Osedax, commonly known as bone-eating worms, are unusual marine annelids belonging to Siboglinidae and represent a remarkable example of evolutionary adaptation to a specialized habitat, namely sunken vertebrate bones. Usually, females of these animals live anchored inside bone owing to a ramified root system from an ovisac, and obtain nutrition via symbiosis with Oceanospirillales gamma-proteobacteria. Since their discovery, 26 Osedax operational taxonomic units (OTUs) have been reported from a wide bathymetric range in the Pacific, the North Atlantic, and the Southern Ocean. Using experimentally deployed and naturally occurring bones we report here the presence of Osedax deceptionensis at very shallow-waters in Deception Island (type locality; Antarctica) and at moderate depths near South Georgia Island (Subantarctic). We present molecular evidence in a new phylogenetic analysis based on five concatenated genes (28S rDNA, Histone H3, 18S rDNA, 16S rDNA, and cytochrome c oxidase I–COI–), using Maximum Likelihood and Bayesian inference, supporting the placement of O. deceptionensis as a separate lineage (Clade VI) although its position still remains uncertain. This phylogenetic analysis includes a new unnamed species (O. ‘mediterranea’) recently discovered in the shallow-water Mediterranean Sea belonging to Osedax Clade I. A timeframe of the diversification of Osedax inferred using a Bayesian framework further suggests that Osedax diverged from other siboglinids during the Middle Cretaceous (ca. 108 Ma) and also indicates that the most recent common ancestor of Osedax extant lineages dates to the Late Cretaceous (ca. 74.8 Ma) concomitantly with large marine reptiles and teleost fishes. We also provide a phylogenetic framework that assigns newly-sequenced Osedax endosymbionts of O. deceptionensis and O. ‘mediterranea’ to ribospecies Rs1. Molecular analysis for O. deceptionensis also includes a COI-based haplotype network indicating that individuals from Deception Island and the South Georgia Island (ca. 1,600 km apart) are clearly the same species, confirming the well-developed dispersal capabilities reported in other congeneric taxa. In addition, we include a complete description of living features and morphological characters (including scanning and transmission electron microscopy) of O. deceptionensis, a species originally described from a single mature female, and compare it to information available for other congeneric OTUs.
Stable carbon and nitrogen isotope ratios in the skeletal elements of both ancient and modern marine species from the Beagle Channel were used to compare the structure of Late Holocene and modern food webs, and predict potential changes as a result of a Sea Surface Temperature (SST) increase in the region. Complementary, ancient and modern shells of limpets and mussels were isotopically analysed to explore changes in the isotopic baseline and compare marine food webs through time after an appropriate correction for baseline shifts. Results confirmed a declining pattern of marine primary productivity during the Late Holocene in the Beagle Channel. In general, the isotopic niches overlapped largely in the ancient food web in comparison to the current marine one, with the exception of that of cormorants (Phalacrocorax sp.). Our data suggest that all the species that have undergone intense human exploitation (Arctocephalus australis, Otaria flavescens and Merluccius sp.) significantly increased their trophic levels. The most important finding of this work was the very high isotopic overlap between snoek (Thyrsites atun) and hake (Merluccius sp.) during the Late Holocene. Increasing SST as a result of global warming could favour the recolonization of the southern South‐Western Atlantic Ocean by snoek from the South‐Eastern Pacific Ocean, with a potential impact on the landings of the economically important Argentine and Austral hake. These findings highlight the relevance of using zooarchaeological remains for providing predictions about marine food webs changes in the near future.
Invertebrate and microbial marine communities associated with mammal bones are interesting and poorly understood habitats, mainly known from studies on deep-water whale remains. In order to characterize these communities in the shallow-water Mediterranean, we present here the results of a pioneering experiment using mammal bones. Minke whale, pig and cow bones were experimentally deployed on three different background communities: rocky substrate, soft-bottom and a Posidonia oceanica meadow. Bones were deployed for a year at about 20 m depth and collected every 3 months, and the invertebrate fauna colonizing the bones was identified to the lowest possible taxonomic level. As expected, mammal bones showed remarkable differences when compared with background communities. Within bones, four different clusters could be identified, primarily on the basis of the polychaete fauna, the most abundant and diverse group in the survey. Clusters A1-A3 corresponded to high to moderately altered successional stages composed by a fauna closer to that of anthropogenically enriched shallow-water environments. These clusters were characterized by the occurrence of the opportunist polychaetes Ophryotrocha puerilis, Neanthes caudata (Cluster A1), Protodorvillea kefersteini (Cluster A2) and Ophryotrocha alborana (Cluster A3). Cluster B was characterized by the presence of the polychaete Oxydromus pallidus together with typical invertebrate background fauna, which suggests that this community, after a year of deployment, was closer to that found in natural conditions. As opposed to similar shallow-water studies in other geographic areas, no occurrence of the polychaete Osedax (commonly known as bone-eating worms) was reported from our experiments. Apart from the study on the invertebrate communities, insights about the population dynamics of three of the most abundant species (O. puerilis, O. alborana, N. caudata) are given as well as remarks on a hypothetical trophic network based on fecal pellet analysis.
Stable isotope ratios of C and N in the bone tissue of three different skeletal elements (angular, cleithrum and vertebra) of three fish species from different evolutionary lineages (Clupeiformes, Atheriniformes and Notothenioidei) were determined before (δ C and δ N ) and after demineralization and delipidation (δ C and δ N ). One of the species had cellular bone and the other two had acellular bone. Results revealed that δ N and δ C values from different skeletal elements were interchangeable in species with acellular bone, but caution was needed in species with cellular bone, as δ N values varied among skeletal elements. Furthermore, δ N values were significantly lower than δ N values in the three species, thus suggesting that they are not comparable. This difference is probably because δ N refers to total bone protein and δ N to collagen only.
Fish skeletal remains recovered from two archaeological sites dated in the Middle Holocene of Tierra del Fuego (Argentina) were analysed to describe habitat use patterns by hake in the past and predict changes in a warmer world. Mitochondrial DNA was successfully extracted and amplified from 42 out of 45 first vertebra from ancient hake and phylogenetic analysis assigned all haplotypes to Argentine hake (Merluccius hubbsi). According to osteometry, the Argentine hake recovered from the archaeological site were likely adults ranging 37.2-58.1 cm in standard length. C and N stable isotope analysis showed that currently Argentine hake use foraging grounds deeper than those of Patagonian blenny and pink cusk-eel. Argentine hake, however, had a much broader isotopic niche during the Middle Holocene, when a large part of the population foraged much shallower than contemporary pink cusk-eel. The overall evidence suggests the presence of large numbers of Argentine hake onshore Tierra del Fuego during the Middle Holocene, which allowed exploitation by hunter-gatherer-fisher groups devoid of fishing technology. Interestingly, average SST off Tierra del Fuego during the Middle Holocene was higher than currently (11 °C vs 7 °C) and matched SST in the current southernmost onshore spawning aggregations, at latitude 47 °S. This indicates that increasing SST resulting from global warming will likely result into an increased abundance of adult Argentine hake onshore Tierra del Fuego, as during the Middle Holocene. Furthermore, stable isotope ratios from mollusc shells confirmed a much higher marine primary productivity during the Middle Holocene off Tierra del Fuego. Keywords Hake • Osteometry • Stable isotopes • Tierra del Fuego • ZooarchaeologyCommunicated by Leon A. Barmuta.
Over the past several years, there has been growing interest in how bones of decaying mammals are colonized in the marine seabed. One of the most common opportunistic taxa occurring worldwide on bones is dorvilleid polychaetes of the genus Ophryotrocha. In a recent study in the Mediterranean, Ophryotrocha puerilis and Ophryotrocha alborana were two of the most abundant species occurring in experimentally deployed bones. These species have direct development and this makes them a suitable model to study the mechanisms and processes allowing organisms lacking a dispersive larval phase to colonize new substrates. Here, we address the colonization processes at the molecular level for populations of O. puerilis and O. alborana on experimentally deployed mammal bones in the shallow‐water Mediterranean collected over a year at 3‐month intervals. High genetic distances between some of the O. puerilis organisms collected indicated the occurrence of at least two cryptic sibling species (O. puerilis ‘Shallow’ and O. puerilis ‘Deep’) apart from O. puerilis sensu stricto. This was corroborated with phylogenetic analyses using an alignment of three concatenated genes (COI, 16S, H3) and with species delimitation analyses using COI. The haplotype network inferred from COI sequences for O. puerilis ‘Shallow’ showed a few common haplotypes shared between the two trimesters analysed and several other less represented haplotypes only present in one trimester. Thus, colonization of these experimental bones may have been achieved by a few organisms that arrived to the bones and were able to reseed, and by several individuals arriving to the experimental bones and not persisting across time. In contrast, the haplotype network for O. alborana revealed that none of the haplotypes present in three different trimesters were shared, suggesting that the populations arriving at the bones during each trimester were totally replaced by new individuals during the subsequent trimesters. Our study suggests that different species of shallow‐water Ophryotrocha occurring in the Mediterranean may have different patterns of substrate colonization despite sharing similar life histories.
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