Scavenging amphipods of the Tonga Trench: an analysis of community assemblage and population structure

<p>The hadal zone is the common name for the deepest section of the ocean (6,000-11,000 m depth). It encompasses 45 % of the ocean’s depth range, and is mostly represented by oceanic trenches. Trench habitats lack sufficient sampling and the communities within are not well understood. Often, samples are derived from a single depth and thus the population dynamics of trench communities have not been analysed comprehensively. Scavenging amphipods are abundant and diverse taxa in the trench environment, and have been found in every trench sampled to date. They rapidly intercept and consume carrion falls at the deepest trench depths, and act as key prey items to predators in the shallower depths of the hadal zone. There appears to be a relationship of increasing abundance and decreasing diversity of scavenging amphipods with depth. However in the Tonga Trench, sampling of hadal amphipods has been limited, and these patterns remain unclear. The QUELLE (Quest for the Limit of Life) project in 2013 was led by The Japan Agency for Marine-Earth Science and Technology (JAMSTEC). As part of this project, the YOK 13-10 voyage examined scavenging amphipods in the Tonga Trench. The voyage used baited traps to sample depths of ˜6,250 m and ˜10,800 m from October 6 – October 21 in 2013. The main objectives of the present study were to: identify scavenging amphipod assemblages within the Tonga Trench and compare them to other trenches of the South Pacific; analyse the population structure of Hirondellea dubia between depths in the Tonga Trench; and identify a suitable total length proxy for H. dubia. Six species of amphipods were identified from depths of ˜6,250 m and ˜10,800 m in the Tonga Trench. At ˜6,250 m Alicella gigantea, Eurythenes gryllus, H. dubia, Bathycallisoma schellenbergi, an alicellid species, and a gammarid species were recovered. In contrast, H. dubia was the only species recovered from ˜10,800 m. The abundance of amphipods was higher at the ˜10,800 m site while the diversity was much lower. The assemblage of scavenging amphipods in the Tonga Trench was similar to those from past sampling efforts in the same trench. There were also similarities to the assemblages in the adjacent Kermadec Trench, and together these observations support the classification of these two trenches as a single biogeographic province. The assemblages in the Peru-Chile Trench in the South East Pacific were more dissimilar sharing only a few species. The present study provides new Tonga Trench records of the vertical ranges of A. gigantea, E. gryllus, and H. dubia. It also extends the maximum known depth of H. dubia to 10,807 m. This thesis expanded our current knowledge of A. gigantea, by reporting the first instance of this large amphipod in the Tonga Trench, and the second known instance of the species at hadal depths. An analysis of Hirondellea dubia population structure revealed ontogenetic vertical structuring in the Tonga Trench. Juveniles dominated the composition in the shallow end of the H. dubia vertical range, while very few juveniles were found at the deepest site. Juveniles were substantially smaller at ˜6,250 m compared to ˜10,800 m, and this may suggest that juveniles migrate down the trench slope with increasing age. The most likely mechanism for distributing juveniles to the shallower depths is the ascending migration of brooding females. However, this is still not certain as no brooding females were captured. The shallower depth provides a higher quality of food source and the reduced hydrostatic pressure allows for a faster metabolic rate. Thus, this distribution is likely driven by the distribution of food sources throughout the trench in combination with hydrostatic pressure. The dimensions of several established proxies for total length were evaluated for H. dubia. Pereonite 2-7 had the strongest correlation to total length, however it was highly distorted by dorsal curvature. Both the pereonite 2-7 and the pleosome were considered inaccurate due to sexual dimorphism making them inappropriate as proxies. Pereonite 1 was proportionately larger in juvenile lifestages. However, overall pereonite 1 was considered the strongest candidate for a proxy, this is because it was the least influenced by dorsal curvature and was a conspicuous segment that was easy to measure.</p>

Scavenging amphipods of the Tonga Trench: an analysis of community assemblage and population structure

<p>The hadal zone is the common name for the deepest section of the ocean (6,000-11,000 m depth). It encompasses 45 % of the ocean’s depth range, and is mostly represented by oceanic trenches. Trench habitats lack sufficient sampling and the communities within are not well understood. Often, samples are derived from a single depth and thus the population dynamics of trench communities have not been analysed comprehensively. Scavenging amphipods are abundant and diverse taxa in the trench environment, and have been found in every trench sampled to date. They rapidly intercept and consume carrion falls at the deepest trench depths, and act as key prey items to predators in the shallower depths of the hadal zone. There appears to be a relationship of increasing abundance and decreasing diversity of scavenging amphipods with depth. However in the Tonga Trench, sampling of hadal amphipods has been limited, and these patterns remain unclear. The QUELLE (Quest for the Limit of Life) project in 2013 was led by The Japan Agency for Marine-Earth Science and Technology (JAMSTEC). As part of this project, the YOK 13-10 voyage examined scavenging amphipods in the Tonga Trench. The voyage used baited traps to sample depths of ˜6,250 m and ˜10,800 m from October 6 – October 21 in 2013. The main objectives of the present study were to: identify scavenging amphipod assemblages within the Tonga Trench and compare them to other trenches of the South Pacific; analyse the population structure of Hirondellea dubia between depths in the Tonga Trench; and identify a suitable total length proxy for H. dubia. Six species of amphipods were identified from depths of ˜6,250 m and ˜10,800 m in the Tonga Trench. At ˜6,250 m Alicella gigantea, Eurythenes gryllus, H. dubia, Bathycallisoma schellenbergi, an alicellid species, and a gammarid species were recovered. In contrast, H. dubia was the only species recovered from ˜10,800 m. The abundance of amphipods was higher at the ˜10,800 m site while the diversity was much lower. The assemblage of scavenging amphipods in the Tonga Trench was similar to those from past sampling efforts in the same trench. There were also similarities to the assemblages in the adjacent Kermadec Trench, and together these observations support the classification of these two trenches as a single biogeographic province. The assemblages in the Peru-Chile Trench in the South East Pacific were more dissimilar sharing only a few species. The present study provides new Tonga Trench records of the vertical ranges of A. gigantea, E. gryllus, and H. dubia. It also extends the maximum known depth of H. dubia to 10,807 m. This thesis expanded our current knowledge of A. gigantea, by reporting the first instance of this large amphipod in the Tonga Trench, and the second known instance of the species at hadal depths. An analysis of Hirondellea dubia population structure revealed ontogenetic vertical structuring in the Tonga Trench. Juveniles dominated the composition in the shallow end of the H. dubia vertical range, while very few juveniles were found at the deepest site. Juveniles were substantially smaller at ˜6,250 m compared to ˜10,800 m, and this may suggest that juveniles migrate down the trench slope with increasing age. The most likely mechanism for distributing juveniles to the shallower depths is the ascending migration of brooding females. However, this is still not certain as no brooding females were captured. The shallower depth provides a higher quality of food source and the reduced hydrostatic pressure allows for a faster metabolic rate. Thus, this distribution is likely driven by the distribution of food sources throughout the trench in combination with hydrostatic pressure. The dimensions of several established proxies for total length were evaluated for H. dubia. Pereonite 2-7 had the strongest correlation to total length, however it was highly distorted by dorsal curvature. Both the pereonite 2-7 and the pleosome were considered inaccurate due to sexual dimorphism making them inappropriate as proxies. Pereonite 1 was proportionately larger in juvenile lifestages. However, overall pereonite 1 was considered the strongest candidate for a proxy, this is because it was the least influenced by dorsal curvature and was a conspicuous segment that was easy to measure.</p>

Biomineralization in Polychaete Annelids: A Review

Polychaete annelids are a very important group of calcifiers in the modern oceans. They can produce calcite, aragonite, and amorphous phosphates. Serpulids possess very diverse tube ultra-structures, several unique to them. Serpulid tubes are composed of aragonite or calcite or a mixture of both polymorphs. The serpulid tubes with complex oriented microstructures, such as lamello fibrillar, are exclusively calcitic, whereas tubes with prismatic structures can be composed either of calcite or aragonite. In serpulids, the calcareous opercula also have complex microstructures. Evolutionarily, calcitic serpulid taxa belong to one clade and the aragonitic taxa belong to another clade. Modern ocean acidification affects serpulid biomineralization. Serpulids are capable of biomineralization in extreme environments, such as the deepest part (hadal zone) of the ocean. The tubes of calcareous sabellids are aragonitic and have two layers, the inner irregular spherulitic prismatic layer and the outer spherulitic layer. The tube wall of cirratulids is composed of aragonitic lamellae with a spherulitic prismatic structure. In some other polychaetes, biominerals are formed in different parts of the animal body, such as chaetae or body shields, or occur within the body as granule-shaped or rod-shaped inclusions.

Megafaunal Community Structure From the Abyssal to Hadal Zone in the Yap Trench

Hadal trenches remain one of the unexplored ocean ecosystems due to the challenges of sampling at great depths. It is still unclear how a faunal community changes from the abyssal to the hadal zone, and which environmental variables are the key impacting factors. In this study, nine dives of the Human Occupied Vehicle (HOV) “JIAOLONG” were conducted from abyssal to hadal depths (4,435–6,796 m) in the Yap Trench on the southeastern boundary of the Philippine Sea Plate in the western Pacific, divided into 48,200 m video transects, to describe the megafaunal communities and reveal their relationship with environmental factors. A total of 1,171 megafauna organisms was recorded, 80 morphospecies (msps) from 8 phyla were identified based on the video data, most of which were reported for the first time in the Yap Trench. Arthropoda was the most abundant phylum and Echinodermata was the most diverse phylum of the megafaunal community. The faunal abundance increased with depth, whereas the Shannon diversity index decreased with depth. Cluster analysis suggested seven assemblages, with five abyssal groups, one mixed group, and one hadal dominant group. Although megafaunal communities changed gradually from abyssal zone to hadal zone, both PERMANOVA and PERMDISP analyses revealed that the communities are significantly different between abyssal zone and hadal zone, indicating 6,000 m as the boundary between the two depth zones. Depth, substrate, slope, and latitude were identified as four important environmental factors with significant influence on megafaunal community structure. This study proposed a transition pattern from the abyssal to hadal zone in the Yap Trench, highlighted the importance of habitat heterogeneity in structuring megafaunal community in a hadal trench.

Shift and Metabolic Potentials of Microbial Eukaryotic Communities Across the Full Depths of the Mariana Trench

Microbial eukaryotes are widespread and play important roles in marine ecosystems. However, their ecological characteristics in the deep sea (&gt;1,000 m), especially hadal trenches, were largely unknown. Here, we investigated the diversity and metabolic potentials of microbial eukaryotes along the whole water column of the Mariana Trench by metagenomics. Our results showed clear depth-related distribution of microbial eukaryotic community and associated metabolic potentials. Surface seawater was dominated by phototrophic/mixotrophic groups (e.g., Dinoflagellata) and genes involved in biosynthesis (photosynthesis and fatty acid biosynthesis), while deep (bathypelagic and/or hadal) seawaters were enriched with heterotrophic groups (e.g., Bicoecea) and genes related to digestion (lysosomal enzymes and V-type ATPase) and carbohydrate metabolism. Co-occurrence analysis revealed high intra-domain connectivity, indicating that microbial eukaryotic composition was more influenced by microbial eukaryotes themselves than bacteria. Increased abundance of genes associated with unsaturated fatty acid biosynthesis likely plays a role in resisting high hydrostatic pressure. Top1 and hupB genes, responsible for the formation and stabilization of DNA structure, were unique and abundant in the hadal zone and thus may be helpful to stabilize DNA structure in the deep sea. Overall, our results provide insights into the distribution and potential adaptability of microbial eukaryotes in the hadal zone.

Unveiling the Ocean Viromes of Challenger Deep, the Deepest Place in the World’s Oceans

Background: The hadal ocean biosphere, i.e the deepest part of the world’s oceans, harbors a unique community of cellular microbes, implying that there is also a novel assemblage of co-occurring viruses. However, the diversity and lifestyle of viroplanktons in hadal zone is poorly studied. Results: Herein, we show the unique nature of the Mariana Trench DNA virome (MTV) comprising a dataset of 95,813 non-redundant assembled viral sequences (contigs) from the ocean’s surface (2m) to the hadal zone at 8727 m below the surface. We assigned 29% of the contigs into 236 viral taxa, of which all but 3% belonged to groups with no cultured representatives. The remaining 71% of the contigs could not be assigned to a taxonomic group. The dominant viral contigs were almost more abundant in deep even hadal zone than in surface zone. The MTV is unlike any other viral assemblage described to date, and presents a novel viral ecological zone in the global ocean. The dominant viral contigs in the MTV were abundant and significantly specific in the “Trench” zone, and were associated with viruses that had signature genes indicative of a lysogenic life strategy, suggesting that horizontal gene transfer by viruses among bacteria is likely more prevelant in hadal zone than in the overlying waters. Conclusions: This study demonstrates that viruses dominating the hadal zone of the Mariana Trench are unlike those associated with other marine viral assemblages sampled to date, representing a unique ecological assemblage characterized by a lysogenic life style and horizontal gene transfer events. These results establish a foundation against which viral assemblages from other deep trenches can be compared. Keywords: Challenger Deep, Mariana Trench, ocean viromes, viral metagenomics, lysogenic life strategy, horizontal gene transfer

Scavenging amphipods from the Wallaby-Zenith Fracture Zone: Extending the hadal paradigm beyond subduction trenches

Our understanding of the ecology of the hadal zone (> 6000 m depth) is based solely on subduction trenches, leaving other geomorphological features, such as fracture zones, troughs, and basins, understudied. To address this knowledge gap, the Wallaby-Zenith Fracture Zone, Indian Ocean (WZFZ; ~ 22°S, 102°E; maximum depth 6625 m measured during Expedition SO258) was studied using free-fall baited landers. We assessed the amphipod distribution and community assemblage of this non-subduction hadal feature and compared it to subduction hadal features. Eleven species were identified across the abyssal-hadal transition zone using a paired morphological and DNA barcoding approach. The community composition was found to change gradually from abyssal to hadal depths, which contrasts with the ecotone shift characteristic of subduction trenches. A large population of Bathycallisoma schellenbergi (Birstein & Vinogradov, 1958), a quintessential hadal amphipod, was present at the flat bottom of the WZFZ. Further, an mtDNA phylogeny resolved a degree of phylogeographic structure between the B. schellenbergi WZFZ population and four previously sampled Pacific Ocean subduction trench populations, indicating these features are not interconnected through ongoing gene flow. Combined, these data indicate that some amphipods have far broader distributions than previously understood, with some species present in both hadal subduction trenches and non-subduction fracture zones and basins interspersed across the abyssal plains. This initial exploration highlights that whilst non-subduction features are an overlooked minor fraction of the total hadal area, they are essential to our understanding of the ecological and evolutionary dynamics across the hadal zone.