Early Oligocene kelp holdfasts and stepwise evolution of the kelp ecosystem in the North Pacific.

Kelp forests are highly productive and economically important ecosystems worldwide, especially in the North Pacific Ocean. However, current hypotheses for their evolutionary origins are reliant on a scant fossil record. Here, we report fossil hapteral kelp holdfasts from western Washington State, USA, indicating that kelp has existed in the northeastern Pacific Ocean since the earliest Oligocene. This is consistent with the proposed North Pacific origin of kelp associated with global cooling around the Eocene-Oligocene transition. These fossils also support the hypotheses that a hapteral holdfast, rather than a discoid holdfast, is the ancestral state in complex kelps and suggest that early kelps likely had a flexible rather than a stiff stipe. Early kelps were possibly grazed upon by mammals like desmostylians, but fossil evidence of the complex ecological interactions known from extant kelp forests is lacking. The fossil record further indicates that the present-day, multi-story kelp forest had developed at latest after the mid-Miocene climate optimum. In summary, the fossils signify a stepwise evolution of the kelp ecosystem in the North Pacific, likely enabled by changes in the ocean-climate system.

A biogeographic network reveals evolutionary links between deep-sea hydrothermal vent and methane seep faunas.

Deep-sea hydrothermal vents and methane seeps are inhabited by members of the same higher taxa but share few species, thus scientists have long sought habitats or regions of intermediate character that would facilitate connectivity among these habitats. Here, a network analysis of 79 vent, seep, and whale-fall communities with 121 genus-level taxa identified sedimented vents as a main intermediate link between the two types of ecosystems. Sedimented vents share hot, metal-rich fluids with mid-ocean ridge-type vents and soft sediment with seeps. Such sites are common along the active continental margins of the Pacific Ocean, facilitating connectivity among vent/seep faunas in this region. By contrast, sedimented vents are rare in the Atlantic Ocean, offering an explanation for the greater distinction between its vent and seep faunas compared with those of the Pacific Ocean. The distribution of subduction zones and associated back-arc basins, where sedimented vents are common, likely plays a major role in the evolutionary and biogeographic connectivity of vent and seep faunas. The hypothesis that decaying whale carcasses are dispersal stepping stones linking these environments is not supported.

Did shifting seawater sulfate concentrations drive the evolution of deep-sea methane-seep ecosystems?

The origin and evolution of the faunas inhabiting deep-sea hydrothermal vents and methane seeps have been debated for decades. These faunas rely on a local source of sulfide and other reduced chemicals for nutrition, which spawned the hypothesis that their evolutionary history is independent from that of photosynthesis-based food chains and instead driven by extinction events caused by deep-sea anoxia. Here I use the fossil record of seep molluscs to show that trends in body size, relative abundance and epifaunal/infaunal ratios track current estimates of seawater sulfate concentrations through the last 150 Myr. Furthermore, the two main faunal turnovers during this time interval coincide with major changes in seawater sulfate concentrations. Because sulfide at seeps originates mostly from seawater sulfate, variations in sulfate concentrations should directly affect the base of the food chain of this ecosystem and are thus the likely driver of the observed macroecologic and evolutionary patterns. The results imply that the methane-seep fauna evolved largely independently from developments and mass extinctions affecting the photosynthesis-based biosphere and add to the growing body of evidence that the chemical evolution of the oceans had a major impact on the evolution of marine life.

First glimpse into Lower Jurassic deep-sea biodiversity: in situ diversification and resilience against extinction.

Owing to the assumed lack of deep-sea macrofossils older than the Late Cretaceous, very little is known about the geological history of deep-sea communities, and most inference-based hypotheses argue for repeated recolonizations of the deep sea from shelf habitats following major palaeoceanographic perturbations. We present a fossil deep-sea assemblage of echinoderms, gastropods, brachiopods and ostracods, from the Early Jurassic of the Glasenbach Gorge, Austria, which includes the oldest known representatives of a number of extant deep-sea groups, and thus implies that in situ diversification, in contrast to immigration from shelf habitats, played a much greater role in shaping modern deep-sea biodiversity than previously thought. A comparison with coeval shelf assemblages reveals that, at least in some of the analysed groups, significantly more extant families/superfamilies have endured in the deep sea since the Early Jurassic than in the shelf seas, which suggests that deep-sea biota are more resilient against extinction than shallow-water ones. In addition, a number of extant deep-sea families/superfamilies found in the Glasenbach assemblage lack post-Jurassic shelf occurrences, implying that if there was a complete extinction of the deep-sea fauna followed by replacement from the shelf, it must have happened before the Late Jurassic.

Adaptive radiation of chemosymbiotic deep-sea mussels.

Adaptive radiations present fascinating opportunities for studying the evolutionary process. Most cases come from isolated lakes or islands, where unoccupied ecological space is filled through novel adaptations. Here, we describe an unusual example of an adaptive radiation: symbiotic mussels that colonized island-like chemosynthetic environments such as hydrothermal vents, cold seeps and sunken organic substrates on the vast deep-sea floor. Our time-calibrated molecular phylogeny suggests that the group originated and acquired sulfur-oxidizing symbionts in the Late Cretaceous, possibly while inhabiting organic substrates and long before its major radiation in the Middle Eocene to Early Oligocene. The first appearance of intracellular and methanotrophic symbionts was detected only after this major radiation. Thus, contrary to expectations, the major radiation may have not been triggered by the evolution of novel types of symbioses. We hypothesize that environmental factors, such as increased habitat availability and/or increased dispersal capabilities, sparked the radiation. Intracellular and methanotrophic symbionts were acquired in several independent lineages and marked the onset of a second wave of diversification at vents and seeps. Changes in habitat type resulted in adaptive trends in shell lengths (related to the availability of space and energy, and physiological trade-offs) and in the successive colonization of greater water depths.

Fossil traces of the bone-eating worm Osedax in early Oligocene whale bones.

Osedax is a recently discovered group of siboglinid annelids that consume bones on the seafloor and whose evolutionary origins have been linked with Cretaceous marine reptiles or to the post-Cretaceous rise of whales. Here we present whale bones from early Oligocene bathyal sediments exposed in Washington State, which show traces similar to those made by Osedax today. The geologic age of these trace fossils ( approximately 30 million years) coincides with the first major radiation of whales, consistent with the hypothesis of an evolutionary link between Osedax and its main food source, although older fossils should certainly be studied. Osedax has been destroying bones for most of the evolutionary history of whales and the possible significance of this "Osedax effect" in relation to the quality and quantity of their fossils is only now recognized.

Osedax borings in fossil marine bird bones.

The bone-eating marine annelid Osedax consumes mainly whale bones on the deep-sea floor, but recent colonization experiments with cow bones and molecular age estimates suggesting a possible Cretaceous origin of Osedax indicate that this worm might be able grow on a wider range of substrates. The suggested Cretaceous origin was thought to imply that Osedax could colonize marine reptile or fish bones, but there is currently no evidence that Osedax consumes bones other than those of mammals. We provide the first evidence that Osedax was, and most likely still is, able to consume non-mammalian bones, namely bird bones. Borings resembling those produced by living Osedax were found in bones of early Oligocene marine flightless diving birds (family Plotopteridae). The species that produced these boreholes had a branching filiform root that grew to a length of at least 3 mm, and lived in densities of up to 40 individuals per square centimeter. The inclusion of bird bones into the diet of Osedax has interesting implications for the recent suggestion of a Cretaceous origin of this worm because marine birds have existed continuously since the Cretaceous. Bird bones could have enabled this worm to survive times in the Earth's history when large marine vertebrates other than fish were rare, specifically after the disappearance of large marine reptiles at the end-Cretaceous mass extinction event and before the rise of whales in the Eocene.

Resource partitioning among brachiopods and bivalves at ancient hydrocarbon seeps: A hypothesis.

Brachiopods were thought to have dominated deep-sea hydrothermal vents and hydrocarbon seeps for most of the Paleozoic and Mesozoic, and were believed to have been outcompeted and replaced by chemosymbiotic bivalves during the Late Cretaceous. But recent findings of bivalve-rich seep deposits of Paleozoic and Mesozoic age have questioned this paradigm. By tabulating the generic diversity of the dominant brachiopod and bivalve clades-dimerelloid brachiopods and chemosymbiotic bivalves-from hydrocarbon seeps through the Phanerozoic, we show that their evolutionary trajectories are largely unrelated to one another, indicating that they have not been competing for the same resources. We hypothesize that the dimerelloid brachiopods generally preferred seeps with abundant hydrocarbons in the bottom waters above the seep, such as oil seeps or methane seeps with diffusive seepage, whereas seeps with strong, advective fluid flow and hence abundant hydrogen sulfide were less favorable for them. At methane seeps typified by diffusive seepage and oil seeps, oxidation of hydrocarbons in the bottom water by chemotrophic bacteria enhances the growth of bacterioplankton, on which the brachiopods could have filter fed. Whereas chemosymbiotic bivalves mostly relied on sulfide-oxidizing symbionts for nutrition, for the brachiopods aerobic bacterial oxidation of methane and other hydrocarbons played a more prominent role. The availability of geofuels (i.e. the reduced chemical compounds used in chemosynthesis such as hydrogen sulfide, methane, and other hydrocarbons) at seeps is mostly governed by fluid flow rates, geological setting, and marine sulfate concentrations. Thus rather than competition, we suggest that geofuel type and availability controlled the distribution of brachiopods and bivalves at hydrocarbon seeps through the Phanerozoic.

Deep-sea food bonanzas: early Cenozoic whale-fall communities resemble wood-fall rather than seep communities.

The evolutionary history of invertebrate communities utilizing whale carcasses and sunken wood in the deep-sea is explored using fossil evidence. Compared to modern whale-fall communities, the Eo-Oligocene examples lack those vent-type taxa that most heavily rely on sulphide produced by anaerobic breakdown of bone lipids, but are very similar in their trophic structure to contemporaneous wood-falls. This sheds doubt on the hypothesis that whale-falls were evolutionary stepping stones for taxa that now inhabit hydrothermal vents and seeps. We suggest that the whale-fall communities reported here represent a new ecologic stage among whale-falls, which we have coined the 'chemosymbiotic opportunist stage' and that the 'sulphophilic stage' of modern whale-falls developed during the Early Miocene, resulting from a significant increase in both body size and/or oil content of bones among cetaceans during this time.

Cenozoic Methane-Seep Faunas of the Caribbean Region.

We report new examples of Cenozoic cold-seep communities from Colombia, Cuba, the Dominican Republic, Trinidad, and Venezuela, and attempt to improve the stratigraphic dating of Cenozoic Caribbean seep communities using strontium isotope stratigraphy. Two seep faunas are distinguished in Barbados: the late Eocene mudstone-hosted 'Joes River fauna' consists mainly of large lucinid bivalves and tall abyssochrysoid gastropods, and the early Miocene carbonate-hosted 'Bath Cliffs fauna' containing the vesicomyid Pleurophopsis, the mytilid Bathymodiolus and small gastropods. Two new Oligocene seep communities from the Sinú River basin in Colombia consist of lucinid bivalves including Elongatolucina, thyasirid and solemyid bivalves, and Pleurophopsis. A new early Miocene seep community from Cuba includes Pleurophopsis and the large lucinid Meganodontia. Strontium isotope stratigraphy suggests an Eocene age for the Cuban Elmira asphalt mine seep community, making it the oldest in the Caribbean region. A new basal Pliocene seep fauna from the Dominican Republic is characterized by the large lucinid Anodontia (Pegophysema). In Trinidad we distinguish two types of seep faunas: the mudstone-hosted Godineau River fauna consisting mainly of lucinid bivalves, and the limestone-hosted Freeman's Bay fauna consisting chiefly of Pleurophopsis, Bathymodiolus, and small gastropods; they are all dated as late Miocene. Four new seep communities of Oligocene to Miocene age are reported from Venezuela. They consist mainly of large globular lucinid bivalves including Meganodontia, and moderately sized vesicomyid bivalves. After the late Miocene many large and typical 'Cenozoic' lucinid genera disappeared from the Caribbean seeps and are today known only from the central Indo-Pacific Ocean. We speculate that the increasingly oligotrophic conditions in the Caribbean Sea after the closure of the Isthmus of Panama in the Pliocene may have been unfavorable for such large lucinids because they are only facultative chemosymbiotic and need to derive a significant proportion of their nutrition from suspended organic matter.

Effects of sample storage and shell orientation on LA-ICPMS trace element measurements on deep-sea mussels.

Geochemical markers are being increasingly applied to fundamental questions in population and community ecology in marine habitats because they allow inferences on individuals dispersal, but vital effects, small sample size and instrumental limitation are still challenging particularly in deep-sea studies. Here we use shells of the deep-sea bivalve Idas modiolaeformis to assess potential effects of sample storage, mineralogy, and valve orientation on LA-ICPMS measurements. Trace element concentrations of (24)Mg, (43)Ca, (88)Sr, (137)Ba, (208)Pb, and (238)U are not affected by the two most commonly used storage methods of biologic deep-sea samples (frozen at -20°C and fixed in 95% ethanol); thus combined analysis of differently preserved specimens is possible when the number of individuals is insufficient and distinct sample fixation is needed for multiple purposes. Valve orientation had a strong impact on quantification of trace elements in the calcitic but not in the aragonitic layer of adult shells. Hence, to enable comparisons between adult shells and entirely aragonitic embryonic shells, a reference map of site-specific signatures can potentially be generated using the aragonitic layer of the adult shells. Understanding ontogenetic changes and environmental effects in trace element incorporation is critical before geochemical fingerprinting can be used as a tool for larval dispersal studies in the deep-sea.

Mollusks from late Mesozoic seep deposits, chiefly in California.

Twenty-nine mollusk species from Late Jurassic to Eocene hydrocarbon seep deposits from California (USA), Japan, New Zealand, and Barbados are described and illustrated. Twenty species belong to Gastropoda and nine to Bivalvia. Seven new species, three new genera, and one new family are introduced. The gastropod Hikidea gen. nov. includes smooth-shelled Cantrainea-like colloniins from Cretaceous hydrocarbon seeps and plesiosaur falls. Hikidea osoensis sp. nov. is the oldest species of this genus. Chilodonta? reticulata sp. nov. is a distinctive vetigastropod though its supraspecific position is unclear. Phanerolepida onoensis sp. nov. is the first species of this colloniin genus from a seep deposit. We describe two new genera of Hokkaidoconchidae: Abyssomelania gen. nov. and Ascheria gen. nov.; this family includes now four genera (including Hokkaidoconcha and Humptulipsia) and ranges from the Late Jurassic to the Eocene. Abyssomelania is characterized by a large, high-spired shell and unusual widely-spaced prosocline riblets (here called abyssomelaniid riblets). Abyssomelania is represented by two new species: A. cramptoni sp. nov. from the Late Cretaceous of New Zealand and A. campbellae sp. nov. from the Early Cretaceous of California. Ascheria gen. nov. is characterized by a large high-spired cerithiform shell, a subsutural constriction, and mostly reticulate ornament. Two nominate species are included: Ascheria gigantea (Kiel et al., 2008) and A. eucosmeta (Ascher, 1906), both of Early Cretaceous age. Two further species potentially belonging to Ascheria from the Eocene of Barbados are reported in open nomenclature and are re-illustrated and re-described for comparison. Humtulipsia nobuharai sp. nov. is described based on specimens from the Campanian-Maastrichtian Sada Limestone seep deposit in Japan. The new family Paskentanidae fam. nov. is introduced for the genera Paskentana and Atresius. The species of this family are characterized by thin-shelled, broad to high-spired littoriniform adult shells and juvenile teleoconchs with a subsutural ramp. Paskentana hamiltonensis sp. nov. is described from the Early Cretaceous of California. Ataphrus is considered to represent a nomen dubium because its type species is poorly preserved and there are uncertainties regarding its type locality and age. The bivalves reported herein belong to known species, but our new material revealed additional characters, and/or their supraspecific position is revised and new combinations are proposed: Solemya stantoni Vokes, 1955 is transferred to Acharax, Nucula gabbi Stanton, 1895 is transferred to Leionucula, Pecten complexicostata Gabb, 1869 is transferred to Lyriochlamys, Astarte californica Stanton, 1895 is transferred to Neocrassina, Astarte trapezoidalis Stanton, 1895 is transferred to Oxyeurax, and Corbula? persulcata Stanton, 1895 is transferred to Cuspidaria? 

The paleoecology, habitats, and stratigraphic range of the enigmatic cretaceous brachiopod peregrinella.

Modern and Cenozoic deep-sea hydrothermal-vent and methane-seep communities are dominated by large tubeworms, bivalves and gastropods. In contrast, many Early Cretaceous seep communities were dominated by the largest Mesozoic rhynchonellid brachiopod, the dimerelloid Peregrinella, the paleoecologic and evolutionary traits of which are still poorly understood. We investigated the nature of Peregrinella based on 11 occurrences world wide and a literature survey. All in situ occurrences of Peregrinella were confirmed as methane-seep deposits, supporting the view that Peregrinella lived exclusively at methane seeps. Strontium isotope stratigraphy indicates that Peregrinella originated in the late Berriasian and disappeared after the early Hauterivian, giving it a geologic range of ca. 9.0 (+1.45/-0.85) million years. This range is similar to that of rhynchonellid brachiopod genera in general, and in this respect Peregrinella differs from seep-inhabiting mollusks, which have, on average, longer geologic ranges than marine mollusks in general. Furthermore, we found that (1) Peregrinella grew to larger sizes at passive continental margins than at active margins; (2) it grew to larger sizes at sites with diffusive seepage than at sites with advective fluid flow; (3) despite its commonly huge numerical abundance, its presence had no discernible impact on the diversity of other taxa at seep sites, including infaunal chemosymbiotic bivalves; and (4) neither its appearance nor its extinction coincides with those of other seep-restricted taxa or with global extinction events during the late Mesozoic. A preference of Peregrinella for diffusive seepage is inferred from the larger average sizes of Peregrinella at sites with more microcrystalline carbonate (micrite) and less seep cements. Because other seep-inhabiting brachiopods occur at sites where such cements are very abundant, we speculate that the various vent- and seep-inhabiting dimerelloid brachiopods since Devonian time may have adapted to these environments in more than one way.

Cold-seep mollusks are older than the general marine mollusk fauna.

The origin and possible antiquity of faunas at deep-sea hydrothermal vents and seeps have been debated since their discovery. We used the fossil record of seep mollusks to show that the living seep genera have significantly longer geologic ranges than the marine mollusks in general, but have ranges similar to those of deep-sea taxa, suggesting that seep faunas may be shaped by the factors that drive the evolution of life in the deep sea in general. Our data indicate that deep-sea anoxic/dysoxic events did not affect seep faunas, casting doubt on the suggested anoxic nature and/or global extent of these events.