species.

Researchers have sought to understand the process of Holocene biodiversity loss in Madagascar by comparing pre- and post-human eras 2. Archaeological evidence for settled villages dates from years B. Archaeological, genetic, and linguistic data all indicate that these colonists were of both Austronesian and East African heritage 4 — 8. Evidence available in the s to s suggested a first human arrival about years B. However, several lines of evidence have been proposed to suggest a longer period of prehistoric human occupation of Madagascar across the middle to late Holocene.

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These microlithic tools are similar to those used in composite projectiles, and their morphology is consistent with des from southern and eastern Africa. Two proposed examples of human modification of elephant bird bones have both been rejected as evidence of anthropogenic exploitation. An undated, unidentified leg element of Mullerornis sp. Reworked elephant bird eggshell fragments have been reported from archaeological contexts in coastal rock shelters and settlements, but direct radiometric dates on eggshell are substantially older than dates on charcoal predicted by human activity at these sites 6 Here, we present new evidence of prehistoric human modification of multiple elephant bird postcranial elements, representing both currently recognized genera.

We distinguish pathological and taphonomic damage from anthropogenic marks using the empirical classification of Corron et al. Anthropogenic marks described here as clefts or kerfs differ in morphology and orientation from traces resulting from natural processes Clefts and kerfs are consistent with patterns of butchery in ratites through disarticulation, as evidenced by marks at interarticular epiphyses of long bones 35 and phalanges 37associated with hyperextension of limb ts followed by chopping and cutting through connective tissues on their exposed fascia, leaving comparatively few anthropogenic marks on the surfaces of the diaphysis The Christmas River Ilakakabe site Fig.

The bedrock of the region is Permian and Triassic in age and belongs to the Karroo group of the Morondava basin. The bedrock is overlain by recent sediments that include layers of beige sandy soil, black clay, and a highly fossiliferous to m-deep layer of slate gray clay. No lithic tools or other human artifacts or remains have been reported from the single excavation so far conducted at the site. Two skeletal elements from a single Aepyornis maximus individual collected by E. Simons as an articulated pair from the bone bed show perimortem anthropogenic modification Fig.

Bone collagen samples from USNM A were directly dated at two separate AMS radiocarbon facilities, with a combined calibrated date range of 10, to 10, years B. Table 2. Highlighted elements correspond to Figs. Adapted from original drawing by A. Calibrated date years B. Table 2 List of newly recognized elephant bird bones with perimortem anthropogenic modification and associated AMS radiocarbon dates.

A third groove is present on the medial condyle of the central trochlea posterior to the two marksand a fourth groove is present on the medial condyle of the medial trochlea. A fifth is more centrally located on the lateral trochlea. All of these grooves have centrally oriented bevels and v-shaped floors. While the penetrating marks are intact and well defined, the edges are irregular and undefined at their centers, with portions of the bone surface absent. These marks are consistent with kerfs made by single-bladed, sharp lithic tools and multiple cutting actions intended to disarticulate the central phalanges A Distal aspect of A.

Photo credit: V. The diaphysis exhibits two depression fractures, one on the anterior fascia of the proximal surface and another on the lateral portion of the posterior fascia of the distal surface, which may be hobbling impact marks from immobilizing the animal. A large, laterally oriented linear anthropogenic mark is also present on the medial condyle of the distal process, ending in a large undefined fragmentation of the anterior medial portion of the condyle and exposing a rough and uneven trabecular surface. Bevels are oriented centrally with an off-center v-shaped floor biased toward the anterior.

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The mark penetrates through cortical tissue, leaving exposed trabeculae forming both wall aspects. Groove edges are defined at the medial limit, becoming undefined at the center. The groove is rugose with varying relief in posterior aspect, characteristic of perimortem damage caused by a lithic tool 35and is smooth and straight in anterior aspect. The lack of undefined cracking extending away from the central extremity of the mark indicates that this kerf was made upon fresh bone, and the homogeneous coloration of the bone surface and exposed fascia also indicates that it was made before deposition.

A secondary anthropogenic linear groove is present off-center of the medial fascia, oriented toward the missing anterior medial condyle and with similar kerf morphology. The posterior-lateral bevel edge is defined at the anterior-medial end and undefined from the center to the posterior-lateral end. The morphology and orientation of the cleft and kerf are consistent with disarticulation at the intertarsal t, including high-impact chopping actions associated with disarticulation of large animals 35 A Depression fracture on the anterior fascia of the proximal end of A.

B Depression fracture on the lateral aspect of the posterior fascia. D Close-up and profile of cut mark TT-3 on the medial condyle of the distal articular process digital thin section shows the wall and kerf floor of the mark. Additional evidence of ancient Holocene exploitation of elephant birds is also available in historical museum collections from Madagascar that have been reexamined. A Mullerornis sp. Bevels are oriented centrally with a central v-shaped floor.

The distal aspect of the groove is less regular and has more crenellations along the margin than the proximal aspect. This mark is again consistent with a kerf made by a lithic tool, with the orientation and morphology indicative of butchery fig. S2 to S4. Our study therefore reveals a ly unrecognized period of human presence and coexistence with now-extinct fauna on Madagascar, which is now documented through intermittent records of butchery of aepyornithids across almost the entirety of the Holocene.

These findings pose major archaeological and paleontological questions, of crucial importance for understanding early human migrations and Quaternary faunal extinction dynamics. Fundamentally, evidence for long-term coexistence of humans and megafauna in Madagascar demonstrates that a radically different extinction paradigm is required to understand biodiversity loss in this island ecosystem. This discovery of early Holocene evidence of human presence on Madagascar also raises the important question of why, if the island was occupied by prehistoric migrants continually throughout the Holocene, direct archaeological evidence of human settlement predating the late Holocene has not yet been detected.

Archaeological research in Madagascar has largely concentrated on relatively recent open-air village sites and early Holocene sediments have rarely been examined 23 and so it is possible that evidence of older human presence has so far been missed. Alternatively, early-mid Holocene human presence on Madagascar may have been restricted to transient Late Stone Age migration spresumably across the Mozambique Channel, rather than permanent island-wide settlement.

New well-described excavations are required to test between these alternative potential hypotheses for prehistoric human colonization, and provide further insights into human-megafaunal interactions in Late Quaternary Madagascar. Aepyornithid pelvic limb specimens held in museum collections in Europe, United States, and Madagascar were investigated for anthropogenic marks. Length and width measurements of each mark were taken by hand using digital calipers. Length was defined using two points for each mark including origin and termination of the mark, following standards in cut mark morphology at multiple magnifications.

Width is defined as the widest point of modified bone, with termination points at the unmodified bone surface perpendicular to the long axis of the cut mark. When possible, measurements were taken using a Keyence VHX microscope with built-in visualization software, allowing measurements to be taken without molding. Cut mark depth can be measured at the deepest point of the mark directly from the scan. The stitch function creates a three-dimensional composite image from several image planes and overlapping focus levels.

The visualization software then creates a true focus reproduction of the scanned bone surface. When access to the Keyence microscope was not possible, Xantopren L blue putty was used to generate casts of affected areas 41where there would be no possibility of causing further damage. These casts were observed and measured using a Hitachi TM tabletop scanning electron microscope.

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Impact marks were compared to the morphology and position of tool marks ly reported from late Holocene Madagascar 2142modern assessments of meat utility and butchery of emu, archaeological records of tool marks on rhea, and modern frameworks of archaeological exploitation analysis 35 Here, the conservative frameworks of Corron et al. The authors recognized that this framework underestimates butchery practices, as s of exploitation through tool marks are rare due to false-negative or type II errors, where flesh is sufficiently thick that tools do not cut all the way through it.

New AMS radiocarbon dates were obtained by extracting 0. All radiocarbon data used were calibrated using OxCal version 4. Author contributions: J. Figure 2 was adapted from A. Competing interests: The authors declare that they have no competing interests. Additional data related to this paper may be requested from the authors. Supplementary Material Summary Fig.

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