CORRESPONDENCE Early Holocene Survival of Megafauna in South America

Journal of Biogeography (J. Biogeogr.) (2007) 34, 1642–1646

CORRESPONDENCE

Early Holocene survival of World was concomitant with, and a megafauna, albeit two of these ages are megafauna in South America consequence of, the human occupation of potentially unreliable, and four were the Americas. Their argument is two- obtained from one single specimen (indeed, fold. First, the radiocarbon dates (14C) one of the unreliable dates comes from this Comments on Steadman, D.W., Martin, P.S., accepted by them for the last appearance specimen; Table 1). Other reports not MacPhee, R.D.E., Jull, A.J.T., McDonald, dates (LADs) of these animals roughly cor- included in Barnosky et al. (2004) provide H.G., Woods, C.A., Iturralde-Vinent, M. & respond to megafaunal extinction dates in two direct radiocarbon ages of megafa- Hodgins, G.W.L. (2005) Asynchronous ex- South and North America and the West unal bone remains from central Brazil at tinction of late Quaternary sloths on con- Indies. These dates coincide with the human the Pleistocene⁄Holocene boundary tinents and islands. Proceedings of the colonization of these regions and they argue (Table 1; Neves & Pilo´ , 2003; Araujo National Academy of Sciences USA, 102, that this supports the thesis that human et al., 2004). Politis et al. (2004; also not 11763–11768. arrival caused extinction of the ground included in Barnosky et al., 2004) presen- sloth. Second, according to Steadman et al., ted two additional Holocene direct The debate over the causes of the Pleisto- extinctions caused by climatic fluctuation radiocarbon ages of Megatherium ameri- cene megafaunal extinction dates back to would result in concomitant LADs across canum (Blumenbach) specimens (Table 1) the early 19th century (Grayson, 1984), the entire continent and associated islands, and a third one from the Holocene⁄Pleis- 14 and continues to generate considerable as they viewed these fluctuations as being tocene boundary (10,190 Æ 120 CyrBP; controversy (e.g. Grayson & Meltzer, widespread and uniform, whilst they found c. 11,820–12,020 cal. BP; Table 1), all in 2003; Araujo et al., 2004; De Vivo & that the LADs for the West Indies, around Argentina; and Marshall et al. (1984; also 14 Carmignotto, 2004; Fiedel & Haynes, 4400 CyrBP [c. 4800–5050 calibrated not included in Barnosky et al., 2004) 2004; Burney & Flannery, 2005; Wroe years before present (cal. BP); dates calib- reported a single Holocene age of 14 et al., 2006). Typically, protagonists in rated with CALIB 5.0, Stuiver et al., 2005], 8910 Æ 200 CyrBP (c. 9780–10,150 cal. this debate can be classified into two are much younger than those found in the BP; GIF-4116) of a Scelidodon chiliensis 14 groups. One group argues that Late continent (c. 11,000 CyrBP; c. 12,880– (Lydekker) in Peru (Marshall et al., 1984; Pleistocene megafaunal extinctions were 12,950 cal. BP for North America and Pujos & Salas, 2004). 14 primarily caused by direct and indirect c. 10,500 CyrBP; c. 12,390–12,640 cal. BP Four of the sites where these dates were human action through hunting, habitat for South America). obtained are located in Argentina, while two modification or introduction of new We contend that the chronological data are located in central Brazil and the last in predators (Burney & Flannery, 2005, presented by Steadman et al. (2005) are Peru (Fig. 1). All the Argentinean sites 2006; Barnosky et al., 2004; Fiedel & incomplete, especially when considering (Arroyo Seco 2, La Moderna, Campo Haynes, 2004). The other interpretation South America. While Steadman et al. Laborde and Paso Otero 5) are open-air is that humans had at most a minor role (2005) suggest that there are no accept- archaeological sites, i.e. the megafaunal in the megafaunal extinction, and that the able Holocene LADs for ground sloths, a remains are associated with prehistoric loss was attributable principally to a cli- large number of Holocene dates gener- human occupations (see Borrero et al., matic cause (Ficcarelli et al., 2003; Gray- ated through direct dating of bone and 1998; Politis et al., 2004 for detailed son & Meltzer, 2003, 2004; Barnosky dung remains are indeed available in the descriptions). Arroyo Seco 2 is inter- et al., 2004; De Vivo & Carmignotto, literature. Barnosky et al. (2004; sup- preted as a base camp where a large 2004; Boeskorov, 2006; Guthrie, 2006; porting material) revised the radiocarbon variety of activities were undertaken Wroe et al., 2006; Wroe & Field, 2006). dates available for megafaunal remains (Politis et al., 2004), including the Here we contest the position of Stead- throughout the world. In South America, exploitation of ground sloths and other man et al. (2005), who favour the overkill they listed four articles with remains of megafauna by humans. However, Borr- hypothesis to explain the ground sloth megafauna dated within the Holocene, ero et al. (1998) and Politis et al. (2004) extinction in the Americas. Although based both on direct and indirect dates. do not state clearly if the two specimens making an important contribution to the Even when considering only the results (M. americanum and Equus neogeus Lund) debate on extinction of the New World based on direct dates of bone remains, that dated to the Holocene (Table 1) megafauna, Steadman et al. (2005) make sufficient evidence still supports Holocene showed marks of human manipulation. some important assumptions in their LADs for subequatorial ground sloths. The remaining open-air sites are believed analysis. For instance, from Argentina, Borrero to be sites used for specific activities Steadman et al. (2005) argue that the et al. (1998) presented a total of seven 14C (Politis et al., 2004): La Moderna is extinction of ground sloths in the New dates consistent with a Holocene survival of interpreted as an occasional megafaunal

1642 www.blackwellpublishing.com/jbi ª 2007 The Authors doi:10.1111/j.1365-2699.2007.01744.x Journal compilation ª 2007 Blackwell Publishing Ltd Correspondence

processing site, where the remains of a single glyptodont (Doedicurus clavicauda- (1984) (2003) (2003) (1998) (1998) (1998) (1998) (1998) (1998) (1998) tus Owen) dated to the Holocene (Table 1) (2004) ´ ´ (2004) (2004) (2004) (1998) were recovered; Campo Laborde presents et al. et al. et al. et al. et al. et al. et al. et al. evidence that it was used as a hunting and et al. et al. et al. et al. et al. processing site for ground sloths (M. americanum; Table 1); and Paso Otero 5, was also identiﬁed as a hunting and processing site for local megafauna. The two Brazilian sites, in contrast, are exclusively palaeontological, i.e. they are not associated with human occupations, and are located in limestone caves in the karstic region of Lagoa Santa. Gruta Cuvieri is a cave where three vertical chambers func- tioned as natural traps for the now extinct megafauna and other animals. The only

) Technique References megafauna species found so far is Catonyx BP . 9740–10,150 AMS Borrero . 9780–10,150 ? Marshall . 8420–8540 AMS Politis . 9290–9440 Standart Borrero . 9920–10,190 ? Garcia (2003) . 8020–8160 AMS Borrero . 7330–7470 Standart Borrero . 7700–7840 AMS Borrero . 8200–8340 AMS Borrero . 8180–8320 AMS Borrero . 8780–9010 AMS Politis cuvieri (Lund), a medium-sized ground c c c c c c c c c c c . 11,320–11,600 AMS Neves & Pilo . 10,680–10,860. 11,820–12,020 Standart AMS Long Politis . 13,980–14,140 AMS Politis c c c c Two sigma calibration (cal. sloth. The Holocene date presented in Table 1 was obtained from one of these ground sloths, found at the surface of one à

of the chambers. The other Brazilian site, ) 120 150 c. 10,260–10,480 AMS Neves & Pilo 40 90 200 250 240 90 50* 90 160 100 370 80 200 170* BP Escrivaˆnia 5, is part of a complex of Æ Æ Æ Æ Æ Æ Æ Æ Æ Æ Æ Æ Æ Æ Æ Æ caves, generically referred to as Escrivaˆ- nia, representing one of the richest palaeontological limestone outcrops known at Lagoa Santa. Together with tons of animal fossil bones, in one of the chambers (Escrivaˆnia 3) an almost complete human skeleton was also recently recov- 14 ered, dated to 7650 Æ 80 CyrBP (2004) due to the difference observed between the dates obtained.

Laboratory number Age (yr (c. 8370–8420 cal. BP; Beta 174734). The Peruvian site, Pampa de los Fo´siles, is et al. also a palaeontological site located in the Cupisnique Desert. Several archaeological sites in the region have revealed no evidence of human interaction with the megafauna in the region (Pujos & Salas, 2004). In addition to these reported dates, Steadman et al. (2005; supporting mater- siles Peru GIF-4116 8910 ´ ial) disqualiﬁed two other Holocene dates as unreliable (they also rejected a third date, but it has a very large margin of nia 5 Brazil BETA-174722 9260 ˆ error). These were the only Holocene dates found in their bibliographical revi- (1998). sion and they Ôhave means that are up to 1000 years younger than means of any [of et al. the accepted LADs] [Supplementary online material]Õ. As 10 reliable Holocene direct BoneBone Gruta Cuvieri Arroyo Seco 2 Brazil Argentina TO-1504 BETA-165398 9990 8890 Bone Pampa de los Fo Bone Campo Laborde Argentina AA-55117 7750 Bone Arroyo Seco 2 Argentina LP-53 8390 Bone Arroyo Seco 2 Argentina TO-1506 7320 Bone Arroyo Seco 2 Argentina CAMS-58182 12,200 Bone La Moderna Argentina BETA-7824 6555 Bone La Moderna Argentina TO-1507-1 7010 Bone La Moderna Argentina TO-1507-2 7510 Bone La Moderna Argentina TO-2610 7460 Bone Campo Laborde Argentina AA-55118radiocarbon 8080 dates for megafauna are des- cribed here, there is no further reason to Early Holocene radiocarbon dates obtained for South American megafaunal specimens. ⁄ 14 reject the dates of 8990 Æ 90 CyrBP (c. 9920–10,190 cal. BP; LP-925; Garcia, 14 (Lund) Bone Escriva 2003) and 9560 Æ 90 CyrBP (c. 10,680– 10,860 cal. BP; GrN-5772; Long et al., 1998) as unacceptable outliers. These two

Late Pleistocene dates are from an Argentinean site, Gruta del Indio (Fig. 1; see Long et al., 1998; Garcia, 2003 for detailed descriptions). Dates obtained from oneConsidered single problematic specimen. by Borrero à Table 1 Taxa Sample Site Country *Dates obtained from one single specimen. Considered problematic by Politis Smilodon populator Catonyx cuvieri Equus neogeus Scelidodon chiliensis Megatherium americanum Megatherium americanum Sloth Dung Gruta del Indio Argentina LP-925 8990 Megatherium americanum Sloth Bone Gruta del Indio Argentina GrN-5772 9560 Megafauna Bone Paso Otero 5 Argentina AA-19291 10,190 Megatherium americanum Doedicurus clavicaudatus Doedicurus clavicaudatus Doedicurus clavicaudatus Doedicurus clavicaudatus Megatherium americanum This site is a rockshelter, and although it

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Finally, it must be emphasized that there is a general lack of evidence of sloth remains in archaeological contexts in the Americas as a whole (but see Politis et al., 2004 for an exception), which also speaks against the overkill hypothesis. Specifically, in Lagoa Santa, despite the excavation of dozens of archaeological sites dated to the Pleisto- cene⁄Holocene transition (showing human 14 evidence as old as 11,000–11,500 CyrBP; c. 12,880–13,400 cal. BP; Neves et al., 1999), evidence is lacking of megafaunal use by humans, either as a source of food or raw material (Kipnis, 1998; Prous & Fogaça, 1999). In North America, a similar situation is observed. According to Grayson & Meltzer (2003), there are only two genera of megafauna (Mam- muthus Burnett, 1830 and Mammut Blu- menbach, 1799) known to have been hunted by humans during the Clovis period (Grayson & Meltzer, 2003). This sce- nario is accepted even by Fiedel & Haynes (2004), strong defenders of the overkill hypothesis. Thus, at least in South America (and most probably in North and Central America as well), the idea that ground sloths went extinct due to overkill lacks archaeological support. In conclusion, the ground sloth overkill hypothesis, as defended by Steadman et al. Figure 1 Archaeological and palaeontological sites in South America presenting (2005), is not sufficiently supported in the 14 direct Late Pleistocene⁄Early Holocene radiocarbon ( C) dates for megafaunal remains. empirical world. As we have briefly Circles represent sites with no evidence of human exploitation of the megafaunal remains, pointed out: (1) a considerable number of whereas triangles represent sites with evidence of human exploitation of megafauna. 1, Gruta reliable Holocene dates for megafaunal Cuvieri; 2, Escrivaˆnia 5; 3, Gruta del Indio; 4, La Moderna; 5, Campo Laborde; 6, Arroyo specimens in South America already exist, Seco 2; 7, Paso Otero 5; 8, Pampa de los Fo´siles. including for ground sloths; (2) the existence of late megafaunal LADs in presents chronological information delay observed in the LADs of Central Central America islands can be equally placing humans together with megafauna America islands, when compared with the well explained through overkilling or in time, there is no evidence of humans continental ones, favours the overkill environmental changes; and (3) the gen- exploiting the local megafauna (Long hypothesis. Delayed LADs in insular eral lack of megafaunal killing sites and et al., 1998; Garcia, 2003). regions have been found in other parts megafaunal remains in archaeological As presented in Table 1, from the 14 of the world, independent of human pre- contexts is inconsistent with the overkill existing Holocene dates we found for sence (Guthrie, 2004; Boeskorov, 2006). hypothesis. Nonetheless, it is important to megafaunal remains in South America Boeskorov (2006) showed that in northern emphasize that the amount of informa- eight are derived from ground sloths, Eurasian islands, megafauna survived into tion regarding the presence of megafauna which severely weakens the position of the Holocene, e.g. the mammoths of in archaeological sites is still too small to Steadman et al. (2005), that there are no Wrangel Island. Nonetheless, the extinction be considered as strong evidence against acceptable Holocene LADs for ground of megafauna in Eurasia as a whole is human predation of megafauna, and thus sloths in the Americas. Assuming that believed to be primarily due to climatic this piece of information must be inter- human groups already inhabited South changes (Barnosky et al., 2004; Boeskorov, preted as complementary to the others. 14 America around 12,500 CyrBP 2006), particularly because no human Collectively, the data presented here are (c. 14,300–14,950 cal. BP; Dillehay, 2000), presence is found in the Wrangel Islands more consistent with a model explaining the argument that the ground sloth LADs until well after the extinction of the megafaunal extinction through climatic were concomitant with the human arrival megafauna (Boeskorov, 2006). Although fluctuations, although in South America the in the New World can no longer be these data do not peremptorily disqualify poor chronological contextualization of the accepted, at least not as an immediate SteadmanÕs argument, they do bring into megafaunal decline does not yet allow for a phenomenon. question whether the overkill hypothesis percentage estimate of megafaunal genera The second argument presented by is the most parsimonious explanation for that survived until human arrival. In North Steadman et al. (2005) is that the apparent megafaunal extinctions. America (Grayson & Meltzer, 2002,

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2003) and in Australia (Wroe et al., 2006; 2Instituto de Investigaciones Arqueolo´gicas y zerÕs ÔRequiem for overkillÕ. Journal of Wroe & Field, 2006), this percentage Museo, Universidad Cato´ lica del Norte, Archaeological Science, 31, 121–131. seems to have been small, suggesting that Calle Gustavo LePaige, 380, 141-0000 Garcia, A. (2003) On the coexistence of man the megafaunal extinction was a pro- San Pedro de Atacama Chile and extinct Pleistocene megafauna at tracted process, beginning much earlier Gruta del Indio (Argentina). Radiocarbon, than the human settlement of these con- 45, 33–39. REFERENCES tinents. Such a decline may have been the Grayson, D.K. (1984) Nineteenth-century case in South America, as only a few Araujo, A.G.M., Neves, W.A. & Pilo´, L.B. explanations of Pleistocene extinctions: a megafaunal genera apparently survived (2004) Vegetation changes and megafau- review and analysis. Quaternary extinction (ed. by P.S. Martin and R.G. Klein), pp. until the Holocene. 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BIOSKETCHES

Alex Hubbe is a graduate student at the Laboratory for Human Evolutionary Studies, Instituto de Biocieˆncias, Universidade de Sa˜o Paulo. His main interests are the palaeoecology and extinction of the South America megafauna.

Mark Hubbe is an investigator at the Instituto de Investigaciones Arqueolo´gicas y Museo, Universidad Cato´lica del Norte, Chile. His main research interest is the origin and dispersion of the First Americans.

Walter Neves is the coordinator of the Laboratory for Human Evolutionary Studies, Instituto de Biocieˆncias, Universidade de Sa˜o Paulo. His main research interest is the origins and adaptations of the First Americans.

Editor: Mark Bush

1646 Journal of Biogeography 34, 1642–1646 ª 2007 The Authors. Journal compilation ª 2007 Blackwell Publishing Ltd