Complete Primate Skeleton from the Middle Eocene of Messel in Germany: Morphology and Paleobiology

Background

The best European locality for complete Eocene mammal skeletons is Grube Messel, near Darmstadt, Germany. Although the site was surrounded by a para-tropical rain forest in the Eocene, primates are remarkably rare there, and only eight fragmentary specimens were known until now. Messel has now yielded a full primate skeleton. The specimen has an unusual history: it was privately collected and sold in two parts, with only the lesser part previously known. The second part, which has just come to light, shows the skeleton to be the most complete primate known in the fossil record.

Methodology/Principal Findings

We describe the morphology and investigate the paleobiology of the skeleton. The specimen is described as Darwinius masillae n.gen. n.sp. belonging to the Cercamoniinae. Because the skeleton is lightly crushed and bones cannot be handled individually, imaging studies are of particular importance. Skull radiography shows a host of teeth developing within the juvenile face. Investigation of growth and proportion suggest that the individual was a weaned and independent-feeding female that died in her first year of life, and might have attained a body weight of 650–900 g had she lived to adulthood. She was an agile, nail-bearing, generalized arboreal quadruped living above the floor of the Messel rain forest.

Conclusions/Significance

Darwinius masillae represents the most complete fossil primate ever found, including both skeleton, soft body outline and contents of the digestive tract. Study of all these features allows a fairly complete reconstruction of life history, locomotion, and diet. Any future study of Eocene-Oligocene primates should benefit from information preserved in the Darwinius holotype. Of particular importance to phylogenetic studies, the absence of a toilet claw and a toothcomb demonstrates that Darwinius masillae is not simply a fossil lemur, but part of a larger group of primates, Adapoidea, representative of the early haplorhine diversification.     

The dentition of a well-preserved specimen of <Emphasis Type="Italic">Camarasaurus</Emphasis> sp.: implications for function,tooth replacement,soft part reconstruction,and food intake

The basal macronarian genus Camarasaurus was the most common sauropod in the Upper Jurassic Morrison Formation of North America and is known from several complete and partial skeletons. The specimen used for this study is Camarasaurus sp. SMA 0002 from the Sauriermuseum Aathal, Switzerland. This specimen was found in the Howe-Stephens Quarry, Bighorn Basin, WY, USA. In this study, the dental morphology, characterized by the spatulate, broad-crowned teeth, the tooth replacement pattern, and the function of the dentition and its implications for food intake is described. Features such as the absence of denticles, the wrinkled pattern of the enamel, and the occurrence of large wear facets on older teeth are characteristic for Camarasaurus sp. A slab of sediment with soft tissue impressions ranging up to the middle part of the crown suggests the presence of a gingival soft tissue structure partially covering the teeth. The wrinkled enamel on the crown of the teeth of Camarasaurus sp. and other sauropods is interpreted as indication of this cover of gingival connective tissue. In addition, there possibly was a keratinous beak, which together with the gingiva held the teeth in the jaw and provided stability for teeth in which the root is almost completely resorbed.     

Callistoe vincei, a new Proborhyaenidae (Borhyaenoidea, Metatheria, Mammalia) from the Early Eocene of Argentina

Callistoe vincei nov. gen., nov. sp. is a new South American carnivorous marsupial (Proborhyaenidae, Borhyaenoidea) from Salta Province (Argentina). It is preliminarily described and its phylogenetic relationships with other borhyaenoids are analyzed. The holotype is a complete skull with almost complete postcranial skeleton (missing the pelvis and the tail). It is from the Lumbrera Formation (Early Eocene of northwestern Argentina). It represents the most complete proborhyaenid specimen ever discovered and one of the best-preserved borhyaenoid. In the present paper we analyze the major cranial and dental features, the essential elements to compare C. vincei to Arminiheringia auceta, a Casamayoran proborhyaenid of Patagonia. C. vincei is smaller, much more gracile; its skull is narrower; its lower canines are not procumbent; the metacrista of M3 is U-shaped; the postmetacrista of M4 is present and the mandibular symphysis is shorter. This new material allows reconsideration of some dental traits proposed to diagnose the Proborhyaenidae such as the number of incisors and the open-rooted canines.     

First partial cranium of Togocetus from Kpogamé (Togo) and the protocetid diversity in the Togolese phosphate basin

Earliest cetaceans (whales) originated from the early Eocene of Indo-Pakistan, but the group dispersed through most of the oceans of the planet by the late middle to late Eocene. This late Eocene global distribution indicates that important dispersal events took place during the middle Eocene (Lutetian), a globally undersampled time interval that is well documented in the Togolese phosphate series. We report here the first discovery of a partial cetacean cranium from middle Eocene deposits of Togo (West Africa). A 3D model of the cranium and teeth was reconstructed in order to reveal hidden anatomical features. The dental and cranial characteristics of the Togolese specimen recall those of protocetid taxa described in Africa, Asia, and North America, but also display significant differences. In particular, we show that the new specimen shares a number of morphological features with the Togolese taxon Togocetus. Such a hypothesis is further supported by a cladistic analysis including 45 taxa and 167 morphological characters, which recovers the new specimen close to Togocetus as the first offshoot of protocetids. Phylogenetic analysis including all the protocetids remains of Kpogamé confirms the singular diversity of the Togolese phosphate basin, and enables to examine potential connections with faunas from contemporaneous localities in Africa.     

New Protocetid Whale from the Middle Eocene of Pakistan: Birth on Land,Precocial Development,and Sexual Dimorphism

Background

Protocetidae are middle Eocene (49–37 Ma) archaeocete predators ancestral to later whales. They are found in marine sedimentary rocks, but retain four legs and were not yet fully aquatic. Protocetids have been interpreted as amphibious, feeding in the sea but returning to land to rest.

Methodology/Principal Findings

Two adult skeletons of a new 2.6 meter long protocetid, Maiacetus inuus, are described from the early middle Eocene Habib Rahi Formation of Pakistan. M. inuus differs from contemporary archaic whales in having a fused mandibular symphysis, distinctive astragalus bones in the ankle, and a less hind-limb dominated postcranial skeleton. One adult skeleton is female and bears the skull and partial skeleton of a single large near-term fetus. The fetal skeleton is positioned for head-first delivery, which typifies land mammals but not extant whales, evidence that birth took place on land. The fetal skeleton has permanent first molars well mineralized, which indicates precocial development at birth. Precocial development, with attendant size and mobility, were as critical for survival of a neonate at the land-sea interface in the Eocene as they are today. The second adult skeleton is the most complete known for a protocetid. The vertebral column, preserved in articulation, has 7 cervicals, 13 thoracics, 6 lumbars, 4 sacrals, and 21 caudals. All four limbs are preserved with hands and feet. This adult is 12% larger in linear dimensions than the female skeleton, on average, has canine teeth that are 20% larger, and is interpreted as male. Moderate sexual dimorphism indicates limited male-male competition during breeding, which in turn suggests little aggregation of food or shelter in the environment inhabited by protocetids.

Conclusions/Significance

Discovery of a near-term fetus positioned for head-first delivery provides important evidence that early protocetid whales gave birth on land. This is consistent with skeletal morphology enabling Maiacetus to support its weight on land and corroborates previous ideas that protocetids were amphibious. Specimens this complete are virtual ‘Rosetta stones’ providing insight into functional capabilities and life history of extinct animals that cannot be gained any other way.     

Paratritemnodon indicus (Creodonta: Mammalia) from the early Middle Eocene Subathu Formation,NW Himalaya,India, and the Kalakot mammalian community structure

A complete post-incisor upper dentition and a left mandible with P/3-M/3 of the proviverrine hyaenodontid (Creodonta: Mammalia)Paratritemnodon indicus, which was hitherto known by heavily worn P/3-M/3, are described from the uppermost Subathu Formation (Middle Eocene) of the Kalakot-Metka-Mohgala area, Rajauri District, Jammu and Kashmir.P. indicus is most closely related to the North American Early Eocene proviverrine,Tritemnodon; its relationships withProdissopsalis from the Middle Eocene of Europe andPropterodon from the Middle to Late Eocene of China are also close. In the Kalakot Eocene vertebrate community of the Subathu vertebrate bioprovince,P. indicus is the only land dwelling carnivorous mammal against more than 20 species of herbivorous mammals, a majority of which are larger than it. This is viewed as an imbalance in trie community and it reflects an immaturity of the ecosystem supporting the fauna. The scarcity of carnivore remains in the Kalakot mammalian fauna is not an artifact.     

The giant bird Gastornis in Asia: A revision of Zhongyuanus xichuanensis Hou, 1980, from the Early Eocene of China

The type specimen of the gastornithid Zhongyuanus xichuanensis Hou, 1980, from the Early Eocene of Henan (central China) is redescribed and compared with European and North American representatives of Gastornis. Differences between the Chinese specimen (the distal end of tibiotarsus) and its European and North American counterparts are of a minor nature, and it is concluded that it can be referred to as Gastornis xichuanensis (Hou, 1980). Stratigraphic evidence suggests that Gastornis originated in Europe, where it is known as early as the Paleocene. Whether the Asian Gastornis dispersed from North America via the Bering land bridge, or directly from Europe across the Turgai Strait, remains uncertain.     

First substantial Middle Eocene record of the Lithornithidae (Aves): A postcranial skeleton from Messel (Germany)

A postcranial skeleton of a representative of the palaeognathous Lithornithidae (Aves) is described from the Middle Eocene of Messel in Germany. The specimen is slightly smaller than Lithornis plebius from which it, however, differs in limb bone proportions. It constitutes the latest fossil record of the Lithornithidae in Europe, whose only other Middle Eocene record is a fragmentary tibiotarsus from North America.     

Body mass estimates of an exceptionally complete Stegosaurus (Ornithischia: Thyreophora): comparing volumetric and linear bivariate mass estimation methods

Body mass is a key biological variable, but difficult to assess from fossils. Various techniques exist for estimating body mass from skeletal parameters, but few studies have compared outputs from different methods. Here, we apply several mass estimation methods to an exceptionally complete skeleton of the dinosaur Stegosaurus. Applying a volumetric convex-hulling technique to a digital model of Stegosaurus, we estimate a mass of 1560 kg (95% prediction interval 1082–2256 kg) for this individual. By contrast, bivariate equations based on limb dimensions predict values between 2355 and 3751 kg and require implausible amounts of soft tissue and/or high body densities. When corrected for ontogenetic scaling, however, volumetric and linear equations are brought into close agreement. Our results raise concerns regarding the application of predictive equations to extinct taxa with no living analogues in terms of overall morphology and highlight the sensitivity of bivariate predictive equations to the ontogenetic status of the specimen. We emphasize the significance of rare, complete fossil skeletons in validating widely applied mass estimation equations based on incomplete skeletal material and stress the importance of accurately determining specimen age prior to further analyses.     

Revision of the scorpionfly family Holcorpidae (Mecoptera), with description of a new species from Early Eocene McAbee,British Columbia,Canada

The scorpionfly family Holcorpidae (Mecoptera) has been informally discussed since the early 1960’s, but a detailed treatment in accordance with the provisions of the International Code of Zoological Nomenclature for naming families was not provided until Willmann did so in 1989; he is recognized as author of the family. The Holcorpidae concept is revised here based on examination of its two specimens of Holcorpa maculosa from the Late Eocene of Florissant, Colorado, and a third, new specimen from the Early Eocene Okanagan Highlands locality at McAbee, British Columbia, Canada. This new specimen belongs to a second, new species, which is described here, Holcorpa dillhoffi n. sp.     

Characterization of pediatric microtia cartilage: a reservoir of chondrocytes for auricular reconstruction using tissue engineering strategies

The external ear is composed of elastic cartilage. Microtia is a congenital malformation of the external ear that involves a small reduction in size or a complete absence. The aim of tissue engineering is to regenerate tissues and organs clinically implantable based on the utilization of cells and biomaterials. Remnants from microtia represent a source of cells for auricular reconstruction using tissue engineering. To examine the macromolecular architecture of microtia cartilage and behavior of chondrocytes, in order to enrich the knowledge of this type of cartilage as a cell reservoir. Auricular cartilage remnants were obtained from pediatric patients with microtia undergoing reconstructive procedures. Extracellular matrix composition was characterized using immunofluorescence and histological staining methods. Chondrocytes were isolated and expanded in vitro using a mechanical-enzymatic protocol. Chondrocyte phenotype was analyzed using qualitative PCR. Microtia cartilage preserves structural organization similar to healthy elastic cartilage. Extracellular matrix is composed of typical cartilage proteins such as type II collagen, elastin and proteoglycans. Chondrocytes displayed morphological features similar to chondrocytes derived from healthy cartilage, expressing SOX9, COL2 and ELN, thus preserving chondral phenotype. Cell viability was 94.6 % during in vitro expansion. Elastic cartilage from microtia has similar characteristics, both architectural and biochemical to healthy cartilage. We confirmed the suitability of microtia remnant as a reservoir of chondrocytes with potential to be expanded in vitro, maintaining phenotypical features and viability. Microtia remnants are an accessible source of autologous cells for auricular reconstruction using tissue engineering strategies.     

Spontaneous complete clefting of the palates in a mouse fetus: a study by scanning electron microscopy and serial section reconstruction

A 15 day mouse fetus having spontaneous complete clefting of the primary and secondary palates was studied in comparison with its normal litter mates and with normal 14 day fetuses. Specimens were studied by scanning electron microscopy at various stages of microdissection, by light microscopy of thin serial sections and by serial section reconstruction of the anterior chondrocranium of the clefted specimen and one of its normal litter mates. Differentiation of tooth and bone tissue was slightly retarded in the clefted fetus but paranasal and oral landmarks, though distorted, were present. The clefted fetus had a smaller angle between cranial base and nasal capsule and a marked discontinuity between the primary and secondary palates. Cell surfaces on the medial edge of the secondary palate in the clefted fetus resembled cell surfaces of oral areas that do not normally fuse, i.e. they are polygonial, flat and bear few surface projections in contrast to the normal 14 day condition where these cells are spindle shaped, convex and have many microvilli. The observations support the concepts that clefting of the secondary palate is consequential to clefting of the primary palate, that maldevelopment of neural crest mesenchyme is not necessarily a contributing factor, that clefting of the primary and secondary palates is associated with a shorter anterior-posterior dimension of the head and that when fusion of palatal shelves fails to occur the cells of the medial edges modulate in the direction of a generalized type of surface epithelium.     

A new species of Neochelys (Chelonii,Podocnemididae) from the Ypresian (Early Eocene) of the South of France

The known European record of the Gondwanan group Podocnemididae begins in the Early Eocene. Neochelys underwent a rapid diversification and was an abundant and diverse representative of this group during the Eocene of Europe from the Early Ypresian to at least the Bartonian. However, several of its species are poorly known, and the phylogenetic relationships among them are poorly understood. A complete shell from the Ypresian of Hérault (southern France) is described here. It is assigned to a new species, Neochelys liriae. The availability of characters of N. liriae is tested by comparison with the other European species, which appear to be well differentiated, and particularly with the neighbouring French taxa N. eocaenica and N. laurenti, of which the latter has been little known to this point.     

A specimen of Eocuculus Chandler, 1999 (Aves, ? Cuculidae) from the early Oligocene of France

A postcranial skeleton of a small bird from the early Oligocene locality Pichovet in Southern France is described and identified as Eocuculus cf. cherpinae Chandler, 1999. It is the second fossil record of Eocuculus which was hitherto known from a postcranial skeleton from the late Eocene of North America only. Although Eocuculus shares some derived similarities with Cuculidae (cuckoos), it distinctly differs in a number of osteological features from crown group members of this taxon. If future, more complete skeletons prove its cuculiform affinities, Eocuculus is a stem lineage representative of this taxon and not within the crown group. Recognition of Eocuculus in the early Oligocene of France provides evidence for the presence of an extinct late Eocene/early Oligocene avian taxon with an intercontinental Northern Hemisphere distribution.     

Synchrotron analysis of a ‘mummified’ salamander (Vertebrata: Caudata) from the Eocene of Quercy,France

An incomplete ‘mummy’ from the Phosphorites du Quercy (presumed Eocene) was identified as a salamander during the 19^th century. The specimen has now been computed tomography (CT) scanned, and this revealed the incomplete skeleton (with perfectly preserved bones) and soft tissues (lung). The fossil represents a new, well‐characterized taxon. Despite the absence of the skull, several features allow a phylogenetic analysis. The fossil belongs to pseudosaurian caudates; it is tentatively assigned to the Salamandridae, although affinities with Plethodontidae cannot be definitely ruled out.     

A new shell-bearing organism from the Cambrian Spence Shale of Utah

A new shell-bearing organism with preserved soft tissue, Armilimax pauljamisoni n. gen. n. sp., is reported from the middle Cambrian (Miaolingian: Wuliuan) Miners Hollow locality of the Spence Shale of northern Utah. The described organism is known from a single articulated specimen and preserves a prominent shell, a slug-like body, as well as a U-shaped digestive tract. Its overall appearance is similar to halkieriids, but it does not preserve sclerites. The possible affinities of the new taxon and potential reasons for the presence of a U-shaped gut are discussed. Armilimax pauljamisoni is the first shell-bearing animal of its kind from the Great Basin and extends the diversity of body plans in the Spence Shale Fossil-Lagerstätte.     

Ceftiofur derivates in serum and endometrial tissue after intramuscular administration in healthy mares

Endometritis is one of the major problems in the horse breeding industry. The use of antibiotics for treatment of endometritis in the mare is recommended as best practice. The intrauterine application of antibiotics, however, has been under discussion over the last years because of concerns about its efficacy. The systemic use of antibiotics has been considered more effective because of its better distribution within the uterus. The objective of the present study was to determine the concentration of ceftiofur derivates in serum and endometrial tissue after intramuscular administration. Specifically, the authors tested the hypothesis that ceftiofur concentrations in serum and endometrial tissue remain above the minimum inhibitory concentration (MIC) for common uterine pathogens for 24 h. Nine mares in estrus received a single dose of 2.2 mg/kg ceftiofur hydrochloride intramuscular per kg of body weight. Blood samples and endometrial tissue were obtained immediately before treatment (−1 h) and 2 h and 24 h after treatment. Endometrial tissue was collected with a Kevorkian biopsy punch. Additional blood samples were collected 4 h and 10 h after treatment from the jugular veins. For determination of ceftiofur derivates in serum and endometrial tissue a high performance liquid chromatography (HPLC) assay was used. Results in serum and uterine tissue revealed greatest concentration of ceftiofur at 2 h and lowest concentrations at 24 h after treatment. Concentrations of ceftiofur at 2 and 24 h after treatment were significantly greater in serum than in endometrial tissue, but remained above the reported MIC for Streptococcus equi zooepidemicus and Escherichia coli in both serum and endometrial tissue until 24 h after treatment.     

Craniorachischisis in a squirrel monkey

A stillborn squirrel monkey had craniorachischisis. The calvarium was absent and the skin and vertebral neural arches were cleft from the foramen magnum to the midlumbar region. Cranial nerves and degenerating neural tissue were attached to the cranial base and there were remnants of spinal cord in skin-covered areas of the spinal canal. The adrenal glands were normal. This is the only reported case of craniorachischisis in a monkey fetus.     

Macrocranion tupaiodon,an adapisoricid (?) Insectivore from the Eocene of ‘Grube Messel’ (Western Germany)

The anatomical study of several complete skeletons of the Eocene insectivoreMacrocranion tupaiodon from the “Grube Messel” (Western Germany) allows to reconstruct a number of more relevant biological adaptations of this extinct mammal. Its size is to be compared with small squirrels or treeshrews; its limbs are significantly longer, however.Macrocranion is best characterized as an omnivorous, nocturnal forest-floor predator.     

An exceptional cheloniid turtle, Osonachelus decorata nov. gen., nov. sp., from the Eocene (Bartonian) of Catalonia (Spain)

Osonachelus decorata nov. gen., nov. sp., is the first named chelonioid turtle from the Iberian Peninsula. This Eocene turtle was found in the marine sediments of the Vespella Marls Member (Vic-Manlleu Marls Formation, upper Bartonian) that occur in the Osona county (eastern Ebro Basin, Province of Barcelona, Catalonia, Spain). The area is rich in invertebrate, fish, and plant fossils but various vertebrates, including several chelonian taxa, have remained unpublished. This paper is the first dedicated to the fossil turtles of this area. Osonachelus nov. gen. is a large turtle with an impressive, massive skull revealing a specialized diet, a large and well-fenestrated shell (well ornamented dorsally and much lightened ventrally), and large paddles for high-sea locomotion. It is phylogenetically located among relatively advanced cheloniids, just basal to modern forms. Although apparent similarities in shell morphology exist with Allopleuron from the Maastrichtian of Holland, Osonachelus nov. gen. is distinct due to its masticatory apparatus, less usual among cheloniids and seemingly closer to that of the Lutetian Eochelone from Belgium. Based on the deeply concave and smooth lower jaw symphysis, its diet probably consisted of soft animals or plants rather than hard-food items. Therefore, it occupied a specialized ecological niche that is unique for the Eocene of the Iberian Peninsula.