Trace fossil evidence of predation upon bone‐eating worms on a baleen whale skeleton from the Oligocene of New Zealand

The osteophagous worm Osedax (Annelida: Siboglinidae) colonizes vertebrate bones in deep‐sea environments globally. Osedax bioerosion of modern bones suggests a potentially destructive agent in the marine vertebrate fossil record, but the dearth of published reports of abundant Osedax traces suggests an uncertain taphonomic influence of this organism. This study reports Osedax traces (Osspecus boreholes, pockmarks and collapsed galleries) in an Oligocene baleen whale (Cetacea: Eomysticetidae) from New Zealand, which constitute the first record of fossil Osedax traces from the southern hemisphere. Some Osedax traces are cross‐cut by linear biogenic scrape marks, implying that sharks or bony fish fed upon Osedax worms, a process which compounds or potentially accelerates worm‐inflicted damage to vertebrate bones in marine environments.     

Bone-eating Osedax worms lived on Mesozoic marine reptile deadfalls

We report fossil traces of Osedax, a genus of siboglinid annelids that consume the skeletons of sunken vertebrates on the ocean floor, from early-Late Cretaceous (approx. 100 Myr) plesiosaur and sea turtle bones. Although plesiosaurs went extinct at the end-Cretaceous mass extinction (66 Myr), chelonioids survived the event and diversified, and thus provided sustenance for Osedax in the 20 Myr gap preceding the radiation of cetaceans, their main modern food source. This finding shows that marine reptile carcasses, before whales, played a key role in the evolution and dispersal of Osedax and confirms that its generalist ability of colonizing different vertebrate substrates, like fishes and marine birds, besides whale bones, is an ancestral trait. A Cretaceous age for unequivocal Osedax trace fossils also dates back to the Mesozoic the origin of the entire siboglinid family, which includes chemosynthetic tubeworms living at hydrothermal vents and seeps, contrary to phylogenetic estimations of a Late Mesozoic–Cenozoic origin (approx. 50–100 Myr).     

Evidence of Osedax worm borings in Pliocene (∼3 Ma) whale bone from the Mediterranean

Osedax worms subsist entirely on vertebrate skeletons on the seafloor, using root-like tissues to bore into and degrade the bones. Paleontologists have only recently begun to appreciate the possible destructive effect that these worms may have had on the marine vertebrate fossil record and little is known of their evolutionary history. Using microcomputed tomography, we document Osedax-like borings in a fossil whale bone from the Pliocene of Italy and present new data on the borings of extant Osedax worms. The fossil borings are distinguished from those of other known borers and identified as traces of Osedax activity based on diagnostic features. Our results suggest that it is necessary to isolate individual borings for the confident identification of Osedax traces. This is only the second paleogeographic occurrence of Osedax in the fossil record and indicates that by the Pliocene these worms had colonised a large portion of the world's oceans. This is the first evidence for Osedax in the Mediterranean, past or present, and suggests that more species await discovery in this region.     

The skin of Osedax (Siboglinidae,Annelida): An ultrastructural investigation of its epidermis

The symbiotic polychaetes of the genus Osedax living on the bones of whale carcasses have become known as bone‐eating worms. It is believed that whale bones are the source of nutrition for those gutless worms and that fatty acids are produced by their symbionts and transferred to the host. However, the symbionts are of the heterotrophic group Oceanospirillales and as such are not able to synthesize organic carbon de novo. Also, they are not housed in close contact to the bone material. We studied the ultrastructure of the integument overlying the symbiont housing trophosome in the ovisac region and the roots region and of the symbiont‐free trunk region of Osedax to investigate the host's possible contribution in feeding for the whole symbiosis. The epidermis differs conspicuously between the three regions investigated and clearly points to being correlated with different functions carried out by those regions. The ultrastructure of the integument of the root region changed towards the ovisac region and corresponds with the change of the ultrastructure observed in the Osedax trophosome. We suggest that the epidermis in the root region is tightly linked to bone degradation and nutrient uptake. The trunk region possess two types of unicellular gland cells, at least one of which seems to be involved in secretion of the gelatinous tube of adult Osedax females. J. Morphol., 2010. © 2010 Wiley‐Liss, Inc.     

Molecular taxonomy of Osedax (Annelida: Siboglinidae) in the Southern Ocean

We report the discovery of three new species of Osedax in the deep Southern Ocean, expanding the diversity and geographical range of this genus of bone‐eating worms. Osedax rogersi sp. n. and Osedax crouchi sp. n. were found on a whale skeleton at 1444 m in the Kemp Caldera in the East Scotia Sea during the Chemosynthetic Ecosystems of the Southern Ocean (ChEsSo) project. The recently described species, Osedax antarcticus, found on whale bones implanted at a depth of 550–650 m off Smith Island in the Bransfield Strait, was also found inhabiting the whale skeleton in the Kemp Caldera. Osedax crouchi as well as another new species Osedax nordenskjoeldi sp. n. have also been found on the implanted whale bones off Smith Island. These two localities are approximately 1800 km apart demonstrating a wide distribution of species within the genus. We describe the three new species, O. rogersi, O. crouchi and O. nordenskjoeldi and report the second record of O. antarcticus. We also present a new phylogenetic analysis for Osedax, including data examining genetic connectivity between the Scotia Arc and the Bransfield Strait.     

Genomic versatility and functional variation between two dominant heterotrophic symbionts of deep-sea Osedax worms

An unusual symbiosis, first observed at ∼3000 m depth in the Monterey Submarine Canyon, involves gutless marine polychaetes of the genus Osedax and intracellular endosymbionts belonging to the order Oceanospirillales. Ecologically, these worms and their microbial symbionts have a substantial role in the cycling of carbon from deep-sea whale fall carcasses. Microheterogeneity exists among the Osedax symbionts examined so far, and in the present study the genomes of the two dominant symbionts, Rs1 and Rs2, were sequenced. The genomes revealed heterotrophic versatility in carbon, phosphate and iron uptake, strategies for intracellular survival, evidence for an independent existence, and numerous potential virulence capabilities. The presence of specific permeases and peptidases (of glycine, proline and hydroxyproline), and numerous peptide transporters, suggests the use of degraded proteins, likely originating from collagenous bone matter, by the Osedax symbionts. ¹³C tracer experiments confirmed the assimilation of glycine/proline, as well as monosaccharides, by Osedax. The Rs1 and Rs2 symbionts are genomically distinct in carbon and sulfur metabolism, respiration, and cell wall composition, among others. Differences between Rs1 and Rs2 and phylogenetic analysis of chemotaxis-related genes within individuals of symbiont Rs1 revealed the influence of the relative age of the whale fall environment and support possible local niche adaptation of ‘free-living'' lifestages. Future genomic examinations of other horizontally-propogated intracellular symbionts will likely enhance our understanding of the contribution of intraspecific symbiont diversity to the ecological diversification of the intact association, as well as the maintenance of host diversity.     

Genetic Diversity and Potential Function of Microbial Symbionts Associated with Newly Discovered Species of Osedax Polychaete Worms

We investigated the genetic diversity of symbiotic bacteria associated with two newly discovered species of Osedax from Monterey Canyon, CA, at 1,017-m (Osedax Monterey Bay sp. 3 “rosy” [Osedax sp. MB3]) and 381-m (Osedax Monterey Bay sp. 4 “yellow collar”) depths. Quantitative PCR and clone libraries of 16S rRNA gene sequences identified differences in the compositions and abundances of bacterial phylotypes associated with the newly discovered host species and permitted comparisons between adult Osedax frankpressi and juveniles that had recently colonized whalebones implanted at 2,891 m. The newly discovered Osedax species hosted Oceanospirillales symbionts that are related to Gammaproteobacteria associated with the previously described O. frankpressi and Osedax rubiplumus (S. K. Goffredi, V. J. Orphan, G. W. Rouse, L. Jahnke, T. Embaye, K. Turk, R. Lee, and R. C. Vrijenhoek, Environ. Microbiol. 7:1369-1378, 2005). In addition, Osedax sp. MB3 hosts a diverse and abundant population of additional bacteria dominated by Epsilonproteobacteria. Ultrastructural analysis of symbiont-bearing root tissues verified the enhanced microbial diversity of Osedax sp. MB3. Root tissues from the newly described host species and O. frankpressi all exhibited collagenolytic enzyme activity, which covaried positively with the abundance of symbiont DNA and negatively with mean adult size of the host species. Members of this unusual genus of bone-eating worms may form variable associations with symbiotic bacteria that allow for the observed differences in colonization and success in whale fall environments throughout the world's oceans.     

Bones as biofuel: a review of whale bone composition with implications for deep-sea biology and palaeoanthropology

Whales are unique among vertebrates because of the enormous oil reserves held in their soft tissue and bone. These ‘biofuel’ stores have been used by humans from prehistoric times to more recent industrial-scale whaling. Deep-sea biologists have now discovered that the oily bones of dead whales on the seabed are also used by specialist and generalist scavenging communities, including many unique organisms recently described as new to science. In the context of both cetacean and deep-sea invertebrate biology, we review scientific knowledge on the oil content of bone from several of the great whale species: Balaenoptera musculus, Balaenoptera physalus, Balaenoptera borealis, Megaptera novaeangliae, Eschrichtius robustus, Physeter macrocephalus and the striped dolphin, Stenella coeruleoalba. We show that data collected by scientists over 50 years ago during the heyday of industrial whaling explain several interesting phenomena with regard to the decay of whale remains. Variations in the lipid content of bones from different parts of a whale correspond closely with recently observed differences in the taphonomy of deep-sea whale carcasses and observed biases in the frequency of whale bones at archaeological sites.     

First record of a parapithecid primate from the Oligocene of Kenya

Recent excavations in northwestern Kenya have recovered a vertebrate fauna of late early or early late Oligocene age. Among the mammal remains, a fragmentary lower jaw and an isolated upper molar have been attributed to a small primate, Lokonepithecus manai gen. et sp. nov. Lokonepithecus is a primitive member of the Parapithecidae and possibly most closely related to Apidium from the Fayum. The new primate from Kenya is the youngest parapithecid known and its occurrence in the Oligocene of Kenya suggests that sub-Saharan Africa probably played a major role in the evolutionary history of several groups of mammals.     

The reproductive system of Osedax (Annelida,Siboglinidae): ovary structure,sperm ultrastructure,and fertilization mode

Osedax is a genus of siboglinid annelids in which the females live on dead vertebrate bones on the seafloor. These females have a posterior end that lies within the bone and contains the ovarian tissue, as well as the “roots” involved with bone degradation and nutrition. The males are microscopic and live as “harems” in the lumen of the gelatinous tube that surrounds the female trunk, well away from the ovary. Females are known to spawn fertilized primary oocytes, suggesting internal fertilization. However, little is known about sperm transfer, sperm storage, or the location of fertilization, and the morphology of the female reproductive system has not been described and compared with the reproductive systems of other siboglinids. A 3D‐reconstruction of the ovisac of Osedax showed ovarian tissue with multiple lobes and mature oocytes stored in a “uterus” before being released through the single oviduct. The oviduct emerges as a gonopore on the trunk and travels along the trunk to finally open to the seawater as a thin cylindrical tube among the crown of palps. Light and transmission electron microscopy of mature Osedax sperm revealed elongate heads consisting of a nucleus with helical grooves occupied by mitochondria. In contrast to other Siboglinidae, Osedax sperm are not packaged into spermatophores or spermatozeugmata, and Osedax females lack a discrete region for sperm storage. Transmission electron microscopy and fluorescence microscopy allowed detection of sperm associated with ovarian tissue of the female ovisac of four different Osedax species. This provides the first evidence for the site of internal fertilization in Osedax. A heart body was found in the circulatory system, as seen in other siboglinids and some other annelids. The possible presence of nephridia in the anterior ovisac region was also documented. These morphological features provide new insights for comparing the regionalization of Osedax females in relation to other siboglinids.     

Species identification and likely catch time period of whale bones from South Georgia

Skeletal remains of baleen whales killed during the onset of 20th century commercial whaling lie scattered across the shores and abandoned whaling stations of the subantarctic island of South Georgia. Here we report on genetic species identification of whale bones collected from South Georgia using standard historical DNA protocols. We amplified and sequenced short fragments of the mitochondrial DNA (mtDNA) control region from 281 available bone samples. Of these, 231 provided mtDNA sequences of sufficient quality and length (174–194 bp) for species identification: 158 bones were identified as humpback whale (Megaptera novaeangliae), 51 bones were identified as fin whale (Balaenoptera physalus), 18 bones were identified as blue whale (B. musculus), two bones were identified as sei whale (B. borealis), one bone was identified as a southern right whale (Eubalaena australis), and one bone was identified as a southern elephant seal (Mirounga leonina). The prominence of humpback, fin, and blue whale bones in the sample collection corresponds to the catch record of the early years of whaling on the island of South Georgia (pre‐1915), prior to the depletion of these populations.     

A reassessment of the Oligocene hyracoid mammals from Malembo,Cabinda, Angola

The Oligocene Malembo locality, Cabinda exclave, Angola, has yielded a rich vertebrate fauna represented by fragmentary remains. This fossiliferous locality is the only definite occurrence of Oligocene terrestrial mammals in sub-Saharan West Africa. The hyracoids from Malembo have only been very succinctly described and compared thus far, so that their systematic attribution is not consensual among specialists. A revision now allows the identification of three (or four) medium to large-sized species represented by Geniohyus dartevellei, Pachyhyrax cf. crassidentatus, and two undetermined taxa. The species G. dartevellei is revived for the holotype of Palaeochoerus dartevellei Hooijer, 1963; this species is unique to Malembo but appears close to Geniohyus mirus, a species only known from the early Oligocene of the Fayum, Egypt. Other species of Geniohyus and Pachyhyrax crassidentatus are also only known from the early Oligocene of the Fayum. The presence of Geniohyus and Pachyhyrax cf. crassidentatus at Malembo thus supports an early Oligocene age for the fauna.     

A Swedish subfossil find of a bowhead whale from the late Pleistocene: shore displacement,paleoecology in south-west Sweden and the identity of the Swedenborg whale (Balaena swedenborgii Liljeborg, 1867)

The Swedenborg whale Balaena swedenborgii Liljeborg, 1867, is a baleen whale species believed to have existed in the North Sea from the period when the inland ice melted around 13,000 before present (BP) until about 8000 years ago. The first bones attributed to this species were found in Sweden in 1705. When whale remains were discovered on the Swedish west coast during the extension work of a motorway extension, it was speculated that this could be a specimen of the extinct Swedenborg whale. The bones were found 72 m above the present-day sea level embedded in glacial mud. Shelly remains of marine organisms were present in the deposit surrounding the whale-fall, and sediments with the associated specimens were therefore collected for further analyses. We applied radiocarbon dating, thin sectioning, morphological analyses, ancient DNA typing and analyses of the associated shelly assemblage in an interdisciplinary effort to understand the circumstances of this fossil whale-fall. Our results show that the whale is not the putative species B. swedenborgii, but a bowhead whale Balaena mysticetus. The results also indicate that the whale must have been rapidly covered by glacial sediments, highlighting the speed of the deglacial process in the area.     

Première indication de la présence de phorusracidés,famille d'oiseaux géants d'amérique du sud,dans le tertiaire Européen: Ameghinornis nov. gen. (Aves,ralliformes) des phosphorites du quercy,France

Some bird remains, from the «Phosphorites du Quercy deposits are closely related to the corresponding bones of Phorusrhacidae, an extinct family of birds which underwent an extensive diversification in South America from Oligocene to Pleistocene times. It included many giant flightless species. The form of the Quercy is a rather primitive one, of medium size and of probably somewhat reduced flying ability.The simultaneous occurrence of Phorusrhacidae inFrance and South America is of great biogeographical significance. The Phorusrhacidae seem most probably to be the descendants of a rather primitive group of Ralliformes, already diversified in Gondwanaland prior to its separation into different continental masses.     

A small loon and a new species of large owl from the Rupelian of Belgium (Aves: Gaviiformes,Strigiformes)

The early Oligocene Boom Formation in Belgium yielded many avian remains from the Rupelian unit-stratotype, most of which have remained unstudied so far. Here, I describe a small loon (Gaviiformes) and a new species of large owl (Strigiformes) that are represented by associated bones of a single individual each. The loon, of which wing and pectoral girdle bones are preserved, is assigned to Colymboides (?) metzleri, a species previously known from a partial skeleton from the Rupelian of Germany. The owl is based on a tarsometatarsus and distal tibiotarsus and described as a new species, Selenornis steendorpensis. It constitutes the most substantial fossil record of the taxon Selenornis, which was before known from a distal tibiotarsus from an unknown horizon of the Quercy fissure fillings in southwestern France. It is detailed that there are differences in the higher level taxonomic composition of the known early Oligocene avifaunas of northern and southern Europe, which may reflect true zoogeographic facts owing to a different climate and vegetation.     

Novel Psychropiezophilic Oceanospirillales Species Profundimonas piezophila gen. nov., sp. nov., Isolated from the Deep-Sea Environment of the Puerto Rico Trench

The diversity of deep-sea high-pressure-adapted (piezophilic) microbes in isolated monoculture remains low. In this study, a novel obligately psychropiezophilic bacterium was isolated from seawater collected from the Puerto Rico Trench at a depth of ∼6,000 m. This isolate, designated YC-1, grew best in a nutrient-rich marine medium, with an optimal growth hydrostatic pressure of 50 MPa (range, 20 to 70 MPa) at 8°C. Under these conditions, the maximum growth rate was extremely slow, 0.017 h⁻¹, and the maximum yield was 3.51 × 10⁷ cells ml⁻¹. Cell size and shape changed with pressure, shifting from 4.0 to 5.0 μm in length and 0.5 to 0.8 μm in width at 60 MPa to 0.8- to 1.0-μm diameter coccoid cells under 20 MPa, the minimal pressure required for growth. YC-1 is a Gram-negative, facultatively anaerobic heterotroph. Its predominant cellular fatty acids are the monounsaturated fatty acids (MUFAs) C_16:1 and C_18:1. Unlike many other psychropiezophiles, YC-1 does not synthesize any polyunsaturated fatty acids (PUFAs). Phylogenetic analysis placed YC-1 within the family of Oceanospirillaceae, closely related to the uncultured symbiont of the deep-sea whale bone-eating worms of the genus Osedax. In common with some other members of the Oceanospirillales, including those enriched during the Deepwater Horizon oil spill, YC-1 is capable of hydrocarbon utilization. On the basis of its characteristics, YC-1 appears to represent both a new genus and a new species, which we name Profundimonas piezophila gen. nov., sp. nov.     

Données nouvelles sur les mammifères et les nummulites de l'éocène supérieur subalpin (synclinaux du Charbon et d'entrevernes,Bauges, Savoie et Haute-Savoie)

Vertebrate remains and nummulites have been investigated from the Late Eocene—Early Oligocene transgressive sequence of the «Chaînes subalpines south of the lake Annecy. The sedimentary environments range from fluvio-lacustrine shales and conglomerates at the base to hemipelagic Globigerina shales at the top. The fluvio-lacustrine white marls contain mammals of the upper, probably terminal Ludian, with affinities to the assemblage of Saint-Capraise. The brackish Cerithium beds have furnished charophytes of the Bembridge zone. The nummulite limestones are not dated precisely, but isolated, probably redeposited nummulites from the base of the Globigerina shales are of terminal Eocene or basal Oligocene age. The Globigerina shales themselves belong to the Oligocene.