Karen E. Samonds

Teeth, brains, and primate life histories

This paper explores the correlates of variation in dental development across the order Primates. We are particularly interested in how 1) dental precocity (percentage of total postcanine primary and secondary teeth that have erupted at selected absolute ages and life cycle stages) and 2) dental endowment at weaning (percentage of adult postcanine occlusal area that is present at weaning) are related to variation in body or brain size and diet in primates. We ask whether folivores have more accelerated dental schedules than do like-sized frugivores, and if so, to what extent this is part and parcel of a general pattern of acceleration of life histories in more folivorous taxa. What is the adaptive significance of variation in dental eruption schedules across the order Primates? We show that folivorous primate species tend to exhibit more rapid dental development (on an absolute scale) than comparably sized frugivores, and their dental development tends to be more advanced at weaning. Our data affirm an important role for brain (rather than body) size as a predictor of both absolute and relative dental development. Tests of alternative dietary hypotheses offer the strongest support for the foraging independence and food processing hypotheses.

Spatial and temporal arrival patterns of Madagascar's vertebrate fauna explained by distance, ocean currents, and ancestor type

How, when, and from where Madagascars vertebrates arrived on the island is poorly known, and a comprehensive explanation for the distribution of its organisms has yet to emerge. We begin to break that impasse by analyzing vertebrate arrival patterns implied by currently existing taxa. For each of 81 clades, we compiled arrival date, source, and ancestor type (obligate freshwater, terrestrial, facultative swimmer, or volant). We analyzed changes in arrival rates, with and without adjusting for clade extinction. Probability of successful transoceanic dispersal is negatively correlated with distance traveled and influenced by ocean currents and ancestor type. Obligate rafters show a decrease in probability of successful transoceanic dispersal from the Paleocene onward, reaching the lowest levels after the mid-Miocene. This finding is consistent with a paleoceanographic model [Ali JR, Huber M (2010) Nature 463:653–656] that predicts Early Cenozoic surface currents periodically conducive to rafting or swimming from Africa, followed by a reconfiguration to present-day flow 15–20 million years ago that significantly diminished the ability for transoceanic dispersal to Madagascar from the adjacent mainland.

Dental microstructure and life history in subfossil Malagasy lemurs

When compared with their recently extinct relatives, living lemurs represent a mere fraction of a broad radiation that occupied unique niches in the recent past. Among living lemurs, indrids exhibit the fastest rates of dental development. This dental precocity is tightly correlated with rapid pace of postnatal dental eruption, early replacement of the deciduous teeth, high dental endowment at weaning, and relatively slow somatic growth. This pattern is in stark contrast to that seen in extant lemurids, where somatic development is highly accelerated and dental development is relatively slow. We report on the pace of dental development in one species of palaeopropithecid, the sister group to extant indrids. Like much smaller modern indrids, the chimpanzee-sized Palaeopropithecus ingens was dentally precocious at birth as evidenced by the advanced state of molar crown formation. This finding implies a pattern characteristic of Propithecus and other indrids—rapid dental development despite relatively prolonged gestation. Gestation length in this one species of subfossil lemur was likely greater than 9 months. Our results demonstrate that large body size in primates does not preclude exceedingly rapid dental development.

Imperfect Isolation: Factors and Filters Shaping Madagascar's Extant Vertebrate Fauna

Analyses of phylogenetic topology and estimates of divergence timing have facilitated a reconstruction of Madagascar’s colonization events by vertebrate animals, but that information alone does not reveal the major factors shaping the island’s biogeographic history. Here, we examine profiles of Malagasy vertebrate clades through time within the context of the island’s paleogeographical evolution to determine how particular events influenced the arrival of the island’s extant groups. First we compare vertebrate profiles on Madagascar before and after selected events; then we compare tetrapod profiles on Madagascar to contemporary tetrapod compositions globally. We show that changes from the Mesozoic to the Cenozoic in the proportions of Madagascar’s tetrapod clades (particularly its increase in the representation of birds and mammals) are tied to changes in their relative proportions elsewhere on the globe. Differences in the representation of vertebrate classes from the Mesozoic to the Cenozoic reflect the effects of extinction (i.e., the non-random susceptibility of the different vertebrate clades to purported catastrophic global events 65 million years ago), and new evolutionary opportunities for a subset of vertebrates with the relatively high potential for transoceanic dispersal potential. In comparison, changes in vertebrate class representation during the Cenozoic are minor. Despite the fact that the island’s isolation has resulted in high vertebrate endemism and a unique and taxonomically imbalanced extant vertebrate assemblage (both hailed as testimony to its long isolation), that isolation was never complete. Indeed, Madagascar’s extant tetrapod fauna owes more to colonization during the Cenozoic than to earlier arrivals. Madagascar’s unusual vertebrate assemblage needs to be understood with reference to the basal character of clades originating prior to the K-T extinction, as well as to the differential transoceanic dispersal advantage of other, more recently arriving clades. Thus, the composition of Madagascar’s endemic vertebrate assemblage itself provides evidence of the islands paleogeographic history.

LEMUR LATRINES: OBSERVATIONS OF LATRINE BEHAVIOR IN WILD PRIMATES AND POSSIBLE ECOLOGICAL SIGNIFICANCE

Latrine behavior, or the preferential, repeated use of 1 or more specific defecation sites, is well known among mammals and believed to function in olfactory communication among individuals or groups in many circumstances. Primates have reduced their capacity for olfaction in favor of more developed visual systems; however, several prosimian primates regularly use olfactory communication for transmission of social signals, most often using scent gland secretions and urine. Latrine behaviors have been described rarely in primates and have traditionally not been included in reviews of primate olfactory communication, yet we found ample evidence that certain primate species habitually use latrine sites for defecation. Here we review the previous evidence for latrine use in primates and report new and more extensive observations of latrine use in 2 lemuriform primates (Lepilemur sp. and Hapalemur griseus). Based on these new observations, we present and evaluate 4 available hypotheses for the function of latrines (advertisement of sexual cycling, predation avoidance, intragroup spacing, and intergroup resource defense) in lemur taxa for which sufficient evidence of latrine use exists. In all cases, intergroup resource defense is the function most consistent with available observations.

Schultz’s Unruly Rule: Dental Developmental Sequences and Schedules in Small-Bodied, Folivorous Lemurs

Schultz’s rule (as reconstructed by Smith) states that there is a relationship between the pattern (or relative order) of eruption of molar versus secondary (replacement) teeth and the overall pace (or absolute timing) of growth and maturation. Species with ‘fast’ life histories (rapid dental development, rapid growth, early sexual maturation, short life spans) are said to exhibit relatively early eruption of the molars and late eruption of the secondary replacement teeth (premolars, canines, incisors), whereas species with ‘slow’ life histories are said to exhibit relatively late eruption of the molars and early eruption of the secondary dentition. In a recent review, B.H. Smith noted that primates with tooth combs might violate this rule because tooth combs tend to erupt early, regardless of the pace of life history. We show that exceptions to Schultz’s rule among lemurs are not limited to the relative timing of eruption of the tooth comb. Rather, among lemurs, some species with extremely accelerated dental development exhibit a pattern of eruption of molars and of secondary teeth in direct opposition to the expectations of Schultz’s rule. We focus particularly on the pattern (order) and pace (absolute timing) of dental development and eruption in Avahi and Lepilemur – two relatively small, nocturnal folivores with rapid dental development. These taxa differ markedly in their eruption sequences (the premolars erupt after M2 and M3 in Lepilemur but not Avahi ). We offer an explanation for the failure of Schultz’s rule to predict these differences. Schultz’s rule presumes that eruption timing is dependent on the size of the jaw and that, therefore, molar crown formation and eruption will be delayed in species with slow-growing jaws. We show that a variety of processes (including developmental imbrication) allows the crowns of permanent teeth to form and to erupt into jaws that might appear to be too small to accommodate them.

Variation in physiological health of diademed sifakas across intact and fragmented forest at Tsinjoarivo, Eastern Madagascar.

As undisturbed habitat becomes increasingly rare, managers charged with ensuring the survival of endangered primate species must increasingly utilize disturbed and degraded habitats in species survival plans. Yet we have an imperfect understanding of the true long‐term viability of primate populations in disturbed habitat, and census data can be misleading because density is not necessarily correlated with habitat quality and population viability in predictable ways. Here we present clinical laboratory data on hematology, serum biochemistry, fat‐soluble vitamins, minerals, iron analytes, viral serology, and parasitology of diademed sifaka (Propithecus diadema), derived from the capture of 26 individuals spanning eight groups and two habitats (undisturbed vs. disturbed and fragmented) at Tsinjoarivo, Madagascar. Blood from fragment individuals had significantly lower values for several factors: white blood cell counts, bilirubin, total protein, albumin, calcium, sodium, chloride, manganese, zinc, iron and total iron‐binding capacity. Several biochemical variables were higher in immature individuals, probably due to active growth. The large number of interhabitat differences suggests that habitat disturbance has an impact on physiological health within this population, perhaps reflecting dietary stress and/or immunosuppression. These results, combined with previous data showing altered diet, slower juvenile growth, and reduced activity in disturbed forest fragments, suggest that fragment sifakas may be less healthy than continuous forest groups. Finally, Tsinjoarivo sifakas have extremely low blood urea nitrogen (perhaps reflecting protein limitation) and selenium levels relative to other lemurs. Despite their survival and reproduction in the short term in fragments, these sifakas may represent a riskier conservation investment than conspecifics in undisturbed forest, and may be more susceptible to environmental stressors. However, more data on the fitness consequences of these biochemical differences are needed for a better interpretation of their impacts on long‐term viability prospects. Am. J. Primatol. Am. J. Primatol. 72:1013–1025, 2010.

Late Pleistocene bat fossils from Anjohibe Cave, northwestern Madagascar

ABSTRACT In spite of decades of research on Madagascars unique and endemic modern fauna, the evolutionary history of the islands bat fauna remains largely unknown. Their origin and evolution is largely unknown because of the nature of the fossil record; the deepest well-dated glimpse of Madagascars mammal groups comes from only 26,000 years ago. Bat remains have frequently been recovered from paleontological sites, but have been rarely identified or described. It therefore remains unknown whether bats underwent a reduction in species diversity similar to that seen in many of Madagascars vertebrate clades. Herein I describe a collection of newly discovered subfossil bats from Anjohibe Cave, northwestern Madagascar, some estimated to have been deposited about 80,000 years ago. Five bat genera are represented as subfossil (Rousettus, Eidolon, Hipposideros, Triaenops, and Myotis) with four of these genera present in Anjohibe Cave today. The subfossil material has yielded two new species, indicating that Malagasy bats experienced recent species turnover, paralleling what is seen in much of the islands terrestrial vertebrate fauna.

Discovery of Sympatric Dwarf Lemur Species in the High-Altitude Rain Forest of Tsinjoarivo, Eastern Madagascar: Implications for Biogeography and Conservation

The number of species within the Malagasy lemur genus Cheirogaleus is currently under debate. Museum collections are spotty, and field work, supplemented by morphometric and genetic analysis, is essential for documenting geographic distributions, ecological characteristics and species boundaries. We report here field evidence for 2 dwarf lemur species at Tsinjoarivo, an eastern-central high-altitude rain forest: one, from a forest fragment, displaying coat and dental characteristics similar to C. sibreei (previously described only from museum specimens) and the other, from the continuous forest, resembling individuals of Cheirogaleus found today at Ranomafana National Park, further to the south. This study represents the first confirmation of a living population of grey-fawn, C.-sibreei-like, dwarf lemurs in Madagascar.

Stable carbon isotope values confirm a recent increase in grasslands in northwestern Madagascar

Madagascar is home to some of the world’s most unique plants and animals. Unfortunately, anthropogenic forest loss has had a dramatic impact on both floral and faunal communities. In many regions the scale and timing of this loss remains poorly constrained. Such is the case for northwestern Madagascar. Pollen records for this region suggest that fires and grass abundance increased around 1000 calendar years before present (cal. BP), as well as c. 500 cal. BP, presumably reflecting growing human settlements. However, temporal and spatial resolution for these transitions is limited by a hiatus in the sediment record. We present a suite of carbon isotope data from 14C-dated vertebrate bones from Anjohibe Cave, northwestern Madagascar. In agreement with palynological records, isotope data indicate that the transition to open savannah may be a recent phenomenon in northwestern Madagascar. We document dramatic changes in the vertebrate community over the past 2000 years. Remains from extinct taxa are all older than 1500 cal. BP, locally extirpated taxa were in the region until c. 300 years ago, and introduced species are essentially modern. Stable carbon data suggest minimal consumption of C4 resources by extinct, locally extirpated and locally extant endemic taxa. On the contrary, introduced rats and shrews exhibit exceptionally high carbon isotope values; this may reflect a dietary shift to newly introduced grasses or consumption of seeds from C4 plants.