Whale-fall Research Articles

The first whale fall on the Mid-Atlantic Ridge: Monitoring a year of succession

While the Mid-Atlantic Region is a frequented migration route for multiple cetacean species, to date no whale falls have been encountered or studied in the area. In 2015, a juvenile sperm whale was sunk south of Faial (Azores, Portugal), implanted at 760m depth and its decomposition was monitored for one year with seven submersible dives. Based on imagery, two different successional stages were observed: the mobile/scavenging stage characterised by sharks and 3 different species of decapods and the enrichment/opportunistic stage, dominated by polychaetes. While all scavengers were known background fauna for the region, whale fall specialist fauna was observed during the enrichment-opportunistic stage, including bone-eating worms (Osedax spp.). After one year at the bottom, a vertebra and a rib were sampled to assess the species composition. While all Polychaeta, Arthropoda and Mollusca families were known from whale falls, few could be identified to species level, indicating species new to science. Based on the presence of sulphide tolerant organisms (Mytilidae aff. Bathymodiolinae and Polycladida, Platyhelminthes) in the samples, a transition to the chemosynthetic-based stage appeared to have been initiated. Taxon overlap at genus and possible species level of some Polychaeta was observed with the cow fall off the coast of Portugal (Ophryotrocha cf. lusa and O. cf. sadina) and with the whale fall off the coast of Brazil (Pleijelius, Sirsoe syn. Vrijenhoekia), thus connecting both sides of the Atlantic Ocean.

Whale Fall Café by Jacquie Sewell

Whale Fall Café by Jacquie Sewell

Whale Falls, Suspended Ground, and Extinctions Never Known

AbstractThis article contributes to work within extinction studies by asking how one might “story” extinctions of creatures that have been, and will remain, unknown. It grapples with losses that have been unrecorded, unmissed, and unrecognizable via the “lively ethography” approach to storying extinction. This approach, developed by Deborah Bird Rose and Thom van Dooren, seeks to draw readers into imaginative encounters with embodied, specific, and lively creatures to support situated ethical responses. While at first this approach might seem antithetical to exploring unknown extinctions, this article argues that it can provide an important stimulus for developing a situated approach to losses that are often thought of in terms of undifferentiated masses. The article’s focus is on the recently discovered ecosystems of creatures that live on the remnants of dead whales on the sea floor, which are known as “whale falls.” It reads these ecosystems via a notion of “suspended ground,” which brings together philosopher Mick Smith’s rethinking of an ethics of encounter with unknown soil extinctions and Stacy Alaimo’s concept of “suspension.” The article argues that engaging with ethographic writing from this perspective enables one to weave a more explicit account of the mysterious and the unknown into the approach.

From wood to vent: first cocculinid limpet associated with hydrothermal activity discovered in the Weddell Sea

AbstractLush ‘oases’ of life seen in chemosynthetic ecosystems such as hot vents and cold seeps represent rare, localized exceptions to the generally oligotrophic deep ocean floor. Organic falls, best known from sunken wood and whale carcasses, are additional sources of such oases. Kemp Caldera (59°42'S, 28°20'W) in the Weddell Sea exhibits active hydrothermal vents and a natural whale fall in close proximity, where an undescribed cocculinid limpet was found living in both types of chemosynthetic habitats. This represents the first member of the gastropod order Cocculinida discovered from hot vents, and also the first record from the Southern Ocean. Here, we applied an integrative taxonomy framework incorporating traditional dissection, electron microscopy, genetic sequencing and 3D anatomical reconstruction through synchrotron computed tomography in order to characterize this species. Together, our data revealed an unusual member of the genusCocculinawith a highly modified radula for feeding on bacterial film, described herein asCocculina enigmadontan. sp. Its phylogenetically derived position within the largely wood-inhabitingCocculinaindicates that it probably evolved from an ancestor adapted to living on sunken wood, providing a compelling case of the ‘stepping stone’ evolutionary trajectory from organic falls to seeps and vents.

John McCutcheon

John McCutcheon

Whale fall: the Creation of A Unique Marine Ecosystem

When a whale dies in the ocean, its body slowly sinks to the bottom of the sea. In this process, animals and decomposers gather in the ocean to form an ecosystem. Biologists call this unique process "whale fall." Whale fall, together with ocean cold spring and hydrothermal fluid, is called the "oasis" of the ocean.  Whale carcasses provide a rich source of food for all types of consumers in the vast and barren deep-sea food chain, including deep-sea fish, crustaceans, polychaetes and various small organisms.  This review introduces the necessary conditions, causes and ecological characteristics of whale fall from various perspectives, and analyzes the impact of whale fall on the ocean; A large number of facts show that whale fall not only provides a huge driving force for the marine carbon flux, but also promotes the production of new species and enriches the diversity of marine organisms. Whale falling is a wonderful creation of nature. It is of great significance to understand this phenomenon for us to understand this unique marine ecosystem.

Diversity of bone-eating Osedax worms on the deep Atlantic whale falls—bathymetric variation and inter-basin distributions

Bone-eating Osedax worms can quickly colonize exposed bones and are important ecosystem engineers in whale fall communities, contributing to cause of bone degradation. This study shows that the deep SW Atlantic margin harbors many Osedax species. Using DNA barcoding, we found four putative new lineages as well as O. frankpressi Rouse, Goffredi, and Vrijenhoek, 2004 and O. braziliensis Fujiwara, Jimi, Sumida, Kawato, & Kitazato, 2019, with assemblages varying with depth. It is probable that the bathymetric distributions of these species are controlled by different water masses and their directions of flow. The haplotype network of Atlantic and Pacific O. frankpressi populations suggests segregation between populations, as is also seen in the high FST. However, the low p distance between both populations and the few substitution sites separating haplogroups from both regions (Atlantic and Pacific) could be evidence that populations of both basins are somehow close to each other. It is likely that whale fall habitats exist between both populations analyzed, connecting both basins.

Diversity, Distribution and Phylogeny of Hesionidae (Annelida) Colonizing Whale Falls: New Species of Sirsoe and Connections Between Ocean Basins

Whale falls are important environments contributing to biodiversity, connectivity and evolutionary novelty in deep-sea ecosystem. Notwithstanding, most of this knowledge is based in studies from NE Pacific basin. Interestingly, the only known natural whale fall on the SW Atlantic has faunal composition affinities with carcasses from other deep-ocean basins. In this carcass, annelid worms belonging to Hesionidae are abundant and species-rich, and include some shared species with NE Pacific Ocean. Here we evaluate the diversity of Hesionidae on the SW Atlantic using new information of implanted whale bones and explore whether some species have interbasin distribution or if they represent cryptic species in different basins. We described, using morphological and molecular data, a total of 10 new hesionid species and report of a new lineage Sirsoe ‘BioSuOr,’ not formally described herein. Two hesionids found exclusively in deep-sea chemosynthetic environments, SirsoePleijel (1998) and VrijenhoekiaPleijel et al. (2008), are primarily distinguished from each other by the presence of a median antenna on the former and its absence on the latter. However, our analyses showed that Vrijenhoekia should be synonymized with Sirsoe and for this reason we emended the diagnosis of Sirsoe. We also emphasized the presence of Sirsoe balaenophila comb. nov. and S. sirikos in SW Atlantic whale falls confirming their interbasin distribution. Moreover, COI and 16S rDNA data reveal that S. balaenophila comb. nov. also comprises cryptic species on the SW Atlantic (S. pirapuan sp. nov. and S. ypupiara sp. nov) and perhaps also in the Pacific Ocean (herein named as S. balaenophila lineage-2). The new species, S. maximiano, is shared between whale falls from SW Atlantic and vent sites from Mid-Cayman Spreading Center. Our data adds to the growing literature showing species are shared between deep ocean basins and among cognate deep-sea environments. Zoobank registration publication LSID - urn:lsid:zoobank.org:pub:7E891B1D-DCE4-45C8-83F4-8586D286B327.

Western North Atlantic humpback whale fall and spring acoustic repertoire: Insight into onset and cessation of singing behavior.

Humpback whale songs have been described worldwide and studies exploring non-song vocal behavior continue to expand; however, studies on the transition periods when whales shift to and from the seasonal behavioral state of singing are lacking and may be potentially informative regarding the proximal factors controlling the onset and offset of humpback whale male singing. Acoustic recorders collected data off eastern Canada continuously from the Bay of Fundy in the fall of 2015 and near-continuously off northeast Nova Scotia in the spring of 2016. Humpback whale acoustic occurrence and behavior were identified by systematically reviewing a subset of acoustic recordings for presence before analyzing the highest quality recordings for behavior. The onset of singing in the fall was gradual over a period of about three weeks with an intermediate form, termed "song fragment," occurring prior to full songs. In comparison, singing in the spring seemed to end abruptly with few song fragments. Song fragments could be produced by juveniles learning to sing for the first time or mature males preparing for breeding activities prior to migrating to southern breeding grounds. The authors propose an alternative hypothesis that the timing and manner of transitions could be driven by physiological processes similar to those documented in songbirds.

Evidence of selective pressure in whale fall microbiome proteins and its potential application to industry

The present study addresses the microbiome of the first whale fall (YOKO 16) that has been described in the deep sea in the southern Atlantic Ocean (São Paulo Plateau; 4204 m depth), in terms of its metabolic uniqueness. Sets of ten thousand protein sequences from YOKO 16 and 29 public domain metagenomes (SRA and GenBank databases) that represent various marine, terrestrial and gut-associated microbial communities were analyzed. The determination of protein functionality, based on the KAAS server, indicated that the YOKO 16 microbiome has industrially-relevant proteins, such as proteases and lipases, that have low similarity (~50%) with previously-described enzymes. The amino acid usage in the YOKO 16 protein sequences (based on blastp and Clustal analysis) revealed a pattern of preference similar to that of extremophiles, with an increased usage of polar, charged and acidic amino acids and a decreased usage of nonpolar residues. We concluded that the targeted microbiome is of potential biotechnological use, which justifies the allocation of resources for the discovery of enzymes in deep-sea whale fall communities.

Trophic structure and chemosynthesis contributions to heterotrophic fauna inhabiting an abyssal whale carcass

The trophic structure and role of chemosynthesis remain unexplored in deep-sea whale-fall communities in areas other than the California margin. This gap limits the understanding of these communities and their ecological relationships with other chemosynthetic ecosystems, such as vents and seeps. Here, we studied 3 different whale skeleton microhabitats with hypothesized high, intermediate and low reducing conditions as well as the sediments surrounding an abyssal whale fall (4204 m depth, SW Atlantic Ocean). We analyzed trophic structures (δ13C and δ15N) and the contribution of chemosynthetically derived carbon to heterotrophic species. The high and intermediate reducing microhabitats harbored food webs dominated by consumers of chemosynthetic production, similar to those of diffusive areas of hydrothermal vents and seeps. Both the low reducing microhabitat and the sediments harbored food webs with greater trophic complexity, dominated by higher consumers mainly relying on whale and/or photosynthesis-derived organic matter, a type of food web commonly reported in small whale, wood and kelp falls. The main whale-fall ecosystem engineer, the bone-eating worm Osedax, appeared to produce unique food web effects not observed in other chemosynthetic habitats. We conclude that whale falls provide the deep sea with a mosaic of microhabitats that supports assemblages with different chemosynthesis reliance levels and trophic structures, similar to those found at vents and seeps. Such a mosaic allows species-rich communities with numerous trophic levels to develop in a very small area of the food-limited deep sea.

Dominance of Epsilonproteobacteria associated with a whale fall at a 4204 m depth – South Atlantic Ocean

The deep ocean is the largest marine environment on Earth and is home to a large reservoir of biodiversity. Within the deep ocean, large organic falls attract a suite of metazoans and microorganisms, which form an important community that, in part, relies on reduced chemical compounds. Here, we describe a deep-sea (4204m) microbial community associated with sediments collected underneath a whale fall skeleton in the South Atlantic Ocean. Metagenomic analysis of 1Gb of Illumina HiSeq. 2000 reads, including taxonomic and functional genes, was performed by using the MG-RAST pipeline, SEED, COG and the KEGG database. The results showed that Proteobacteria (79%) was the main phylum represented. The most dominant bacterial class in this phylum was Epsilonproteobacteria (69%), and Sulfurovum sp. NBC37-1 (97%) was the dominant species. Different species of Epsilonproteobacteria have been described in marine and terrestrial environments as important organisms for nutrient cycling. Functional analysis revealed key genes for nitrogen and sulfur cycles, including protein sequences for Sox system (sulfur oxidation) enzymes. These enzymes were mainly those of the Epsilonproteobacteria, indicating their importance for nitrogen and sulfur cycles and the balance of nutrients in this environment.

First record of the genus Adipicola (Mollusca: Bivalvia: Mytilidae) and description of a new species from the Argentine SW Atlantic Ocean

This work describes a new species of a whale fall mytilid, Adipicola leticiae n. sp., which was found on the skull of a sei whale, Balaenoptera borealis, collected by a trawling vessel off the Gulf of San Jorge, Argentina. The species represents the first record of a deep water mytilid living on organic remains from the Argentine Sea. The new species is characterized by its combination of an elongated and fragile shell of up to 20 mm in length, lack of periostracal hair, lack of hinge teeth and crenulations, and its straight ventral margin. Adipicola leticiae is morphologically compared to other Bathymodiolinae. Current problems of delimiting Adipicola from Idas and Terua are outlined.

Paramytha ossicola sp. nov. (Polychaeta, Ampharetidae) from mammal bones: Reproductive biology and population structure

Sunken whale carcasses, known as “whale falls”, deliver large, but relatively ephemeral pulses of organic material to the seafloor and serve as habitat for unique assemblages of deep-sea fauna that include generalist-scavenging species, chemosynthetic fauna and bone-specialist species. Despite the great deal of interest that fauna associated with whale falls have attracted, very little is known about this fauna in the deep Atlantic Ocean. Here we describe a new species of Ampharetidae that was found in an experiment using cow carcasses in the Setúbal Canyon (NE Atlantic), as a surrogate of a whale fall. Further, we analyse the size and structure of the population at two different times and use histological analyses to investigate the reproductive biology of this new species. We propose that Paramytha ossicola sp. nov. is a bone-specialist adapted for life in ephemeral habitats. Reproductive traits include rapid maturation, continuous and non-synchronous gametogenesis. Recruitment seems to be controlled by habitat availability and biological interactions that result in post-settlement mortality.

Colwellia and sulfur-oxidizing bacteria: An unusual dual symbiosis in a Terua mussel (Mytilidae: Bathymodiolinae) from whale falls in the Antilles arc

Seven individuals of a single morphotype of mussels (Bivalvia: Mytilidae) were found attached to a naturally sunken whale intervertebral disk collected in Guadeloupe (Caribbean) at 800m depth. These specimens resemble small Idas mussels which are found worldwide at cold seeps and hydrothermal vents, and typically harbor ectosymbiotic bacteria on their gills upon which they depend for nutrition. Based on multi-locus gene sequencing, these specimens appear to belong to a new species closely related to two species now included within the genus Terua. Unexpectedly, its closest relatives are found in the Pacific, questioning how this species has reached the Antilles arc. Based on marker gene sequence analysis, electron and fluorescence microscopy, Terua n. sp. harbors two distinct and abundant extracellular bacterial symbionts located between microvilli at the apical surface of host gill epithelial cells. One is a sulfur-oxidizing bacterium similar to the symbionts previously identified in several deep-sea mussels, while the other is related to Colwellia species, a group of cold-adapted heterotrophic bacteria able to degrade organic compounds. This study provides the first evidence for the existence of a dual symbiosis in mussels from whale fall ecosystems in the Caribbean. The evolutionary history of Terua n. sp. and potential role of its Colwellia symbionts are discussed.

Deep-sea whale fall fauna from the Atlantic resembles that of the Pacific Ocean.

Whale carcasses create remarkable habitats in the deep-sea by producing concentrated sources of organic matter for a food-deprived biota as well as places of evolutionary novelty and biodiversity. Although many of the faunal patterns on whale falls have already been described, the biogeography of these communities is still poorly known especially from basins other than the NE Pacific Ocean. The present work describes the community composition of the deepest natural whale carcass described to date found at 4204 m depth on Southwest Atlantic Ocean with manned submersible Shinkai 6500. This is the first record of a natural whale fall in the deep Atlantic Ocean. The skeleton belonged to an Antarctic Minke whale composed of only nine caudal vertebrae, whose degradation state suggests it was on the bottom for 5–10 years. The fauna consisted mainly of galatheid crabs, a new species of the snail Rubyspira and polychaete worms, including a new Osedax species. Most of the 41 species found in the carcass are new to science, with several genera shared with NE Pacific whale falls and vent and seep ecosystems. This similarity suggests the whale-fall fauna is widespread and has dispersed in a stepping stone fashion, deeply influencing its evolutionary history.

Cohn, Scotti, illustrated byBersani, Shennen. 2014. Animal Partners. Abordale Publishing,Mount Pleasant, SC, USA, ISBN 978‐1628554564, 32 pp., $9.95, PBKurtz, Kevin, illustrated byHunter, Erin E. 2013. A Day in the Deep. Sylvan Dell Publishing,Mount Pleasant, SC, USA, ISBN‐13 978‐1607186298, 32 pp., $9.95, PB

I was pleasantly surprised to see both “Animal Partners” and “Day in the Deep” by Arbordale Publishing because too many children's books do not convey accurate science or may not reflect the most intriguing scientific discoveries. As an oceanographer, I want my field to be accessible and exciting for children and, personally, to be able to read science books to the young people in my life. As a sampling of what science-related books Arbordale Publishing has to offer, “Animal Partners” and “A Day in the Deep” mostly achieve those goals. Both books are a short collection of vignettes on each page spread; “Animal Partners” describes a different land or water-based animal symbiosis while “Day in the Deep” illustrates symbioses in 500-foot depth increments from the ocean surface to the seafloor. In both books, there are no introductory comments, no linkages between vignettes such that each stands on its own, nor a conclusion to tie all of the individual vignettes together, which represents a missed opportunity for synthesis and conceptual learning. Strengths of these books include their scientific accuracy, both in text and illustration, and their curriculum connections. For these reasons, they are good supplemental out-of-class learning experiences. The content of the books is aligned into the Common Core and Next Generation Science Standards, and standards alignment is available on the publisher's website. The books have 4 pages of interactive review activities at the end of the book and an additional teaching activities guide (publisher's website). I put my deep-sea biology experience to the test as I critically reviewed “A Day in the Deep” for scientific accuracy, and I can attest to the fact that this book is scientifically sound. The best stories in “Animal Partners” explain the biological interactions of the symbiosis (almost all mutualisms). Likewise, my least favorite stories just describe two creatures living together without an explanation for the nature of the symbiosis. For instance, one vignette discusses how barnacles can live on shells of sea turtles, but the reader learns nothing about the commensal relationship. A microbiologist like myself will be disappointed to not find any vignettes about microbe-animal symbioses. “A Day in the Deep” describes deep-sea adaptations for some of the world's weirdest-looking critters, including the gulper eel, the deep-sea angler fish (and her parasitic males), and the viperfish, all critters whose day in the sun has finally come. I was pleasantly surprised to see a vignette about a whale fall, but, sadly, it failed to hint at chemosynthesis. The author missed a fantastic opportunity for generating interest in ocean discovery when the illustrator put in three pictures of an ROV (resembling Jason) but failed to even mention ROVs in the text. Although the books had a few shortcomings in promoting conceptual learning, I am still excited to share these aquatic science children's books with the young people in my life! Rachel E. A. Horak, American Society for Microbiology, 8901B Connecticut Ave., Chevy Chase, MD 20815 USA; rahorak@gmail.com

Seven-year enrichment: macrofaunal succession in deep-sea sediments around a 30 tonne whale fall in the Northeast Pacific

Whale falls cause massive organic and sulfide enrichment of underlying sediments, yielding energy-rich conditions in oligotrophic deep-sea ecosystems. While the fauna colonizing whale skeletons has received substantial study, sediment macrofaunal community response to the geochemical impacts of deep-sea whale falls remains poorly evaluated. We present a 7 yr case study of geochemical impacts, macrofaunal community succession, and chemoautotrophic community persistence in sediments around a 30 t gray-whale carcass implanted at 1675 m in the well-oxygenated Santa Cruz Basin on the California margin. The whale fall yielded intense, patchy organic-carbon enrichment (>15% organic carbon) and pore-water sulfide enhancement (>5 mM) in nearby sediments for 6 to 7 yr, supporting a dense assemblage of enrichment opportunists and chemosymbiotic vesicomyid clams. Faunal succession in the whale-fall sediments resembled the scavenger-opportunist-sulfophile sequence previously described for epifaunal communities on sunken whale skeletons. The intense response of enrichment opportunists functionally resembles responses to organic loading in shallow-water ecosystems, such as at sewer outfalls and fish farms. Of 100 macrofaunal species in the whale-fall sediments, 10 abundant species were unique to whale falls; 6 species were shared with cold seeps, 5 with hydrothermal vents, and 12 with nearby kelp and wood falls. Thus, whale-fall sediments may provide dispersal stepping stones for some generalized reducing-habitat species but also support distinct macrofaunal assemblages and contribute significantly to beta diversity in deep-sea ecosystems.

Methyloprofundus sedimenti gen. nov., sp. nov., an obligate methanotroph from ocean sediment belonging to the 'deep sea-1' clade of marine methanotrophs.

We report the isolation and growth characteristics of a gammaproteobacterial methane-oxidizing bacterium (Methylococcaceae strain WF1(T), 'whale fall 1') that shares 98 % 16S rRNA gene sequence identity with uncultivated free-living methanotrophs and the methanotrophic endosymbionts of deep-sea mussels, ≤94.6 % 16S rRNA gene sequence identity with species of the genus Methylobacter and ≤93.6 % 16S rRNA gene sequence identity with species of the genera Methylomonas and Methylosarcina. Strain WF1(T) represents the first cultivar from the 'deep sea-1' clade of marine methanotrophs, which includes members that participate in methane oxidation in sediments and the water column in addition to mussel endosymbionts. Cells of strain WF1(T) were elongated cocci, approximately 1.5 µm in diameter, and occurred singly, in pairs and in clumps. The cell wall was Gram-negative, and stacked intracytoplasmic membranes and storage granules were evident. The genomic DNA G+C content of WF1(T) was 40.5 mol%, significantly lower than that of currently described cultivars, and the major fatty acids were 16 : 0, 16 : 1ω9c, 16 : 1ω9t, 16 : 1ω8c and 16 : 2ω9,14. Growth occurred in liquid media at an optimal temperature of 23 °C, and was dependent on the presence of methane or methanol. Atmospheric nitrogen could serve as the sole nitrogen source for WF1(T), a capacity that had not been functionally demonstrated previously in members of Methylobacter. On the basis of its unique morphological, physiological and phylogenetic properties, this strain represents the type species within a new genus, and we propose the name Methyloprofundus sedimenti gen. nov., sp. nov. The type strain of Methyloprofundus sedimenti is WF1(T) ( = LMG 28393(T) = ATCC BAA-2619(T)).

Adaptation to environmental factors shapes the organization of regulatory regions in microbial communities.

BackgroundIt has been shown in a number of metagenomic studies that the addition and removal of specific genes have allowed microbiomes to adapt to specific environmental conditions by losing and gaining specific functions. But it is not known whether and how the regulation of gene expression also contributes to adaptation.ResultsWe have here characterized and analyzed the metaregulome of three different environments, as well as their impact in the adaptation to particular variable physico-chemical conditions. For this, we have developed a computational protocol to extract regulatory regions and their corresponding transcription factors binding sites directly from metagenomic reads and applied it to three well known environments: Acid Mine, Whale Fall, and Waseca Farm. Taking the density of regulatory sites in promoters as a measure of the potential and complexity of gene regulation, we found it to be quantitatively the same in all three environments, despite their different physico-chemical conditions and species composition. However, we found that each environment distributes their regulatory potential differently across their functional space. Among the functions with highest regulatory potential in each niche, we found significant enrichment of processes related to sensing and buffering external variable factors specific to each environment, like for example, the availability of co-factors in deep sea, of oligosaccharides in soil and the regulation of pH in the acid mine.ConclusionsThese results highlight the potential impact of gene regulation in the adaptation of bacteria to the different habitats through the distribution of their regulatory potential among specific functions, and point to critical environmental factors that challenge the growth of any microbial community.Electronic supplementary materialThe online version of this article (doi:10.1186/1471-2164-15-877) contains supplementary material, which is available to authorized users.