Journal of Human Evolution 81 (2015) 83e87
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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, USA Brooklyn College: NYCEP (New York Consortium in Evolutionary Primatology), USA Department of Anthropology, Machmer Hall, 240 Hicks Way, University of Massachusetts, Amherst, MA 01003, USA d Department of Anatomy, Arizona College of Osteopathic Medicine, Midwestern University, 19555 N. 59th Avenue, Glendale, AZ 85308, USA e Division of Fossil Primates, Duke Lemur Center, 1013 Broad Street, Durham, NC 27705, USA f Departement de Pal eontologie et d'Anthropologie Biologique, Facult e des Sciences, Universit e d'Antananarivo, BP 906, Ankatso, 101 Antananarivo, Madagascar g National Geographic Society, 1145 17St NW, Washington, DC 20036, USA b c
a r t i c l e i n f o Article history: Received 15 January 2015 Accepted 16 January 2015 Available online 6 March 2015 Keywords: Madagascar Subfossil lemurs Underwater paleontology Flooded caves
In October, 2014, we organized a paleontological expedition to investigate flooded freshwater caves in Tsimanampetsotsa National Park, Madagascar, located in the arid southwestern region of the country where the karst landscape is pocked with dry caves and large water-filled sinkholes (Fig. 1). Our team of nine scuba divers was led by Phillip Lehman of the Dominican Republic Speleological Society (Supplementary Online Material [SOM] Video 1). The discovery of subfossils in Tsimanampetsotsa was made initially by Ryan Dart of Antananarivo. The director of Tsimanampetsotsa National Park, Mr. Lovasoa Dresy, immediately recognized their importance to science and encouraged the work reported here. Substantial numbers of subfossil remains were found in three caves. In Aven Cave we discovered what is likely to be the single largest cache of giant subfossil lemurs ever uncovered. The other
* Corresponding author. E-mail address: [email protected] (A.L. Rosenberger). http://dx.doi.org/10.1016/j.jhevol.2015.01.004 0047-2484/© 2015 Elsevier Ltd. All rights reserved.
two fossiliferous caves were Mitoho and Malaza Manga. Subfossils had been previously reported from around the entrance to Mitoho ^thie, 1934; Goodman and Jungers, 2014) but Cave (Perrier de la Ba no underwater investigation of remains inside any of these caves had been conducted prior to this expedition. Thus the primary objective was to establish the paleontological potential of these caves, with the principal aim of assessing the biodiversity of the subfossil content of Aven (Fig. 1). Aven is a karstic dissolution cave or sink hole produced by water draining through the porous limestone shelf. It is a classic vertical sink hole with deep horizontal cave passageways, each ending in a collapse of limestone blocks. In the complex of tunnels and passages, many sections can be accessed only through narrow restrictions, a challenge that requires advanced cave diving techniques as a precondition to safe exploration of this dark, uncharted subterranean environment (Fig. 2C). It is readily apparent that these spaces were dry in the past as there is substantial speleothem (stalactite and stalagmite) formation. The full extent of Aven's passageways has yet to be explored, but our team laid about 268 m of safety line during the expedition, running at an average depth of 42 m. The opening of the sink hole is some 25 m in circumference, and the water table is located 10e12 m below the rim. A small island in the center of the water pool is the very top of a debris cone, what's left of the collapsed overhead rock (Fig. 1). The mound falls gently into the depths of the lit cavern to about 25 m, from where the cave extends into the blackness in all directions. It is in this transitional zone where most of the more visible subfossil remains have been located. During the survey, standard cave mapping techniques were employed to locate and mark areas with materials of interest, such as dense bone accumulations or the location of important specimens. It became immediately apparent that there were multiple sites of import and hundreds of cranial and postcranial remains
84
A.L. Rosenberger et al. / Journal of Human Evolution 81 (2015) 83e87
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 National Park; (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 the cavern debris cone (left). Sketch map by Phillip Lehman.
that deserve close attention. We also employed 3D photographic techniques to document the morphology and in situ context of specimens, such as the horned crocodile Voay robustus (SOM Fig. 1). The geological context, age, speleology and taphonomy of Aven will be subjects of future studies. Considering the importance of
establishing a stratigraphic chronology, we tested the sediment by pushing meter-length probes into it at three widely separated areas where bones were exposed on the surface. The probes were easily inserted and met little or no bottom resistance. Furthermore, since speleothems would have formed only when the cave was not
A.L. Rosenberger et al. / Journal of Human Evolution 81 (2015) 83e87
85
Figure 2. High resolution, in situ photographs of Aven subfossils. (a) Pachylemur insignis cranium associated with postcranials; (b) bone concentration with at least three Pachylemur crania visible; (c) Victoria Alexandrova marking a horned crocodile, Voay robustus; (d) two adult Pachylemur crania (“the twins”). Photos courtesy of Phillip Lehman and Pietro Donaggio Bitner.
flooded, uranium-series-disequilibrium (230Th/U) dating should provide accurate estimates of the timing of the flooding episode or episodes (Richards and Dorale, 2003), and stable oxygen and carbon isotope analysis of speleothem samples can be expected to reveal much about climatic fluctuations. As has been the case for primates and other vertebrates found in freshwater caves in the eastern Dominican Republic (e.g., Rosenberger et al., 2011), the subfossils at Aven are remarkably well
preserved, and they are abundant (Figs. 2 and 3, SOM Video 2). Remains are commonly scattered in full view on the surface of the sediment that makes up the cave floor. Because Aven is still actively accumulating material from the outside, and also decaying from the inside as its limestone shield disintegrates, specimens are sometimes sprinkled with organic and/or inorganic residue. Their disposition suggests this is a low energy environment and has been so in the recent past. In some areas, bones of birds and small
Figure 3. Processing Aven subfossils. (a) Eight Pachylemur insignis crania; (b) close up of adult Mesopropithecus globiceps cranium, femur and unattributed astragalus; (c) remains of the same Mesopropithecus individual with assorted lemur postcrania, including possibly associated femur, tibia, radius (second identifiable as Pachylemur) fibula and innominate; (d) partial cranium and an assortment of postcranial bones of Pachylemur. Photos courtesy of Phillip Lehman and Pietro Donaggio Bitner.
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A.L. Rosenberger et al. / Journal of Human Evolution 81 (2015) 83e87
Table 1 Provisional identification of taxa whose remains have been identified in the cave deposits of Tsimanampetsotsa National Park (Aven, Mitoho, Malaza Manga, as indicated). Cave
Now resident?
Primates Lemuridae ǂPachylemur insignis Lemur catta
Avena Avena
extinct yes
Palaeopropithecidae ǂMesopropithecus globiceps
Avena
extinct
Mitohob and Malaza Mangaa
extinct
Bats Hipposideridae Hipposideros sp. (commersoni?)
Avena
yes
Carnivorans Eupleridae ǂCryptoprocta spelea
Mitohoa
extinct
Viverridae Viverricula indica
Avena
yes
Even-toed ungulates Hippopotamidae ǂHippopotamus lemerlei
Avena
extinct
Rodents Muridae Rattus rattus
Avena
yes
Nesomyidae Hypogeomys antimena
Mitohob
locally extirpated
Crocodylians Crocodylidae ǂVoay robustus
Avena and Mitohoc
extinct
Tortoises Testudinidae ǂAldabrachelys sp. (abrupta?)
Avena and Mitohob,c
extinct
Elephant birds (Aepyornithiformes) Aepyornithidae ǂMullerornis sp.
Avena and Mitohob
extinct
Raptors (Falconiformes) Accipitridae ǂAquila sp.
Mitohoc
extinct
Megaladapidae ǂMegaladapis edwardsi
a b c
Our expedition. Ross MacPhee expedition. Perrier de la B^ athie expedition.
mammals also appear in dense concentrations, suggesting some natural sorting. Skeletal parts of the larger taxa, including primates, carnivorans, crocodiles, hippos, or tortoises, are commonly found in tightly-spaced accumulations, sometimes appearing as if the original cadavers were reduced to skeletons in place. Manually fanning or probing the silt would often yield more material at these locations, ostensibly from that same animal. At numerous bone concentrations, individuals belonging to a single taxon were found in clusters, suggesting a simultaneous, catastrophic event. Due to time constraints and research priorities given to reconnaissance, no attempt was made to produce an estimate of the number 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 richness of this sediment-laden deposit. We are comfortable saying several thousands of bones have accumulated in Aven. For this preliminary survey, we concentrated on identifying the larger vertebrates. Generating a complete faunal list, especially accounting for the
smaller, abundant bird material (crania, postcrania, beaks), amphibians, and reptiles, will be an ongoing priority. We did identify smaller mammals, though, including bats, rodents, and carnivorans (Table 1). After this initial field expedition, we have been able to establish that the subfossil vertebrate assemblage in Aven represents a reasonable cross-section of the known extinct fauna found in the region of Tsimanampetsotsa National Park. The site also preserves species still living in the area (e.g., Lemur catta, the leaf-nosed bat Hipposideros (likely commersoni), the introduced Indian civet Viverricula indica, and introduced rats, Rattus rattus). Non-primate extinct megafauna, including elephant birds (probably the smaller genus, Mullerornis), the horned crocodile Voay robustus, the pygmy hippopotamus Hippopotamus lemerlei, and the giant tortoise Aldabrachelys, are present. We gave less attention to subfossils while exploring the two other caves, both nearby. One, Malaza Manga (literally the “famous blue” cave), an immense cave far larger than Aven, is formed by huge chambers. The most noteworthy find there was a relatively complete cranium of Megaladapis edwardsi. In Mitoho, we found what we believe to be a lair of the extinct giant fosa Cryptoprocta spelea, evidenced by four adult crania plus postcrania found in very close proximity and near a concentration of bones that may have been their prey. But the dominant members of the subfossil fauna here are giant lemurs (Fig. 3). Aven Cave has yielded a large number of specimens of the extinct Pachylemur insignis. This is by far the richest and most significant Pachylemur site in all of Madagascar in terms of quality and quantity of material. There are dozens of extremely well preserved crania visible and an equally large series of Pachylemur skeletal elements, too. The rare giant lemur species Mesopropithecus globiceps is also present, including poorly known and previously undescribed postcranial parts, and specimens belonging to an immature individual as well as adults. While in all likelihood our reconnaissance expedition only documents some of the eye-catching veneer of a rich sedimentary deposit replete with subfossils, their diversity is a strong indication of a large shift in the local ecology. For example, the native carnivorans that still live in this region, Cryptoprocta ferox and the rare Galidictis grandidieri (Wozencraft, 1990), are considerably smaller in body size than the giant fosa, which disappeared with its megafaunal prey. Among the primates, Pachylemur has been reconstructed as one of the most frugivorous of Malagasy lemurs on the basis of its dental anatomy, microwear, relative infraorbital foramen size, and stable isotopes (Godfrey et al., 2008; Crowley et al., 2011; Muchlinski et al., 2011; Godfrey et al., 2012). Morphological features of the dentition (Seligsohn and Szalay, 1974) and ancient DNA (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 the idea drawn from the study of fossil pollen and other data that southwestern Madagascar was wetter in the recent past than it is and Sourdat, 1972; Burney, 1993; Goodman and today (Mahe Rakotozafy, 1997; Goodman and Jungers, 2014). Ring-tailed lemurs, which thrive today at Tsimanampetsotsa, do so in part because they consume many leaves of succulent (CAM) plants (Loudon et al., 2008; LaFleur, M. 2012). Pachylemur stands in striking contrast; there is little evidence for CAM plant consumption in this animal (Crowley et al., 2011). Among the many reasons why the submerged caves of Tsimanampetsotsa hold special scientific promise, three are outstanding. First, as a natural, seemingly indiscriminate aggregator of animal remains, the caves of Aven, Malaza Manga and Mitoho are likely to produce a solid picture of local, past biodiversity. Prior paleonto^thie, 1934; MacPhee expedition, logical expeditions (Perrier de la Ba described by Goodman and Jungers (2014) had revealed the
A.L. Rosenberger et al. / Journal of Human Evolution 81 (2015) 83e87
presence of Megaladapis and other megafauna, including elephant birds, 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 Indian civets) and extinct, archaic subfossils indicates a temporal overlap with humans in the region. Many of the radiometric dates on subfossils from other sites in the southwest fall in the “human period.” Evidence of people in southwestern Madagascar extends more than 2000 years (Burney, 1993; Crowley, 2010); a single dated elephant bird eggshell from Mitoho Cave has a calibrated age of 4480 BP (Crowley, 2010). Third, caves such as Aven differ from typical dry cave deposits on the island where there is little or no stratigraphic control. Technical difficulties notwithstanding, Aven may produce a temporal profile that will lay out the timing of the story of Madagascar's megafaunal disappearance, in connection with environmental change and human-induced ecological disruption. Although humans are widely considered to be the primary trigger of these extinctions (Burney et al., 2003), the relative contributions of climate change and human activities to this ecological transformation are still contested (e.g., Virah-Sawmy et al., 2009). Previous work on the small mammal and avian fauna of southwestern Madagascar has demonstrated that small animals can be an important tool in reconstructing paleoecological history (e.g., Muldoon et al., 2009; Muldoon, 2010; Goodman et al., 2013). The abundant remains within Aven and other flooded caves may thus provide a new level of empirical detail bearing on the driving forces behind the megafaunal holocaust that brought down Madagascar's unique fauna and flora.
Acknowledgments This project was conducted under a collaborative accord for paleobiological and paleoclimatological research between the University of Antananarivo (Department of Biological Anthropology and Paleontology) and the University of Massachusetts (Departments of Anthropology and Geosciences), in extended collaboration with researchers at Brooklyn College, Midwestern University, and Duke University. The team included, in addition to the authors, University of Antananarivo graduate student Noromamy Rahantaharivao. The research was sanctioned by the Madagascar Ministry of Mines, the Ministry of Education, the Ministry of Arts and Culture, and Madagascar National Parks. It was supported financially by the National Science Foundation (RAPID BCS-1446959, awarded to ALR) and the National Geographic Society (9571-14, awarded to ALR, KM, LRG and GFG). It could never have been accomplished without the generosity of Walter Vauthier, proprietor of the Anakao Ocean Lodge, which served as our home base. We are indebted to officials of the various Malagasy ministries mentioned above, and without question our deepest gratitude goes to our international team of highly skilled, selfless divers who contributed freely to accomplish the mission: Ryan Dart (Madagascar), who discovered and recognized the importance of the bone accumulations; Phillip Lehman (Dominican Republic), who planned and coordinated the expedition and supported it in countless ways; cameraman Pietro Donaggio Bitner (Chile), for documenting brilliantly the setting and scientific activities; Victoria Alexandrova (Dominican Republic), Mauro Bordignon (Mexico), Kim Davidsson (Mexico), Pietro Donaggio Bitner (Chile), Hans
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Kaspersetz (USA), and Patrick Widmann (Mexico), for their generosity, 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 southwestern Madagascar. Quat. Res. 40, 98e106. Burney, D.A., Robinson, G.S., Burney, L.P., 2003. Sporormiella and the late Holocene extinctions. Proc. Natl. Acad. Sci. 100, 10800e10805. Crowley, B.E., 2010. A refined chronology of prehistoric Madagascar and the demise of the megafauna. Quat. Sci. Rev. 29, 2591e2603. Crowley, B.E., Godfrey, L.R., Irwin, M.T., 2011. A glance to the past: subfossils, stable isotopes, 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.), Elwyn Simons: A Search for Origins. Springer, New York, pp. 361e395. Godfrey, L.R., Winchester, J.M., King, S.J., Boyer, D.M., Jernvall, J., 2012. Dental topography 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 in western and southwestern Madagascar: A paleoenvironmental reconstruction. In: Goodman, S.M., Patterson, B.D. (Eds.), Natural Change and Human Impact in Madagascar. Smithsonian Institution Press, Washington D.C., pp. 257e279. Goodman, S.M., Raherilalao, M.J., Muldoon, K.M., 2013. Bird subfossils from Ankilitelo Cave: inference about historical environmental changes in southwestern Madagascar. 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 lemur traits. Ph.D. Dissertation. University of Colorado, Boulder. Loudon, J.E., Whitelaw, D.C., Sponheimer, M., Sauther, M.L., Cuozzo, F.P., 2008. Lemurs eating isotopes: A stable isotope analysis of ring-tailed lemurs (Lemur catta) and their menu at the Beza Mahafaly Special Reserve. Am. J. Phys. Anthropol. 135 (Suppl 46), 142. , J., Sourdat, M., 1972. Sur l'extinction des verte bre s subfossiles et l’arMahe ol. France 14, idification du climat dans le Sud-ouest de Madagascar. Bull. Soc. Ge 295e309. Muchlinski, M.N., Godfrey, L.R., Muldoon, K.M., Tongasoa, L., 2011. Evidence for dietary niche separation based on infraorbital foramen size variation among subfossil lemurs. Folia Primatol. 81, 330e345. Muldoon, K.M., DeBlieux, D.D., Simons, E.L., Chatrath, P.S., 2009. The subfossil occurrence and paleoecological significance of small mammals at Ankilitelo cave, southwestern Madagascar. J. Mammal. 90, 1111e1131. Muldoon, K.M., 2010. Paleoenvironment of Ankilitelo Cave (late Holocene, southwestern Madagascar): implications for the extinction of giant lemurs. J. Hum. Evol. 58, 338e352. ^thie, H., 1934. Au sujet de l’a ^ge de la faune a Aepyornis et hippoPerrier de la Ba m. Acad. Malgache 17, 162e168. potames. Me Richards, D.A., Dorale, J.A., 2003. Uranium-series chronology and environmental applications of speleothems. Rev. Mineral. Geochem. 52, 407e460. Rosenberger, A.L., Cooke, S.B., Rímoli, R., Ni, X., Cardoso, L., 2011. First skull of Antillothrix 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 in Lemur and Varecia: their bearing on the systematics of living and fossil primates. 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’: extinction dynamics 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.
Contents lists available at ScienceDirect
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, USA Brooklyn College: NYCEP (New York Consortium in Evolutionary Primatology), USA Department of Anthropology, Machmer Hall, 240 Hicks Way, University of Massachusetts, Amherst, MA 01003, USA d Department of Anatomy, Arizona College of Osteopathic Medicine, Midwestern University, 19555 N. 59th Avenue, Glendale, AZ 85308, USA e Division of Fossil Primates, Duke Lemur Center, 1013 Broad Street, Durham, NC 27705, USA f Departement de Pal eontologie et d'Anthropologie Biologique, Facult e des Sciences, Universit e d'Antananarivo, BP 906, Ankatso, 101 Antananarivo, Madagascar g National Geographic Society, 1145 17St NW, Washington, DC 20036, USA b c
a r t i c l e i n f o Article history: Received 15 January 2015 Accepted 16 January 2015 Available online 6 March 2015 Keywords: Madagascar Subfossil lemurs Underwater paleontology Flooded caves
In October, 2014, we organized a paleontological expedition to investigate flooded freshwater caves in Tsimanampetsotsa National Park, Madagascar, located in the arid southwestern region of the country where the karst landscape is pocked with dry caves and large water-filled sinkholes (Fig. 1). Our team of nine scuba divers was led by Phillip Lehman of the Dominican Republic Speleological Society (Supplementary Online Material [SOM] Video 1). The discovery of subfossils in Tsimanampetsotsa was made initially by Ryan Dart of Antananarivo. The director of Tsimanampetsotsa National Park, Mr. Lovasoa Dresy, immediately recognized their importance to science and encouraged the work reported here. Substantial numbers of subfossil remains were found in three caves. In Aven Cave we discovered what is likely to be the single largest cache of giant subfossil lemurs ever uncovered. The other
* Corresponding author. E-mail address: [email protected] (A.L. Rosenberger). http://dx.doi.org/10.1016/j.jhevol.2015.01.004 0047-2484/© 2015 Elsevier Ltd. All rights reserved.
two fossiliferous caves were Mitoho and Malaza Manga. Subfossils had been previously reported from around the entrance to Mitoho ^thie, 1934; Goodman and Jungers, 2014) but Cave (Perrier de la Ba no underwater investigation of remains inside any of these caves had been conducted prior to this expedition. Thus the primary objective was to establish the paleontological potential of these caves, with the principal aim of assessing the biodiversity of the subfossil content of Aven (Fig. 1). Aven is a karstic dissolution cave or sink hole produced by water draining through the porous limestone shelf. It is a classic vertical sink hole with deep horizontal cave passageways, each ending in a collapse of limestone blocks. In the complex of tunnels and passages, many sections can be accessed only through narrow restrictions, a challenge that requires advanced cave diving techniques as a precondition to safe exploration of this dark, uncharted subterranean environment (Fig. 2C). It is readily apparent that these spaces were dry in the past as there is substantial speleothem (stalactite and stalagmite) formation. The full extent of Aven's passageways has yet to be explored, but our team laid about 268 m of safety line during the expedition, running at an average depth of 42 m. The opening of the sink hole is some 25 m in circumference, and the water table is located 10e12 m below the rim. A small island in the center of the water pool is the very top of a debris cone, what's left of the collapsed overhead rock (Fig. 1). The mound falls gently into the depths of the lit cavern to about 25 m, from where the cave extends into the blackness in all directions. It is in this transitional zone where most of the more visible subfossil remains have been located. During the survey, standard cave mapping techniques were employed to locate and mark areas with materials of interest, such as dense bone accumulations or the location of important specimens. It became immediately apparent that there were multiple sites of import and hundreds of cranial and postcranial remains
84
A.L. Rosenberger et al. / Journal of Human Evolution 81 (2015) 83e87
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 National Park; (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 the cavern debris cone (left). Sketch map by Phillip Lehman.
that deserve close attention. We also employed 3D photographic techniques to document the morphology and in situ context of specimens, such as the horned crocodile Voay robustus (SOM Fig. 1). The geological context, age, speleology and taphonomy of Aven will be subjects of future studies. Considering the importance of
establishing a stratigraphic chronology, we tested the sediment by pushing meter-length probes into it at three widely separated areas where bones were exposed on the surface. The probes were easily inserted and met little or no bottom resistance. Furthermore, since speleothems would have formed only when the cave was not
A.L. Rosenberger et al. / Journal of Human Evolution 81 (2015) 83e87
85
Figure 2. High resolution, in situ photographs of Aven subfossils. (a) Pachylemur insignis cranium associated with postcranials; (b) bone concentration with at least three Pachylemur crania visible; (c) Victoria Alexandrova marking a horned crocodile, Voay robustus; (d) two adult Pachylemur crania (“the twins”). Photos courtesy of Phillip Lehman and Pietro Donaggio Bitner.
flooded, uranium-series-disequilibrium (230Th/U) dating should provide accurate estimates of the timing of the flooding episode or episodes (Richards and Dorale, 2003), and stable oxygen and carbon isotope analysis of speleothem samples can be expected to reveal much about climatic fluctuations. As has been the case for primates and other vertebrates found in freshwater caves in the eastern Dominican Republic (e.g., Rosenberger et al., 2011), the subfossils at Aven are remarkably well
preserved, and they are abundant (Figs. 2 and 3, SOM Video 2). Remains are commonly scattered in full view on the surface of the sediment that makes up the cave floor. Because Aven is still actively accumulating material from the outside, and also decaying from the inside as its limestone shield disintegrates, specimens are sometimes sprinkled with organic and/or inorganic residue. Their disposition suggests this is a low energy environment and has been so in the recent past. In some areas, bones of birds and small
Figure 3. Processing Aven subfossils. (a) Eight Pachylemur insignis crania; (b) close up of adult Mesopropithecus globiceps cranium, femur and unattributed astragalus; (c) remains of the same Mesopropithecus individual with assorted lemur postcrania, including possibly associated femur, tibia, radius (second identifiable as Pachylemur) fibula and innominate; (d) partial cranium and an assortment of postcranial bones of Pachylemur. Photos courtesy of Phillip Lehman and Pietro Donaggio Bitner.
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A.L. Rosenberger et al. / Journal of Human Evolution 81 (2015) 83e87
Table 1 Provisional identification of taxa whose remains have been identified in the cave deposits of Tsimanampetsotsa National Park (Aven, Mitoho, Malaza Manga, as indicated). Cave
Now resident?
Primates Lemuridae ǂPachylemur insignis Lemur catta
Avena Avena
extinct yes
Palaeopropithecidae ǂMesopropithecus globiceps
Avena
extinct
Mitohob and Malaza Mangaa
extinct
Bats Hipposideridae Hipposideros sp. (commersoni?)
Avena
yes
Carnivorans Eupleridae ǂCryptoprocta spelea
Mitohoa
extinct
Viverridae Viverricula indica
Avena
yes
Even-toed ungulates Hippopotamidae ǂHippopotamus lemerlei
Avena
extinct
Rodents Muridae Rattus rattus
Avena
yes
Nesomyidae Hypogeomys antimena
Mitohob
locally extirpated
Crocodylians Crocodylidae ǂVoay robustus
Avena and Mitohoc
extinct
Tortoises Testudinidae ǂAldabrachelys sp. (abrupta?)
Avena and Mitohob,c
extinct
Elephant birds (Aepyornithiformes) Aepyornithidae ǂMullerornis sp.
Avena and Mitohob
extinct
Raptors (Falconiformes) Accipitridae ǂAquila sp.
Mitohoc
extinct
Megaladapidae ǂMegaladapis edwardsi
a b c
Our expedition. Ross MacPhee expedition. Perrier de la B^ athie expedition.
mammals also appear in dense concentrations, suggesting some natural sorting. Skeletal parts of the larger taxa, including primates, carnivorans, crocodiles, hippos, or tortoises, are commonly found in tightly-spaced accumulations, sometimes appearing as if the original cadavers were reduced to skeletons in place. Manually fanning or probing the silt would often yield more material at these locations, ostensibly from that same animal. At numerous bone concentrations, individuals belonging to a single taxon were found in clusters, suggesting a simultaneous, catastrophic event. Due to time constraints and research priorities given to reconnaissance, no attempt was made to produce an estimate of the number 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 richness of this sediment-laden deposit. We are comfortable saying several thousands of bones have accumulated in Aven. For this preliminary survey, we concentrated on identifying the larger vertebrates. Generating a complete faunal list, especially accounting for the
smaller, abundant bird material (crania, postcrania, beaks), amphibians, and reptiles, will be an ongoing priority. We did identify smaller mammals, though, including bats, rodents, and carnivorans (Table 1). After this initial field expedition, we have been able to establish that the subfossil vertebrate assemblage in Aven represents a reasonable cross-section of the known extinct fauna found in the region of Tsimanampetsotsa National Park. The site also preserves species still living in the area (e.g., Lemur catta, the leaf-nosed bat Hipposideros (likely commersoni), the introduced Indian civet Viverricula indica, and introduced rats, Rattus rattus). Non-primate extinct megafauna, including elephant birds (probably the smaller genus, Mullerornis), the horned crocodile Voay robustus, the pygmy hippopotamus Hippopotamus lemerlei, and the giant tortoise Aldabrachelys, are present. We gave less attention to subfossils while exploring the two other caves, both nearby. One, Malaza Manga (literally the “famous blue” cave), an immense cave far larger than Aven, is formed by huge chambers. The most noteworthy find there was a relatively complete cranium of Megaladapis edwardsi. In Mitoho, we found what we believe to be a lair of the extinct giant fosa Cryptoprocta spelea, evidenced by four adult crania plus postcrania found in very close proximity and near a concentration of bones that may have been their prey. But the dominant members of the subfossil fauna here are giant lemurs (Fig. 3). Aven Cave has yielded a large number of specimens of the extinct Pachylemur insignis. This is by far the richest and most significant Pachylemur site in all of Madagascar in terms of quality and quantity of material. There are dozens of extremely well preserved crania visible and an equally large series of Pachylemur skeletal elements, too. The rare giant lemur species Mesopropithecus globiceps is also present, including poorly known and previously undescribed postcranial parts, and specimens belonging to an immature individual as well as adults. While in all likelihood our reconnaissance expedition only documents some of the eye-catching veneer of a rich sedimentary deposit replete with subfossils, their diversity is a strong indication of a large shift in the local ecology. For example, the native carnivorans that still live in this region, Cryptoprocta ferox and the rare Galidictis grandidieri (Wozencraft, 1990), are considerably smaller in body size than the giant fosa, which disappeared with its megafaunal prey. Among the primates, Pachylemur has been reconstructed as one of the most frugivorous of Malagasy lemurs on the basis of its dental anatomy, microwear, relative infraorbital foramen size, and stable isotopes (Godfrey et al., 2008; Crowley et al., 2011; Muchlinski et al., 2011; Godfrey et al., 2012). Morphological features of the dentition (Seligsohn and Szalay, 1974) and ancient DNA (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 the idea drawn from the study of fossil pollen and other data that southwestern Madagascar was wetter in the recent past than it is and Sourdat, 1972; Burney, 1993; Goodman and today (Mahe Rakotozafy, 1997; Goodman and Jungers, 2014). Ring-tailed lemurs, which thrive today at Tsimanampetsotsa, do so in part because they consume many leaves of succulent (CAM) plants (Loudon et al., 2008; LaFleur, M. 2012). Pachylemur stands in striking contrast; there is little evidence for CAM plant consumption in this animal (Crowley et al., 2011). Among the many reasons why the submerged caves of Tsimanampetsotsa hold special scientific promise, three are outstanding. First, as a natural, seemingly indiscriminate aggregator of animal remains, the caves of Aven, Malaza Manga and Mitoho are likely to produce a solid picture of local, past biodiversity. Prior paleonto^thie, 1934; MacPhee expedition, logical expeditions (Perrier de la Ba described by Goodman and Jungers (2014) had revealed the
A.L. Rosenberger et al. / Journal of Human Evolution 81 (2015) 83e87
presence of Megaladapis and other megafauna, including elephant birds, 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 Indian civets) and extinct, archaic subfossils indicates a temporal overlap with humans in the region. Many of the radiometric dates on subfossils from other sites in the southwest fall in the “human period.” Evidence of people in southwestern Madagascar extends more than 2000 years (Burney, 1993; Crowley, 2010); a single dated elephant bird eggshell from Mitoho Cave has a calibrated age of 4480 BP (Crowley, 2010). Third, caves such as Aven differ from typical dry cave deposits on the island where there is little or no stratigraphic control. Technical difficulties notwithstanding, Aven may produce a temporal profile that will lay out the timing of the story of Madagascar's megafaunal disappearance, in connection with environmental change and human-induced ecological disruption. Although humans are widely considered to be the primary trigger of these extinctions (Burney et al., 2003), the relative contributions of climate change and human activities to this ecological transformation are still contested (e.g., Virah-Sawmy et al., 2009). Previous work on the small mammal and avian fauna of southwestern Madagascar has demonstrated that small animals can be an important tool in reconstructing paleoecological history (e.g., Muldoon et al., 2009; Muldoon, 2010; Goodman et al., 2013). The abundant remains within Aven and other flooded caves may thus provide a new level of empirical detail bearing on the driving forces behind the megafaunal holocaust that brought down Madagascar's unique fauna and flora.
Acknowledgments This project was conducted under a collaborative accord for paleobiological and paleoclimatological research between the University of Antananarivo (Department of Biological Anthropology and Paleontology) and the University of Massachusetts (Departments of Anthropology and Geosciences), in extended collaboration with researchers at Brooklyn College, Midwestern University, and Duke University. The team included, in addition to the authors, University of Antananarivo graduate student Noromamy Rahantaharivao. The research was sanctioned by the Madagascar Ministry of Mines, the Ministry of Education, the Ministry of Arts and Culture, and Madagascar National Parks. It was supported financially by the National Science Foundation (RAPID BCS-1446959, awarded to ALR) and the National Geographic Society (9571-14, awarded to ALR, KM, LRG and GFG). It could never have been accomplished without the generosity of Walter Vauthier, proprietor of the Anakao Ocean Lodge, which served as our home base. We are indebted to officials of the various Malagasy ministries mentioned above, and without question our deepest gratitude goes to our international team of highly skilled, selfless divers who contributed freely to accomplish the mission: Ryan Dart (Madagascar), who discovered and recognized the importance of the bone accumulations; Phillip Lehman (Dominican Republic), who planned and coordinated the expedition and supported it in countless ways; cameraman Pietro Donaggio Bitner (Chile), for documenting brilliantly the setting and scientific activities; Victoria Alexandrova (Dominican Republic), Mauro Bordignon (Mexico), Kim Davidsson (Mexico), Pietro Donaggio Bitner (Chile), Hans
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Kaspersetz (USA), and Patrick Widmann (Mexico), for their generosity, 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 southwestern Madagascar. Quat. Res. 40, 98e106. Burney, D.A., Robinson, G.S., Burney, L.P., 2003. Sporormiella and the late Holocene extinctions. Proc. Natl. Acad. Sci. 100, 10800e10805. Crowley, B.E., 2010. A refined chronology of prehistoric Madagascar and the demise of the megafauna. Quat. Sci. Rev. 29, 2591e2603. Crowley, B.E., Godfrey, L.R., Irwin, M.T., 2011. A glance to the past: subfossils, stable isotopes, 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.), Elwyn Simons: A Search for Origins. Springer, New York, pp. 361e395. Godfrey, L.R., Winchester, J.M., King, S.J., Boyer, D.M., Jernvall, J., 2012. Dental topography 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 in western and southwestern Madagascar: A paleoenvironmental reconstruction. In: Goodman, S.M., Patterson, B.D. (Eds.), Natural Change and Human Impact in Madagascar. Smithsonian Institution Press, Washington D.C., pp. 257e279. Goodman, S.M., Raherilalao, M.J., Muldoon, K.M., 2013. Bird subfossils from Ankilitelo Cave: inference about historical environmental changes in southwestern Madagascar. 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 lemur traits. Ph.D. Dissertation. University of Colorado, Boulder. Loudon, J.E., Whitelaw, D.C., Sponheimer, M., Sauther, M.L., Cuozzo, F.P., 2008. Lemurs eating isotopes: A stable isotope analysis of ring-tailed lemurs (Lemur catta) and their menu at the Beza Mahafaly Special Reserve. Am. J. Phys. Anthropol. 135 (Suppl 46), 142. , J., Sourdat, M., 1972. Sur l'extinction des verte bre s subfossiles et l’arMahe ol. France 14, idification du climat dans le Sud-ouest de Madagascar. Bull. Soc. Ge 295e309. Muchlinski, M.N., Godfrey, L.R., Muldoon, K.M., Tongasoa, L., 2011. Evidence for dietary niche separation based on infraorbital foramen size variation among subfossil lemurs. Folia Primatol. 81, 330e345. Muldoon, K.M., DeBlieux, D.D., Simons, E.L., Chatrath, P.S., 2009. The subfossil occurrence and paleoecological significance of small mammals at Ankilitelo cave, southwestern Madagascar. J. Mammal. 90, 1111e1131. Muldoon, K.M., 2010. Paleoenvironment of Ankilitelo Cave (late Holocene, southwestern Madagascar): implications for the extinction of giant lemurs. J. Hum. Evol. 58, 338e352. ^thie, H., 1934. Au sujet de l’a ^ge de la faune a Aepyornis et hippoPerrier de la Ba m. Acad. Malgache 17, 162e168. potames. Me Richards, D.A., Dorale, J.A., 2003. Uranium-series chronology and environmental applications of speleothems. Rev. Mineral. Geochem. 52, 407e460. Rosenberger, A.L., Cooke, S.B., Rímoli, R., Ni, X., Cardoso, L., 2011. First skull of Antillothrix 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 in Lemur and Varecia: their bearing on the systematics of living and fossil primates. 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’: extinction dynamics 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.
