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A Glance to the Past: Subfossils, Stable Isotopes, Seed Dispersal, and Lemur Species Loss in Southern Madagascar

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A Glance to the Past: Subfossils, Stable Isotopes, Seed Dispersal, and Lemur Species Loss in Southern Madagascar American Journal of Primatology 73:25–37 (2011) RESEARCH ARTICLE A Glance to the Past: Subfossils, Stable Isotopes, Seed Dispersal, and Lemur Species Loss in Southern Madagascar 1 2Ã 3 BROOKE E. CROWLEY , LAURIE R. GODFREY , AND MITCHELL T. IRWIN 1Department of Anthropology, University of Toronto, Toronto, Ontario, Canada 2Department of Anthropology, University of Massachusetts, Amherst, Massachusetts 3Redpath Museum, McGill University, Montreal, Quebec, Canada The Spiny Thicket Ecoregion (STE) of Southern and southwestern Madagascar was recently home to numerous giant lemurs and other ‘‘megafauna,’’ including pygmy hippopotamuses, giant tortoises, elephant birds, and large euplerid carnivores. Following the arrival of humans more than 2,000 years ago, dramatic extinctions occurred. Only one-third of the lemur species which earlier occupied the STE survive today; other taxa suffered even greater losses. We use stable isotope biogeochemistry to reconstruct past diets and habitat preferences of the recently extinct lemurs of the STE. We show that the extinct lemurs occupied a wide range of niches, often distinct from those filled by coeval non- primates. Many of the now-extinct lemurs regularly exploited habitats that were drier than the gallery forests in which the remaining lemurs of this ecoregion are most often protected and studied. Most fed predominantly on C3 plants and some were likely the main dispersers of the large seeds of native C3 trees; others included CAM and/or C4 plants in their diets. These new data suggest that the recent extinctions have likely had significant ecological ramifications for the communities and ecosystems of Southern and southwestern Madagascar. Am. J. Primatol. 73:25–37, 2011. r 2010 Wiley-Liss, Inc. Key words: seed dispersal; stable isotope; subfossil lemur; Spiny Thicket Ecoregion INTRODUCTION Winter, 1979]. Additionally, there are patches of endemic or native C4 grasses [Bond et al., 2008; If there is any tropical location on earth where Bosser, 1969]. C3 trees also thrive in the STE; these one might be surprised to see nonhuman primates too may have extreme adaptations to aridity, such as that place would be the ‘‘Spiny Thicket Ecoregion’’ swollen trunks or roots for water storage, or reduced (STE) of Southern and southwestern Madagascar leaves. Whereas many of the CAM plants have tiny [Burgess et al., 2004]. This ‘‘spiny desert’’ covers seeds that are adapted for wind dispersal, some C3 44,300 km2, extending from the Mangoky River on trees have large seeds that are adapted for dispersal the west coast to the Anosyennes Mountain chain in via endozoochory. the southeast. Owing to an extreme rain shadow Today, half a dozen lemur species belonging to effect, the STE dry season lasts up to 11 months of four families inhabit the STE. Four of these, ranging the year, and in the driest areas, annual rainfall may in size from 60 g to slightly more than 3 kg, are not exceed 350 mm. Its vegetation is diverse, and common. In the recent past, there were eight varies depending on water sources and the porosity additional lemur species, ranging in size from just and chemistry of the soils [DuPuy & Moat, 1996]. It over 10 kg (Mesopropithecus globiceps and Pachylemur includes grasslands, spiny bush, bushy scrub, and insignis)toaround85kg(Megaladapis edwardsi). denser (but usually narrow) gallery or riparian forests bordering streams or rivers, few of which are perennial. The more open ‘‘spiny’’ forests are usually Contract grant sponsor: NSF; Contract grant number: 0129185; only 3–6 m in height, with rare emergent trees Contract grant sponsors: David and Lucille Packard Foundation; exceeding 10 m, creating a discontinuous canopy. John Simon Guggenheim Foundation; Nancy Skinner Clark This ecoregion is renowned for its unusual flora Vassar Graduate Fellowship. with special adaptations to store water or minimize ÃCorrespondence to: Laurie R. Godfrey, Department of Anthro- water loss. Plant endemism is higher here than pology, 240 Hicks Way, University of Massachusetts, Amherst, MA 01003. E-mail: [email protected] anywhere else in Madagascar [Burgess et al., 2004]. Received 17 August 2009; revised 26 January 2010; revision The most dominant plants are succulents (Didier- accepted 27 January 2010 eaceae, Crassulaceae, and Euphorbiaceae) that use DOI 10.1002/ajp.20817 the Crassulacean Acid Metabolism (CAM) photosyn- Published online 4 March 2010 in Wiley Online Library (wiley thetic pathway [Kluge et al., 1991, 1995, 2001; onlinelibrary.com). r 2010 Wiley-Liss, Inc. 26 / Crowley et al. These species belonged to Madagascar’s famed ‘‘mega- Many lighter elements, such as carbon and nitrogen, fauna,’’ known through their bony remains at ‘‘sub- have isotopes that are stable and do not radioactively fossil’’ (late Pleistocene and Holocene) sites decay. A standardized ‘‘d’’ notation is used to refer to throughout the island. The megafauna, which also the relative proportion of heavy-to-light isotopes, 13 12 included giant ratites, giant tortoises, and pygmy where d 5 ((Rsample/Rstandard)-1)Ã1,000, and R 5 C/ C hippopotamuses, disappeared after humans arrived or 15N/14N. Values are measured in parts per roughly around 2,000 years ago [Burney et al., 2004]. thousand (%). The standards for carbon and nitro- All Madagascar’s extant lemur families (Cheirogalei- gen, respectively, are Pee Dee Belemnite (a marine dae, Lepilemuridae, Indriidae, Lemuridae, and Dau- carbonate fossil) and air. The different number of bentoniidae) and extinct families (Megaladapidae, neutrons in isotopes of the same element results in Palaeopropithecidae, and Archaeolemuridae) are re- different masses, causing each isotope to behave presented in subfossil deposits throughout the STE. slightly differently during chemical and physical Burney et al. [2003] have shown that pre- reactions; these differences lead to relatively more settlement megafaunal biomass was high in what or less heavy isotope in different materials. When were then open areas, likely reflecting an abundance relatively more of the heavy isotope is present, the of giant tortoises, pygmy hippopotamuses, and ‘‘d’’ value is higher; when relatively less is present, it elephant birds. However, the remains of giant is lower. lemurs have been found alongside those of non- primates, and the extent to which primates were key elements of the various ecosystems of the extreme Carbon South and Southwest is unknown. Although extant Carbon isotope ratios have been used to differ- species have mainly been studied in gallery forests entiate C3 and C4 plants, or the relative contribution (e.g. Beza Mahafaly Special Reserve Parcel I; of these plant groups to animal diets. Carbon isotope Berenty), lemurs survive today in the STE outside ratios for C3 and C4 plants range from À21 to À35% the gallery forests, and giant lemurs may have done (average À28%), and from À10 to À20% (average the same. Furthermore, whereas there is clear À14%), respectively [O’Leary, 1988]. Plants utilizing anatomical evidence that even the largest-bodied the CAM photosynthetic pathway have intermediate extinct lemurs were adept tree-climbers [Godfrey d13C values, depending on the degree of succulence et al., 2006], none could have been strictly arboreal, and water stress [Ehleringer & Monson, 1993]. even in gallery forests. At Beza Mahafaly, which Nonphotosynthetic plant tissues, such as fruits has both gallery and spiny forest habitats, three and flowers, tend to have d13C values 1–1.5% higher of the four locally surviving lemur species (Lemur than leaves [Codron et al., 2005; Cernusak et al., catta, ring-tailed lemur; Propithecus verreauxi, 2009], but this pattern has not been observed in Verreaux’s sifaka; and Microcebus griseorufus, Madagascar’s dry forests [Crowley et al., submitted; grey-brown mouse lemur) regularly descend to the Dammhahn & Kappeler, 2009]. Collagen d13C values ground [Brockman et al., 2008; Youssouf Jacky & in herbivores are roughly 5% higher than those in Rasoazanabary, 2008]. Only the sportive lemur, consumed plants, and consumers that eat animal Lepilemur leucopus, is strictly arboreal. matter should have slightly higher d13C values than Here, we use stable isotope biogeochemistry to sympatric herbivores [Koch, 1998]. explore lemur paleoecology in the STE. Specifically, Average foliar d13C values for C3 and CAM we investigate whether the extinct lemurs of this plants from the gallery forest at Beza Mahafaly are region occupied niches likely not filled by sympatric À29.672.6% and À15.370.9%, respectively, and species and how their loss may have affected plant their ranges do not overlap (from À37.3 to À23.5% communities. Stable isotope ratios can be expected to for C3 plants, and from À17.0 to À13.2% for CAM differ among animals belonging to different trophic plants) [Crowley et al., submitted]. Carbon isotope groups, consuming plants using different photosyn- ratios have not been measured for any C4 plants thetic pathways or living in different habitats. We from the Beza region, but their d13C values should be suggest that, by carefully combining what have higher than those in CAM plants. Assuming a hitherto been rather separate fields—subfossil lemur fractionation of ca. 5% between lemurs and plants paleobiology, isotope geochemistry, lemur ecology, [Crowley et al., submitted; Koch, 1998; Krueger & and floristic surveys of Madagascar’s habitats—we Sullivan, 1984], lemurs eating pure C3 plant diets in might be able to unravel traces of the still-reverber- gallery forest habitat should on average
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