Mid-Cenozoic climate change, extinction, and faunal turnover in Madagascar, and their bearing on the evolution of lemurs.

BACKGROUND: Was there a mid-Cenozoic vertebrate extinction and recovery event in Madagascar and, if so, what are its implications for the evolution of lemurs? The near lack of an early and mid-Cenozoic fossil record on Madagascar has inhibited direct testing of any such hypotheses. We compare the terrestrial vertebrate fauna of Madagascar in the Holocene to that of early Cenozoic continental Africa to shed light on the probability of a major mid-Cenozoic lemur extinction event, followed by an "adaptive radiation" or recovery. We also use multiple analytic approaches to test competing models of lemur diversification and the null hypothesis that no unusual mid-Cenozoic extinction of lemurs occurred. RESULTS: Comparisons of the terrestrial vertebrate faunas of the early Cenozoic on continental Africa and Holocene on Madagascar support the inference that Madagascar suffered a major mid-Cenozoic extinction event. Evolutionary modeling offers some corroboration, although the level of support varies by phylogeny and model used. Using the lemur phylogeny and divergence dates generated by Kistler and colleagues, RPANDA and TESS offer moderate support for the occurrence of unusual extinction at or near the Eocene-Oligocene (E-O) boundary (34 Ma). TreePar, operating under the condition of obligate mass extinction, found peak diversification at 31 Ma, and low probability of survival of prior lineages. Extinction at the E-O boundary received greater support than other candidate extinctions or the null hypothesis of no major extinction. Using the lemur phylogeny and divergence dates generated by Herrera & Dàvalos, evidence for large-scale extinction diminishes and its most likely timing shifts to before 40 Ma, which fails to conform to global expectations. CONCLUSIONS: While support for large-scale mid-Cenozoic lemur extinction on Madagascar based on phylogenetic modeling is inconclusive, the African fossil record does provide indirect support. Furthermore, a major extinction and recovery of lemuriforms during the Eocene-Oligocene transition (EOT) would coincide with other major vertebrate extinctions in North America, Europe, and Africa. It would suggest that Madagascar's lemurs were impacted by the climate shift from "greenhouse" to "ice-house" conditions that occurred at that time. This could, in turn, help to explain some of the peculiar characteristics of the lemuriform clade.

Challenging endocrinology students with a critical-thinking workbook.

A central goal of science education is to help students develop higher order thinking skills to enable them to face the challenges of life. Accordingly, science instructors are now urged to craft their classrooms such that they serve as not only spaces for disseminating information, but also an arena through which students are encouraged to think scientifically and develop critical-thinking skills. This project aimed to develop a workbook that helps postsecondary students learn endocrinology and engages them in critical thinking. Each of the five chapters focuses on a different topic rooted within core biological concepts relevant to endocrinology. Such topics were identified on cross-referencing seminal reports on science education. Tenants of Numrich's Sequence of Critical-Thinking Tasks were used to guide the development of chapter sections with the intent of engaging students in critical thinking over time by way of practice and scaffolded guidance. Chapter sections of modeling, event sequencing, clinical application, research and communication, and simulation, target different skills presented in Numrich's framework. Students' learning, experiences, and behaviors were used to evaluate the workbook and inform the revision of the workbook into the publicly available second edition.

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

How, when, and from where Madagascar's 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.

Ancient DNA elucidates the lost world of western Indian Ocean giant tortoises and reveals a new extinct species from Madagascar.

Before humans arrived, giant tortoises occurred on many western Indian Ocean islands. We combined ancient DNA, phylogenetic, ancestral range, and molecular clock analyses with radiocarbon and paleogeographic evidence to decipher their diversity and biogeography. Using a mitogenomic time tree, we propose that the ancestor of the extinct Mascarene tortoises spread from Africa in the Eocene to now-sunken islands northeast of Madagascar. From these islands, the Mascarenes were repeatedly colonized. Another out-of-Africa dispersal (latest Eocene/Oligocene) produced on Madagascar giant, large, and small tortoise species. Two giant and one large species disappeared c. 1000 to 600 years ago, the latter described here as new to science using nuclear and mitochondrial DNA. From Madagascar, the Granitic Seychelles were colonized (Early Pliocene) and from there, repeatedly Aldabra (Late Pleistocene). The Granitic Seychelles populations were eradicated and later reintroduced from Aldabra. Our results underline that integrating ancient DNA data into a multi-evidence framework substantially enhances the knowledge of the past diversity of island faunas.

Assessing how students value learning communication skills in an undergraduate anatomy and physiology course.

Students, particularly those in science, technology, engineering and mathematics (STEM) and healthcare-related programs, should develop proficient interpersonal skills, including communication. To help students develop effective communication skills, instructors need to consider the value students give to learning these skills. The Student Attitudes Toward Communication Skills Survey (SATCSS) was developed to measure how undergraduate students value learning communication skills based on Expectancy-Value Theory across three modes of communication (verbal, written, non-verbal). The survey was given to students interested in healthcare professions and enrolled in an undergraduate anatomy and physiology (A&P) course (n = 233) at a Midwest research active university. The survey showed evidence of validity, measuring two components: (1) "Value to Profession" (attainment and utility value) and (2) "Value to Self" (intrinsic value and cost). There was a significant difference in sub-scores among the four task values such that students thought that learning communication skills was important and relevant (high attainment and utility value) but not interesting (low intrinsic value) and costly. Students with high total scores valued communication skills across all four task values. As total value scores decreased, it was first due to students finding learning communication skills to be time prohibitive and then a lack of interest in learning communication skills. Based on these results, it is recommended that instructors incorporate communication skills training into content that is already part of their A&P course to reduce time concerns. Additional recommendations include using reflective activities and humor to increase student interest.

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.

Costly teeth? Gestation length in primates suggests that neonate dentition is not expensive to produce.

Variation in the relationship between gestation length and body mass can arise because different types of tissue require varying amounts of energy to build, and not all species build such tissues in the same proportions. Given that a pregnant female has a finite amount of energy, trade-offs between investment in different tissues may occur. Here we examine if dental precocity accounts for variation in primate gestation length. If true, this could explain why folivorous species with precocial dentition have longer gestation lengths than predicted by neonatal brain and body mass. We compiled data on gestation length, neonate and adult female body and brain mass from the literature. We used published postcanine eruption schedules at 4 months of age and measured the total occlusal area as dental endowment to approximate dental precocity at birth. Species with embryonic delay in growth or altricial neonates were not considered because they represent grade shifts regarding gestation length. Consequently, our data were biased toward Simiiformes and Old World monkeys, specifically. We performed a phylogenetic generalized least squares regression (pGLS) of neonate brain mass in relation to neonate body mass, and a second pGLS with dental endowment as an additional predictor variable. Including dental endowment in the pGLS did not improve the model. Dental endowment did not systematically impact primate gestation length. Concordant with results from previous studies, this indicates that the energetically expensive period of tooth mineralization may occur postnatally. More data are required to examine if the results are typical across primates.

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.

A middle - late Eocene neoselachian assemblage from nearshore marine deposits, Mahajanga Basin, northwestern Madagascar.

We report here the first neoselachian fossil fauna from Eocene nearshore marine deposits of the Mahajanga Basin, northwestern Madagascar. The fauna includes seven species of shark: Nebrius blankenhorni, Brachycarcharias koerti, Galeocerdo eaglesomei, two species of Carcharhinus (one of which is described as a new species), Physogaleus, Rhizoprionodon and Sphyrna. Three species of rays were also recovered: Pristis, Myliobatis and an undetermined dasyatid ray. This fauna represents the first Cenozoic neoselachian fossil record from the Eocene of Madagascar and broadens our understanding of their evolutionary and biogeographic history in the southern hemisphere during this time. Although the diversity of the genera and species of the fauna is very low, the age and similarity of genera to those in Congo, west Africa, Arabia, Asia, Europe, and North, Central, and South America suggests that these genera were broadly distributed and diverse within the shallow marine settings of the Tethyan and southern provinces during middle and late Eocene.

Morphometric signals of population decline in diademed sifakas occupying degraded rainforest habitat in Madagascar.

Anthropogenic habitat change can have varied impacts on primates, including both negative and positive outcomes. Even when behavioural shifts are seen, they may reflect decreased health, or simply behavioural flexibility; understanding this distinction is important for conservation efforts. This study examines habitat-related variation in adult and immature morphometrics among diademed sifakas (Propithecus diadema). We collected morphometric data from sifakas at Tsinjoarivo, Madagascar (19 years, 188 captures, 113 individuals). Captures spanned 12 groups, five within continuous forest ("CONT"), and seven in degraded fragments ("FRAG") where sifakas have lower nutritional intakes. Few consistent differences were found between CONT and FRAG groups. However, using home range quality as a covariate rather than a CONT/FRAG dichotomy revealed a threshold: the two FRAG groups in the lowest-quality habitat showed low adult mass and condition (wasting), and low immature mass and length (stunting). Though less-disturbed fragments apparently provide viable habitat, we suggest the sifakas in the most challenging habitats cannot evolve fast enough to keep up with such rapid habitat change. We suggest other long-lived organisms will show similar morphometric "warning signs" (wasting in adults, stunting in immatures); selected morphometric variables can thus be useful at gauging vulnerability of populations in the face of anthropogenic change.

New evidence indicates the presence of barracuda (Sphyraenidae) and supports a tropical marine environment in the Miocene of Madagascar.

Recent exploration of Miocene-age deposits at Nosy Makamby, a small island ~50 km southwest of Mahajanga city in northwestern Madagascar, has led to the recovery of a large sample [82] of isolated barracuda teeth (Sphyraena sp.). in a tropical marine fauna that also includes diverse marine invertebrates, chondrichthyans, bony fishes, turtles, crocodylians, and sirenians. Characteristically for barracudas, the teeth are labiolingually flattened and fang-like with a broadly triangular and blade-like acuminate outline and sharply edged but unserrated cutting margins. These barracudas inhabited an environment that included coral reefs (based on fossil scleractinians) and seagrass beds (evidenced by the epiphytic benthic foraminifera Elphidium sp.). The relatively common occurrence of Miocene barracuda at Nosy Makamby corroborates the presence of a tropical marine ecosystem encircling Madagascar by the Miocene, likely similar overall to the environment found there today.

A juvenile subfossil crocodylian from Anjohibe Cave, Northwestern Madagascar.

Madagascar's subfossil record preserves a diverse community of animals including elephant birds, pygmy hippopotamus, giant lemurs, turtles, crocodiles, bats, rodents, and carnivorans. These fossil accumulations give us a window into the island's past from 80,000 years ago to a mere few hundred years ago, recording the extinction of some groups and the persistence of others. The crocodylian subfossil record is limited to two taxa, Voay robustus and Crocodylus niloticus, found at sites distributed throughout the island. V. robustus is extinct while C. niloticus is still found on the island today, but whether these two species overlapped temporally, or if Voay was driven to extinction by competing with Crocodylus remains unknown. While their size and presumed behavior was similar to each other, nearly nothing is known about the growth and development of Voay, as the overwhelming majority of fossil specimens represent mature adult individuals. Here we describe a nearly complete juvenile crocodylian specimen from Anjohibe Cave, northwestern Madagascar. The specimen is referred to Crocodylus based on the presence of caviconchal recesses on the medial wall of the maxillae, and to C. niloticus based on the presence of an oval shaped internal choana, lack of rostral ornamentation and a long narrow snout. However, as there are currently no described juvenile specimens of Voay robustus, it is important to recognize that some of the defining characteristics of that genus may have changed through ontogeny. Elements include a nearly complete skull and many postcranial elements (cervical, thoracic, sacral, and caudal vertebrae, pectoral elements, pelvic elements, forelimb and hindlimb elements, osteoderms). Crocodylus niloticus currently inhabits Madagascar but is locally extinct from this particular region; radiometric dating indicates an age of ∼460-310 years before present (BP). This specimen clearly represents a juvenile based on the extremely small size and open sutures/detached neural arches; total body length is estimated to be ∼1.1 m (modern adults of this species range from ∼4-6 m). This fossil represents the only juvenile subfossil crocodylian specimen reported from Madagascar.

Miocene Shark and Batoid Fauna from Nosy Makamby (Mahajanga Basin, Northwestern Madagascar).

Madagascar is well known for producing exceptional fossils. However, the record for selachians remains relatively poorly known. Paleontological reconnaissance on the island of Nosy Makamby, off northwest Madagascar, has produced a previously undescribed assemblage of Miocene fossils. Based on isolated teeth, ten taxonomic groups are identified: Otodus, Carcharhinus, Galeocerdo, Rhizoprionodon, Sphyrna, Hemipristis, Squatina, Rostroraja, Himantura and Myliobatidae. Six are newly described from Madagascar for the Cenozoic (Galeocerdo, Rhizoprionodon, Sphyrna, Squatina, Rostroraja and Himantura). In association with these specimens, remains of both invertebrates (e.g., corals, gastropods, bivalves) and vertebrates (e.g., bony fish, turtles, crocodylians, and sirenian mammals) were also recovered. The sedimentary facies are highly suggestive of a near-shore/coastal plain depositional environment. This faunal association shares similarities to contemporaneous sites reported from North America and Europe and gives a glimpse into the paleoenvironment of Madagascar's Miocene, suggesting that this region was warm, tropical shallow-water marine.

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 island's paleogeographic history.

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.

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.