lable at ScienceDirect

Journal of Human Evolution 81 (2015) 83e87

Contents lists avai

Journal of Human Evolution

journal homepage: www.elsevier .com/locate/ jhevol

News and views

Giant subfossil lemur graveyard discovered, submerged,in Madagascar

Alfred L. Rosenberger a, b, *, Laurie R. Godfrey c, Kathleen M. Muldoon d, Gregg F. Gunnell e,Haingoson Andriamialison f, Lovasoa Ranivoharimanana f, Jean Freddy Ranaivoarisoa f,Armand Hubert Rasoamiaramanana f, Jeannot Randrianasy f, Fabio Esteban Amador g

a Department of Anthropology and Archaeology, Brooklyn College, CUNY, 2900 Bedford Avenue, Brooklyn, NY 11210, USAb Brooklyn College: NYCEP (New York Consortium in Evolutionary Primatology), USAc Department of Anthropology, Machmer Hall, 240 Hicks Way, University of Massachusetts, Amherst, MA 01003, USAd Department of Anatomy, Arizona College of Osteopathic Medicine, Midwestern University, 19555 N. 59th Avenue, Glendale, AZ 85308, USAe Division of Fossil Primates, Duke Lemur Center, 1013 Broad Street, Durham, NC 27705, USAf D�epartement de Pal�eontologie et d'Anthropologie Biologique, Facult�e des Sciences, Universit�e d'Antananarivo, BP 906, Ankatso,101 Antananarivo, Madagascarg National Geographic Society, 1145 17St NW, Washington, DC 20036, USA

a r t i c l e i n f o

Article history:Received 15 January 2015Accepted 16 January 2015Available online 6 March 2015

Keywords:MadagascarSubfossil lemursUnderwater paleontologyFlooded caves

In October, 2014, we organized a paleontological expedition toinvestigate flooded freshwater caves in Tsimanampetsotsa NationalPark, Madagascar, located in the arid southwestern region of thecountry where the karst landscape is pocked with dry caves andlarge water-filled sinkholes (Fig. 1). Our team of nine scuba diverswas led by Phillip Lehman of the Dominican Republic SpeleologicalSociety (Supplementary Online Material [SOM] Video 1). The dis-covery of subfossils in Tsimanampetsotsa was made initially byRyan Dart of Antananarivo. The director of Tsimanampetsotsa Na-tional Park, Mr. Lovasoa Dresy, immediately recognized theirimportance to science and encouraged the work reported here.Substantial numbers of subfossil remains were found in threecaves. In Aven Cave we discovered what is likely to be the singlelargest cache of giant subfossil lemurs ever uncovered. The other

* Corresponding author.E-mail address: alfredr@brooklyn.cuny.edu (A.L. Rosenberger).

http://dx.doi.org/10.1016/j.jhevol.2015.01.0040047-2484/© 2015 Elsevier Ltd. All rights reserved.

two fossiliferous caves were Mitoho and Malaza Manga. Subfossilshad been previously reported from around the entrance to MitohoCave (Perrier de la Bathie, 1934; Goodman and Jungers, 2014) butno underwater investigation of remains inside any of these caveshad been conducted prior to this expedition. Thus the primaryobjective was to establish the paleontological potential of thesecaves, with the principal aim of assessing the biodiversity of thesubfossil content of Aven (Fig. 1).

Aven is a karstic dissolution cave or sink hole produced bywaterdraining through the porous limestone shelf. It is a classic verticalsink hole with deep horizontal cave passageways, each ending in acollapse of limestone blocks. In the complex of tunnels and pas-sages, many sections can be accessed only through narrow re-strictions, a challenge that requires advanced cave divingtechniques as a precondition to safe exploration of this dark, un-charted subterranean environment (Fig. 2C). It is readily apparentthat these spaces were dry in the past as there is substantial spe-leothem (stalactite and stalagmite) formation. The full extent ofAven's passageways has yet to be explored, but our team laid about268 m of safety line during the expedition, running at an averagedepth of 42 m.

The opening of the sink hole is some 25 m in circumference, andthe water table is located 10e12 m below the rim. A small island inthe center of the water pool is the very top of a debris cone, what'sleft of the collapsed overhead rock (Fig. 1). The mound falls gentlyinto the depths of the lit cavern to about 25 m, fromwhere the caveextends into the blackness in all directions. It is in this transitionalzone where most of the more visible subfossil remains have beenlocated. During the survey, standard cavemapping techniques wereemployed to locate and mark areas with materials of interest, suchas dense bone accumulations or the location of important speci-mens. It became immediately apparent that there were multiplesites of import and hundreds of cranial and postcranial remains

Figure 1. Locational maps of caves and sketches of the Aven Cave sink hole. (a) Base map of Madagascar with symbol at lower left showing location of Tsimanampetsotsa NationalPark; (b) relative positions and sizes of Aven, Mitoho and Malaza Manga Caves, the last being 1.2 km long; (c) cross sectional sketches of the Aven Cave sink hole (right) and thecavern debris cone (left). Sketch map by Phillip Lehman.

A.L. Rosenberger et al. / Journal of Human Evolution 81 (2015) 83e8784

that deserve close attention. We also employed 3D photographictechniques to document the morphology and in situ context ofspecimens, such as the horned crocodile Voay robustus (SOM Fig. 1).

The geological context, age, speleology and taphonomy of Avenwill be subjects of future studies. Considering the importance of

establishing a stratigraphic chronology, we tested the sediment bypushingmeter-length probes into it at three widely separated areaswhere bones were exposed on the surface. The probes were easilyinserted and met little or no bottom resistance. Furthermore, sincespeleothems would have formed only when the cave was not

Figure 2. High resolution, in situ photographs of Aven subfossils. (a) Pachylemur insignis cranium associated with postcranials; (b) bone concentration with at least three Pachylemurcrania visible; (c) Victoria Alexandrova marking a horned crocodile, Voay robustus; (d) two adult Pachylemur crania (“the twins”). Photos courtesy of Phillip Lehman and PietroDonaggio Bitner.

A.L. Rosenberger et al. / Journal of Human Evolution 81 (2015) 83e87 85

flooded, uranium-series-disequilibrium (230Th/U) dating shouldprovide accurate estimates of the timing of the flooding episode orepisodes (Richards and Dorale, 2003), and stable oxygen and car-bon isotope analysis of speleothem samples can be expected toreveal much about climatic fluctuations.

As has been the case for primates and other vertebrates found infreshwater caves in the eastern Dominican Republic (e.g.,Rosenberger et al., 2011), the subfossils at Aven are remarkably well

Figure 3. Processing Aven subfossils. (a) Eight Pachylemur insignis crania; (b) close up of aduthe sameMesopropithecus individual with assorted lemur postcrania, including possibly assopartial cranium and an assortment of postcranial bones of Pachylemur. Photos courtesy of P

preserved, and they are abundant (Figs. 2 and 3, SOM Video 2).Remains are commonly scattered in full view on the surface of thesediment that makes up the cave floor. Because Aven is still activelyaccumulatingmaterial from the outside, and also decaying from theinside as its limestone shield disintegrates, specimens are some-times sprinkled with organic and/or inorganic residue. Theirdisposition suggests this is a low energy environment and has beenso in the recent past. In some areas, bones of birds and small

lt Mesopropithecus globiceps cranium, femur and unattributed astragalus; (c) remains ofciated femur, tibia, radius (second identifiable as Pachylemur) fibula and innominate; (d)hillip Lehman and Pietro Donaggio Bitner.

Table 1Provisional identification of taxa whose remains have been identified in the cavedeposits of Tsimanampetsotsa National Park (Aven, Mitoho, Malaza Manga, asindicated).

Cave Nowresident?

PrimatesLemuridaeǂPachylemur insignis Avena extinctLemur catta Avena yes

PalaeopropithecidaeǂMesopropithecus globiceps Avena extinct

MegaladapidaeǂMegaladapis edwardsi Mitohob and

Malaza Mangaaextinct

BatsHipposideridaeHipposideros sp. (commersoni?) Avena yes

CarnivoransEupleridaeǂCryptoprocta spelea Mitohoa extinct

ViverridaeViverricula indica Avena yes

Even-toed ungulatesHippopotamidaeǂHippopotamus lemerlei Avena extinct

RodentsMuridaeRattus rattus Avena yes

NesomyidaeHypogeomys antimena Mitohob locally

extirpated

CrocodyliansCrocodylidaeǂVoay robustus Avena and Mitohoc extinct

TortoisesTestudinidaeǂAldabrachelys sp. (abrupta?) Avena and Mitohob,c extinct

Elephant birds (Aepyornithiformes)AepyornithidaeǂMullerornis sp. Avena and Mitohob extinct

Raptors (Falconiformes)AccipitridaeǂAquila sp. Mitohoc extinct

a Our expedition.b Ross MacPhee expedition.c Perrier de la Bathie expedition.

A.L. Rosenberger et al. / Journal of Human Evolution 81 (2015) 83e8786

mammals also appear in dense concentrations, suggesting somenatural sorting. Skeletal parts of the larger taxa, including primates,carnivorans, crocodiles, hippos, or tortoises, are commonly found intightly-spaced accumulations, sometimes appearing as if the orig-inal cadavers were reduced to skeletons in place. Manually fanningor probing the silt would often yield more material at these loca-tions, ostensibly from that same animal. At numerous bone con-centrations, individuals belonging to a single taxon were found inclusters, suggesting a simultaneous, catastrophic event.

Due to time constraints and research priorities given to recon-naissance, no attempt was made to produce an estimate of thenumber of bones visible on the surface of the cave floor; besides,what can be seen is likely to be but a small fraction of the richnessof this sediment-laden deposit. We are comfortable saying severalthousands of bones have accumulated in Aven. For this preliminarysurvey, we concentrated on identifying the larger vertebrates.Generating a complete faunal list, especially accounting for the

smaller, abundant bird material (crania, postcrania, beaks), am-phibians, and reptiles, will be an ongoing priority. We did identifysmaller mammals, though, including bats, rodents, and carnivorans(Table 1).

After this initial field expedition, we have been able to establishthat the subfossil vertebrate assemblage in Aven represents areasonable cross-section of the known extinct fauna found in theregion of Tsimanampetsotsa National Park. The site also preservesspecies still living in the area (e.g., Lemur catta, the leaf-nosed batHipposideros (likely commersoni), the introduced Indian civetViverricula indica, and introduced rats, Rattus rattus). Non-primateextinct megafauna, including elephant birds (probably thesmaller genus,Mullerornis), the horned crocodile Voay robustus, thepygmy hippopotamusHippopotamus lemerlei, and the giant tortoiseAldabrachelys, are present. We gave less attention to subfossilswhile exploring the two other caves, both nearby. One, MalazaManga (literally the “famous blue” cave), an immense cave farlarger than Aven, is formed by huge chambers. The most note-worthy find there was a relatively complete cranium ofMegaladapisedwardsi. In Mitoho, we found what we believe to be a lair of theextinct giant fosa Cryptoprocta spelea, evidenced by four adultcrania plus postcrania found in very close proximity and near aconcentration of bones that may have been their prey.

But the dominant members of the subfossil fauna here are giantlemurs (Fig. 3). Aven Cave has yielded a large number of specimensof the extinct Pachylemur insignis. This is by far the richest andmostsignificant Pachylemur site in all of Madagascar in terms of qualityand quantity of material. There are dozens of extremely well pre-served crania visible and an equally large series of Pachylemurskeletal elements, too. The rare giant lemur species Meso-propithecus globiceps is also present, including poorly known andpreviously undescribed postcranial parts, and specimens belongingto an immature individual as well as adults.

While in all likelihood our reconnaissance expedition onlydocuments some of the eye-catching veneer of a rich sedimentarydeposit replete with subfossils, their diversity is a strong indicationof a large shift in the local ecology. For example, the native carni-vorans that still live in this region, Cryptoprocta ferox and the rareGalidictis grandidieri (Wozencraft,1990), are considerably smaller inbody size than the giant fosa, which disappeared with its mega-faunal prey. Among the primates, Pachylemur has been recon-structed as one of the most frugivorous of Malagasy lemurs on thebasis of its dental anatomy, microwear, relative infraorbital fora-men size, and stable isotopes (Godfrey et al., 2008; Crowley et al.,2011; Muchlinski et al., 2011; Godfrey et al., 2012). Morphologicalfeatures of the dentition (Seligsohn and Szalay, 1974) and ancientDNA (Kistler et al., 2015) signal a close relationship to Varecia,which is the most frugivorous of the larger-bodied living lemurs.The abundance of Pachylemur at Tsimanampetsotsa supports theidea drawn from the study of fossil pollen and other data thatsouthwestern Madagascar was wetter in the recent past than it istoday (Mah�e and Sourdat, 1972; Burney, 1993; Goodman andRakotozafy, 1997; Goodman and Jungers, 2014). Ring-tailed le-murs, which thrive today at Tsimanampetsotsa, do so in partbecause they consume many leaves of succulent (CAM) plants(Loudon et al., 2008; LaFleur, M. 2012). Pachylemur stands instriking contrast; there is little evidence for CAM plant consump-tion in this animal (Crowley et al., 2011).

Among the many reasons why the submerged caves of Tsima-nampetsotsa hold special scientific promise, three are outstanding.First, as a natural, seemingly indiscriminate aggregator of animalremains, the caves of Aven, Malaza Manga and Mitoho are likely toproduce a solid picture of local, past biodiversity. Prior paleonto-logical expeditions (Perrier de la Bathie, 1934; MacPhee expedition,described by Goodman and Jungers (2014) had revealed the

A.L. Rosenberger et al. / Journal of Human Evolution 81 (2015) 83e87 87

presence of Megaladapis and other megafauna, including elephantbirds, giant tortoises, crocodiles, and raptors at Tsimanampetsotsa.Our expedition has greatly expanded the faunal list (Table 1).

Second, the mixed presence of introduced species (rats and In-dian civets) and extinct, archaic subfossils indicates a temporaloverlap with humans in the region. Many of the radiometric dateson subfossils from other sites in the southwest fall in the “humanperiod.” Evidence of people in southwestern Madagascar extendsmore than 2000 years (Burney, 1993; Crowley, 2010); a single datedelephant bird eggshell from Mitoho Cave has a calibrated age of4480 BP (Crowley, 2010).

Third, caves such as Aven differ from typical dry cave deposits onthe island where there is little or no stratigraphic control. Technicaldifficulties notwithstanding, Aven may produce a temporal profilethat will lay out the timing of the story of Madagascar's megafaunaldisappearance, in connection with environmental change andhuman-induced ecological disruption. Although humans arewidely considered to be the primary trigger of these extinctions(Burney et al., 2003), the relative contributions of climate changeand human activities to this ecological transformation are stillcontested (e.g., Virah-Sawmy et al., 2009). Previous work on thesmall mammal and avian fauna of southwestern Madagascar hasdemonstrated that small animals can be an important tool inreconstructing paleoecological history (e.g., Muldoon et al., 2009;Muldoon, 2010; Goodman et al., 2013). The abundant remainswithin Aven and other flooded caves may thus provide a new levelof empirical detail bearing on the driving forces behind themegafaunal holocaust that brought down Madagascar's uniquefauna and flora.

Acknowledgments

This project was conducted under a collaborative accord forpaleobiological and paleoclimatological research between theUniversity of Antananarivo (Department of Biological Anthropologyand Paleontology) and the University of Massachusetts (De-partments of Anthropology and Geosciences), in extended collab-oration with researchers at Brooklyn College, MidwesternUniversity, and Duke University. The team included, in addition tothe authors, University of Antananarivo graduate student Nor-omamy Rahantaharivao. The research was sanctioned by theMadagascar Ministry of Mines, the Ministry of Education, theMinistry of Arts and Culture, and Madagascar National Parks. It wassupported financially by the National Science Foundation (RAPIDBCS-1446959, awarded to ALR) and the National Geographic Soci-ety (9571-14, awarded to ALR, KM, LRG and GFG). It could neverhave been accomplished without the generosity ofWalter Vauthier,proprietor of the Anakao Ocean Lodge, which served as our homebase.We are indebted to officials of the variousMalagasyministriesmentioned above, and without question our deepest gratitude goesto our international team of highly skilled, selfless divers whocontributed freely to accomplish the mission: Ryan Dart(Madagascar), who discovered and recognized the importance ofthe bone accumulations; Phillip Lehman (Dominican Republic),who planned and coordinated the expedition and supported it incountless ways; cameraman Pietro Donaggio Bitner (Chile), fordocumenting brilliantly the setting and scientific activities; VictoriaAlexandrova (Dominican Republic), Mauro Bordignon (Mexico),Kim Davidsson (Mexico), Pietro Donaggio Bitner (Chile), Hans

Kaspersetz (USA), and Patrick Widmann (Mexico), for their gener-osity, collegiality and extraordinary teamwork.

Appendix A. Supplementary data

Supplementary data related to this article can be found at http://dx.doi.org/10.1016/j.jhevol.2015.01.004

References

Burney, D.A., 1993. Late Holocene environmental changes in arid southwesternMadagascar. Quat. Res. 40, 98e106.

Burney, D.A., Robinson, G.S., Burney, L.P., 2003. Sporormiella and the late Holoceneextinctions. Proc. Natl. Acad. Sci. 100, 10800e10805.

Crowley, B.E., 2010. A refined chronology of prehistoric Madagascar and the demiseof the megafauna. Quat. Sci. Rev. 29, 2591e2603.

Crowley, B.E., Godfrey, L.R., Irwin, M.T., 2011. A glance to the past: subfossils, stableisotopes, seed dispersal, and lemur species loss in southern Madagascar. Am. J.Primatol. 73, 25e37.

Godfrey, L.R., Jungers, W.L., Schwartz, G.T., Irwin, M.T., 2008. Ghosts and orphans:Madagascar's vanishing ecosystems. In: Fleagle, J.G., Gilbert, C.C. (Eds.), ElwynSimons: A Search for Origins. Springer, New York, pp. 361e395.

Godfrey, L.R., Winchester, J.M., King, S.J., Boyer, D.M., Jernvall, J., 2012. Dentaltopography indicates ecological contraction of lemur communities. Am. J. Phys.Anthropol. 148, 215e227.

Goodman, S.M., Jungers, W.L., 2014. Extinct Madagascar: Picturing the Island's Past.University of Chicago Press, Chicago.

Goodman, S.M., Rakotozafy, L.M.A., 1997. Subfossil birds from coastal sites inwestern and southwestern Madagascar: A paleoenvironmental reconstruction.In: Goodman, S.M., Patterson, B.D. (Eds.), Natural Change and Human Impact inMadagascar. Smithsonian Institution Press, Washington D.C., pp. 257e279.

Goodman, S.M., Raherilalao, M.J., Muldoon, K.M., 2013. Bird subfossils from Anki-litelo Cave: inference about historical environmental changes in southwesternMadagascar. Zootaxa 3750, 534e548.

Kistler, L., Ratan, A., Godfrey, L.R., Crowley, B.E., Hughes, C.E., Lei, R., Cui, Y.,Wood, M.L., Muldoon, K.M., Andriamialison, H., McGraw, J.J., Tomsho, L.P.,Schuster, S.C., Miller, W., Louis, E.E., Yoder, A.D., Malhi, R.S., Petter, G.H., 2015.Comparative and population mitogenomic analyses of Madagascar's extinct,giant ‘subfossil’ lemurs. J. Hum. Evol. 79, 45e54. http://dx.doi.org/10.1016/j.jhevd.2014.06.016.

LaFleur, M., 2012. Ecology of Lemur catta at the Tsimanampetsotsa National Park,Madagascar: Implications for female dominance and the evolution of lemurtraits. Ph.D. Dissertation. University of Colorado, Boulder.

Loudon, J.E., Whitelaw, D.C., Sponheimer, M., Sauther, M.L., Cuozzo, F.P., 2008. Le-murs eating isotopes: A stable isotope analysis of ring-tailed lemurs (Lemurcatta) and their menu at the Beza Mahafaly Special Reserve. Am. J. Phys.Anthropol. 135 (Suppl 46), 142.

Mah�e, J., Sourdat, M., 1972. Sur l'extinction des vert�ebr�es subfossiles et l’ar-idification du climat dans le Sud-ouest de Madagascar. Bull. Soc. G�eol. France 14,295e309.

Muchlinski, M.N., Godfrey, L.R., Muldoon, K.M., Tongasoa, L., 2011. Evidence fordietary niche separation based on infraorbital foramen size variation amongsubfossil lemurs. Folia Primatol. 81, 330e345.

Muldoon, K.M., DeBlieux, D.D., Simons, E.L., Chatrath, P.S., 2009. The subfossiloccurrence and paleoecological significance of small mammals at Ankilitelocave, southwestern Madagascar. J. Mammal. 90, 1111e1131.

Muldoon, K.M., 2010. Paleoenvironment of Ankilitelo Cave (late Holocene, south-western Madagascar): implications for the extinction of giant lemurs. J. Hum.Evol. 58, 338e352.

Perrier de la Bathie, H., 1934. Au sujet de l’age de la faune �a Aepyornis et hippo-potames. M�em. Acad. Malgache 17, 162e168.

Richards, D.A., Dorale, J.A., 2003. Uranium-series chronology and environmentalapplications of speleothems. Rev. Mineral. Geochem. 52, 407e460.

Rosenberger, A.L., Cooke, S.B., Rímoli, R., Ni, X., Cardoso, L., 2011. First skull ofAntillothrix bernensis, an extinct relict monkey from the Dominican Republic.Proc. R. Soc. B 278, 67e74.

Seligsohn, D., Szalay, F.S., 1974. Dental occlusion and the masticatory apparatus inLemur and Varecia: their bearing on the systematics of living and fossil pri-mates. In: Martin, R.D., Doyle, G.A., Walker, A.C. (Eds.), Prosimian Biology.Duckworth, London, pp. 543e561.

Virah-Sawmy, M., Bonsall, M.B., Willis, K.J., 2009. ‘Tales of Symphonia’: extinctiondynamics in response to past climate change in Madagascan rainforests. Biol.Lett. 5, 821e825.

Wozencraft, W.C., 1990. Alive and well in Tsimanampetsotsa. Nat. Hist. 99 (12),28e30.