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Strontium isotopes support low mobility for Lemuriformes Brooke E. Crowley Laurie R. Godfrey Madagascar 4th largest island on the planet. Highly variable climate and topography lead to quite diverse biomes. Flora and fauna found nowhere else on the planet Euplerid carnivores Tenrecs Lemurs Chameleons Arthropods Who are the lemurs? >100 species. Diversity of ecologies but all are relatively small-bodied and weigh <10 kg. Who were the lemurs?Who were the lemurs? Palaeopropithecus ~41.5-46 kg Megaladapis Palaeopropithecus ~41-46 kg ~46-85 kg Mesopropithecus Megaladapis 10-14 kg ~46.5-85 kg MegaladapisHadropithecus ~35 kg Palaeopropithecus ~41-46 kg ~46-85 kg PachylemurIndrisLemur ~7 kgillustrations used with permission from Stephen Nash/ CI International. 11.5-13.5 kg Hadropithecus ~35 kg Microcebus <100 g Archaeoindris IndrisInrdriLemur ~7~7 kgkgillustrations used with permission from Stephen~162 kg Nash/ CI International. Hadropithecus ~35 kg Microcebus <100 Archaeoindrisg ~ 162 kg ArchaeolemurArchaeolemur ~18-26~18-26.5 kgkg Jungers et al. 2008; Images by Stephen Nash/CI International Sussman 2003; Jungers et al. 2008; Images by Stephen Nash/ CI International Jungers et al. 2008; Images by Stephen Nash/ CI International Archaeoindris ~ 162 kg Archaeolemur ~18-26 kg Jungers et al. 2008; Images by Stephen Nash/ CI International Who were the lemurs? Palaeopropithecus spp. • Understanding the ecological roles that now-extinct species played is critical for making conservation and management decisions regarding Madagascar’s remaining biodiversity. • We have learned a lot about the now-extinct taxa over the years, including estimated body masses, locomotion patterns, and reconstructed diets. • However, we do not have a good handle on how mobile they may have been. Megaladapis spp. Expectations and Predictions Mobility Body Size Smaller-bodied Larger-bodied Habit/locomotion Arboreal Terrestrial Diet Folivores; “generalist” herbivores Frugivores; omnivores Habitat Dense/closed forest Open/arid habitat Among mammals (and anthropoid primates specifically), there are a number of factors that affect home ranges. Body size is the primary control but factors are likely inter-related. Reviewed in Milton and May (1976) Nature Available Taxa Eight lemur genera are particularly well-represented in subfossil deposits Extant Extinct Propithecus Megaladapis 3.0-6.5 kg 46.5-85 kg Eulemur Palaeopropithecus 1.1-2.5 kg 41.5-46 kg Lemur Archaeolemur ~2.2 kg 18-26.5 kg Lepilemur Pachylemur 0.5-1.0 kg 11.5-13.5 kg Smith and Jungers (1976); Jungers et al. (2008); Godfrey et al. (2006); Muchlinksi et al. (2011); Godfrey et al. (2012) AJPA Expectations and Predictions Mobility Propithecus Lemur Lepilemur 3.0-6.5 kg ~2.2 kg 0.5-1.0 kg 2.4-9.0 ha 5.7-7.4 ha 0.24 ha Eulemur 1.1-2.5 kg 0.88 ha Based on body size, diet, and habit, we would expect relative mobility to vary slightly among our four extant taxa. Observed home ranges align reasonably well with these expectations Reviewed in Milton and May (1976) Nature Expectations and Predictions Mobility Propithecus Lemur Lepilemur 3.0-6.5 kg ~2.2 kg 0.5-1.0 kg 2.4-9.0 ha 5.7-7.4 ha 0.24 ha Eulemur 1.1-2.5 kg Megaladapis 46.5-85 kg 0.88 ha Palaeopropithecus Based on trends observed for primates as a 41.5-46 kg whole, we might expect that now-extinct Archaeolemur large-bodied lemurs had larger home ranges 18-26.5 kg Pachylemur than extant smaller-bodied taxa. 11.5-13.5 kg Reviewed in Milton and May (1976) Nature Expectations and Predictions Mobility Propithecus Lemur Lepilemur 3.0-6.5 kg ~2.2 kg 0.5-1.0 kg 2.4-9.0 ha 5.7-7.4 ha 0.24 ha Eulemur Megaladapis 1.1-2.5 kg 46.5-85 kg 0.88 ha Palaeopropithecus 41.5-46 kg Expectations change if we consider diet and postcranial Archaeolemur 18-26.5 kg anatomy/locomotion. Pachylemur 11.5-13.5 kg Godfrey et al. (2006) in Lemurs: Ecology and Adaptation; Walker et al. (2008) Evol Anthropol; Hogg et al. (2015) PLoS ONE Expectations and Predictions Mobility Propithecus Lemur Lepilemur 3.0-6.5 kg ~2.2 kg 0.5-1.0 kg 2.4-9.0 ha 5.7-7.4 ha 0.24 ha Eulemur Megaladapis 1.1-2.5 kg 46.5-85 kg 0.88 ha Palaeopropithecus vidence that extinct taxa were relatively inactive: 41.5-46 kg - Brain size Archaeolemur - Semicircular canal radii 18-26.5 kg - Retzius periodicity Pachylemur 11.5-13.5 kg Godfrey et al. (2006) in Lemurs: Ecology and Adaptation; Walker et al. (2008) Evol Anthropol; Hogg et al. (2015) PLoS ONE Expectations and Predictions But… multiple lines of evidence that all extinct taxa were relatively inactive - Brain size - Semicircular canal radii - Retzius periodicity We can use 87Sr/86Sr to compare mobility among co-occurring taxa. More mobile taxa should have more variable strontium isotope ratios (87Sr/86Sr). Strontium Isotopes (87Sr/86Sr) • Strontium (Sr) isotopes (87Sr/86Sr) in animal tissues can track foraging and movement of individuals across climatically homogenous landscapes (unlike C, N, O, or H isotopes). • Primarily affected by geology. 86Sr is non-radiogenic; 87Sr is produced by decay of 87Rb. Abundance of 87Sr is thus determined by the age and original 87Rb content of parent rock. Low 87Sr/86Sr High 87Sr/86Sr 0.70 0.80 Younger Older Mafic igneous (e.g., basalt) Felsic igneous (e.g., granite) Carbonates Clastics (e.g., shale) Sr2+ is incorporated into plants and animal skeletal tissues with minimal fractionation (substitutes for Ca2+). As rocks weather, they release Sr2+ into soils and water. Madagascar is ideally suited for a Sr-based approach Geologically complex! > 3 billion years of time preserved in the island’s rocks Proximal geologies differ in chemistry and age. Currently only two sites have reasonably robust sample size for both extant and extinct lemur genera. N Adapted from Roig et al. (2012) Ampasambazimba 10 km Madagascar is ideally suited for a Sr-based approach Ankilitelo Geologically complex! > 3 billion years of time preserved in the island’s rocks Proximal geologies differ in chemistry and age.Sedimentary 10 km Igneous & Metamorphic Quaternary alluvium Quaternary cuirasse/hardground Eocene limestone, shaley Limestone Qalv Ankilitelo/Mikoboka map c5-6 Taolambiby Eocene limestone, oolitic limestone, and sandstone e4 Upper Cretaceous basalt, basanite, and sakalavite Upper Cretaceous sandstone, shale, marl, coquina, and chalk Qcs River Fault N 10 km10 km10 km Mikoboka/Ankilitelo (a series of sinkholes in a limestone plateau) Adapted from Roig et al. (2012) Madagascar is ideally suited for a Sr-based approach Ampasambazimba Geologically complex! > 3 billion years of time preserved in the island’s rocks 10 km Proximal geologies differ in chemistry and age. Quaternary alluvium Akm3 Akm2 Miocene to Pleistocene basalt, basanite, and ankaratrite At18 Miocene to Pleistocene rhyolite, trachyte, phonolite, ignimbrite Akm2 Ediacaran to Cambrian granite, monzonite, and undifferentiated syenite Ankilitelo Qalv Akm3 Ediacaran to Cambrian stratified granite and syenite At1 Cryogenien paragneiss and schist At1 At18 Neoarchaean granitic to granodioritic migmatitic orthogneiss Vmpm 10 km River Fault Shear zone N Ampasambazimba 10 km Ampasambazimba (wetland underlain by a variety igneous and metamorphic rocks) Adapted from Roig et al. (2012) Taolambiby 10 km Ankilitelo 10 km10 km 10 km Taolambiby 10 km Results Mikoboka/Ankilitelo c2 =7.02, df = 6, p = 0.32 Palaeopropithecus There are no differences in variance or median Bartlett = 0.33 87Sr/86Sr between extinct and extant taxa. Sr 86 Sr/ A single Palaeopropithecus has an elevated 87 87Sr/86Sr compared to other individuals. It is an outlier for the genus, but not the Extinct lemur Extant Extinct group. c2 =0.09, df = 1, p = 0.76 Lemur Eulemur Bartlett = 0.14 Lepilemur Propithecus Megaladapis Archaeolemur Palaeopropithecus Asterisks (*) = non-Ankilitelo sites on the Mikoboka plateau. Results Mikoboka/Ankilitelo c2 =7.02, df = 6, p = 0.32 Palaeopropithecus Bartlett = 0.33 Sr 86 Sr/ 87 Extant Extinct c2 =0.09, df = 1, p = 0.76 Lemur Eulemur Bartlett = 0.14 Lepilemur Propithecus Megaladapis Archaeolemur Palaeopropithecus Asterisks (*) = non-Ankilitelo sites on the Mikoboka plateau. Results Excluding the Palaeoprpithecus Mikoboka/Ankilitelo does not affect results. c2 = 9.75, df = 6, p = 0.14 Palaeopropithecus Bartlett p = 0.41 Sr 86 Sr/ 87 Extant Extinct c2 = 0.51, df = 1, p = 0.47 Lemur Eulemur Bartlett p = 0.12 Lepilemur Propithecus Megaladapis Archaeolemur Palaeopropithecus Asterisks (*) = non-Ankilitelo sites on the Mikoboka plateau. Ampasambazimba 10 km Ankilitelo 10 km Results Qalv c5-6 Taolambiby Ankilitelo/Mikoboka Mikoboka/Ankilitelo Qcs map e4 c2 =7.02, df = 6, p = 0.32 Palaeopropithecus Bartlett = 0.33 10 km 10 km10 km Sr 86 Sr/ 87 Extant Extinct Lemur Eulemur Lepilemur 87 86 Propithecus Sr/ Sr for all individuals Megaladapis Archaeolemur consistent with local geology. Palaeopropithecus Outlier Palaeopropithecus could have foraged on Quaternary seds. It may have fallen into the sinkhole on its own, or it may have been dropped by a predator(e.g., now-extinct eagle). Ampasambazimba 10 km Ankilitelo 10 km J.P. Wallace et al. Results Qalv Taolambiby c5-6 Precipitation & dustMikoboka/Ankilitelo Qcs e4 c2 =7.02, df = 6, p = 0.32 Palaeopropithecus Bartlett = 0.33 10 km 10 km10 km Sr 86 Sr/ 87 Sea spray Atmospheric dust and aerosols Surface geology Bedrock Extant Extinct Fig. 3. Schematic showing anticipated sources of bioavailable strontium in Miocene Florida. The influence of marine-derived strontium should be highest closest to Lemur 87 86 87 86 the coast. Vegetation rooting depth (arrows) mayApparent differences in also influence Sr/ Sr; whereas weathering bedrock should beSr/ the dominantSr among source for deep-rooted trees, grassesEulemur with shallow root systems may be more susceptible to atmospherically deposited strontium.
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  • Ancient DNA from Giant Extinct Lemurs Verifies Single Origin of Malagasy

    Ancient DNA from Giant Extinct Lemurs Verifies Single Origin of Malagasy

    Ancient DNA from giant extinct lemurs confirms single origin of Malagasy primates K. Praveen Karanth†‡, Thomas Delefosse§, Berthe Rakotosamimanana¶, Thomas J. Parsonsʈ, and Anne D. Yoder†‡†† †Department of Ecology and Evolutionary Biology, Yale University, P.O. Box 208105, New Haven, CT 06520; §Laboratoire Codgene, 11 Rue Humann, 67085 Strasbourg, France; ¶34 Cite´ des Professeurs, Fort-Duchesne, Antananarivo 101, Madagascar; and ʈArmed Forces DNA Identification Laboratory, The Armed Forces Institute of Pathology, 1413 Research Boulevard, Rockville, MD 20850 Edited by Elwyn L. Simons, Duke University Primate Center, Durham, NC, and approved February 8, 2005 (received for review November 9, 2004) The living Malagasy lemurs constitute a spectacular radiation of >50 species that are believed to have evolved from a common ancestor that colonized Madagascar in the early Tertiary period. Yet, at least 15 additional Malagasy primate species, some of which were relative giants, succumbed to extinction within the past 2,000 years. Their existence in Madagascar is recorded predominantly in its Holocene subfossil record. To rigorously test the hypothesis that all endemic Malagasy primates constitute a monophyletic group and to determine the evolutionary relationships among living and extinct taxa, we have conducted an ancient DNA analysis of subfossil species. A total of nine subfossil individuals from the extinct genera Palaeopropithecus and Megaladapis yielded ampli- fiable DNA. Phylogenetic analysis of cytochrome b sequences derived from these subfossils corroborates the monophyly of endemic Malagasy primates. Our results support the close rela- tionship of sloth lemurs to living indriids, as has been hypothesized on morphological grounds. In contrast, Megaladapis does not show a sister-group relationship with the living genus Lepilemur.