Alan J. Jamieson

Hadal trenches: the ecology of the deepest places on Earth

Hadal trenches account for the deepest 45% of the oceanic depth range and host active and diverse biological communities. Advances in our understanding of hadal community structure and function have, until recently, relied on technologies that were unable to document ecological information. Renewed international interest in exploring the deepest marine environment on Earth provides impetus to re-evaluate hadal community ecology. We review the abiotic and biotic characteristics of trenches and offer a contemporary perspective of trench ecology. The application of existing, rather than the generation of novel, ecological theory offers the best prospect of understanding deep ocean ecology.

Marine fish may be biochemically constrained from inhabiting the deepest ocean depths

Significance Fish appear to be absent from the oceans greatest depths, the trenches from 8,400–11,000 m. The reason is unknown, but hydrostatic pressure is suspected. We propose that the answer is the need for high levels of trimethylamine oxide (TMAO, common in many marine animals), a potent stabilizer capable of counteracting the destabilization of proteins by pressure. TMAO is known to increase with depth in bony fishes (teleosts) down to 4,900 m. By capturing the worlds second-deepest known fish, the hadal snailfish Notoliparis kermadecensis from 7,000 m, we find that they have the highest recorded TMAO contents, which, moreover, yield an extrapolated maximum for fish at about 8,200 m. This is previously unidentified evidence that biochemistry may constrain depth for a large taxonomic group. No fish have been found in the deepest 25% of the ocean (8,400–11,000 m). This apparent absence has been attributed to hydrostatic pressure, although direct evidence is wanting because of the lack of deepest-living species to study. The common osmolyte trimethylamine N-oxide (TMAO) stabilizes proteins against pressure and increases with depth, going from 40 to 261 mmol/kg in teleost fishes from 0 to 4,850 m. TMAO accumulation with depth results in increasing internal osmolality (typically 350 mOsmol/kg in shallow species compared with seawaters 1,100 mOsmol/kg). Preliminary extrapolation of osmolalities of predicted isosmotic state at 8,000–8,500 m may indicate a possible physiological limit, as greater depths would require reversal of osmotic gradients and, thus, osmoregulatory systems. We tested this prediction by capturing five of the second-deepest known fish, the hadal snailfish (Notoliparis kermadecensis; Liparidae), from 7,000 m in the Kermadec Trench. We found their muscles to have a TMAO content of 386 ± 18 mmol/kg and osmolality of 991 ± 22 mOsmol/kg. These data fit previous extrapolations and, combined with new osmolalities from bathyal and abyssal fishes, predict isosmotic state at 8,200 m. This is previously unidentified evidence that biochemistry could constrain the depth of a large, complex taxonomic group.

Liparid and macrourid fishes of the hadal zone: in situ observations of activity and feeding behaviour

Using baited camera landers, the first images of living fishes were recorded in the hadal zone (6000–11 000 m) in the Pacific Ocean. The widespread abyssal macrourid Coryphaenoides yaquinae was observed at a new depth record of approximately 7000 m in the Japan Trench. Two endemic species of liparid were observed at similar depths: Pseudoliparis amblystomopsis in the Japan Trench and Notoliparis kermadecensis in the Kermadec Trench. From these observations, we have documented swimming and feeding behaviour of these species and derived the first estimates of hadal fish abundance. The liparids intercepted bait within 100–200 min but were observed to preferentially feed on scavenging amphipods. Notoliparis kermadecensis act as top predators in the hadal food web, exhibiting up to nine suction-feeding events per minute. Both species showed distinctive swimming gaits: P. amblystomopsis (mean length 22.5 cm) displayed a mean tail-beat frequency of 0.47 Hz and mean caudal : pectoral frequency ratio of 0.76, whereas N. kermadecensis (mean length 31.5 cm) displayed respective values of 1.04 and 2.08 Hz. Despite living at extreme depths, these endemic liparids exhibit similar activity levels compared with shallow-water liparids.

Bioaccumulation of persistent organic pollutants in the deepest ocean fauna

The legacy and reach of anthropogenic influence is most clearly evidenced by its impact on the most remote and inaccessible habitats on Earth. Here we identify extraordinary levels of persistent organic pollutants in the endemic amphipod fauna from two of the deepest ocean trenches (>10,000 metres). Contaminant levels were considerably higher than documented for nearby regions of heavy industrialization, indicating bioaccumulation of anthropogenic contamination and inferring that these pollutants are pervasive across the world’s oceans and to full ocean depth.

Bone-eating worms from the Antarctic: the contrasting fate of whale and wood remains on the Southern Ocean seafloor.

We report the results from the first experimental study of the fate of whale and wood remains on the Antarctic seafloor. Using a baited free-vehicle lander design, we show that whale-falls in the Antarctic are heavily infested by at least two new species of bone-eating worm, Osedax antarcticus sp. nov. and Osedax deceptionensis sp. nov. In stark contrast, wood remains are remarkably well preserved with the absence of typical wood-eating fauna such as the xylophagainid bivalves. The combined whale-fall and wood-fall experiment provides support to the hypothesis that the Antarctic circumpolar current is a barrier to the larvae of deep-water species that are broadly distributed in other ocean basins. Since humans first started exploring the Antarctic, wood has been deposited on the seafloor in the form of shipwrecks and waste; our data suggest that this anthropogenic wood may be exceptionally well preserved. Alongside the new species descriptions, we conducted a comprehensive phylogenetic analyses of Osedax, suggesting the clade is most closely related to the frenulate tubeworms, not the vestimentiferans as previous reported.

The Effects of Natural Iron Fertilisation on Deep-Sea Ecology: The Crozet Plateau, Southern Indian Ocean

The addition of iron to high-nutrient low-chlorophyll (HNLC) oceanic waters stimulates phytoplankton, leading to greater primary production. Large-scale artificial ocean iron fertilization (OIF) has been proposed as a means of mitigating anthropogenic atmospheric CO2, but its impacts on ocean ecosystems below the photic zone are unknown. Natural OIF, through the addition of iron leached from volcanic islands, has been shown to enhance primary productivity and carbon export and so can be used to study the effects of OIF on life in the ocean. We compared two closely-located deep-sea sites (∼400 km apart and both at ∼4200 m water depth) to the East (naturally iron fertilized; +Fe) and South (HNLC) of the Crozet Islands in the southern Indian Ocean. Our results suggest that long-term geo-engineering of surface oceanic waters via artificial OIF would lead to significant changes in deep-sea ecosystems. We found that the +Fe area had greater supplies of organic matter inputs to the seafloor, including polyunsaturated fatty acid and carotenoid nutrients. The +Fe site also had greater densities and biomasses of large deep-sea animals with lower levels of evenness in community structuring. The species composition was also very different, with the +Fe site showing similarities to eutrophic sites in other ocean basins. Moreover, major differences occurred in the taxa at the +Fe and HNLC sites revealing the crucial role that surface oceanic conditions play in changing and structuring deep-sea benthic communities.

A Large Aggregation of Liparids at 7703 meters and a Reappraisal of the Abundance and Diversity of Hadal Fish

Few biological studies have investigated the hadal depths within oceanic trenches that plummet from 6000 meters (m) to the full ocean depth of almost 11,000 m. Here we present the deepest known in situ observations of fish: a hadal snailfish, Pseudoliparis amblystomopsis (Andriashev 1955), from 7703-m deep in the Japan Trench, which was obtained using a baited video lander. The maximum number of fish we observed was unexpectedly higher than trawl catch records of any known hadal fish. We describe changes in fish abundance and associated behaviors over time, including feeding, resting, and swimming. In light of these new observations, we reappraise the occurrence and diversity records of hadal fishes that have been constructed from fragmentary and often misleading information derived from historical explorations and global data sets. This reappraisal suggests that hadal fish diversity may be lower—although some hadal fish species may attain much larger populations—than previously thought.

High swimming and metabolic activity in the deep-sea eel Synaphobranchus kaupii revealed by integrated in situ and in vitro measurements.

Several complementary studies were undertaken on a single species of deep‐sea fish (the eel Synaphobranchus kaupii) within a small temporal and spatial range. In situ experiments on swimming and foraging behaviour, muscle performance, and metabolic rate were performed in the Porcupine Seabight, northeast Atlantic, alongside measurements of temperature and current regime. Deep‐water trawling was used to collect eels for studies of animal distribution and for anatomical and biochemical analyses, including white muscle citrate synthase (CS), lactate dehydrogenase (LDH), malate dehydrogenase (MDH), and pyruvate kinase (PK) activities. Synaphobranchus kaupii demonstrated whole‐animal swimming speeds similar to those of other active deep‐sea fish such as Antimora rostrata. Metabolic rates were an order of magnitude higher (31.6 mL kg−1 h−1) than those recorded in other deep‐sea scavenging fish. Activities of CS, LDH, MDH, and PK were higher than expected, and all scaled negatively with body mass, indicating a general decrease in muscle energy supply with fish growth. Despite this apparent constraint, observed in situ burst or routine swimming performances scaled in a similar fashion to other studied species. The higher‐than‐expected metabolic rates and activity levels, and the unusual scaling relationships of both aerobic and anaerobic metabolism enzymes in white muscle, probably reflect the changes in habitat and feeding ecology experienced during ontogeny in this bathyal species.

Measurement of in situ oxygen consumption of deep-sea fish using an autonomous lander vehicle

Conventional laboratory studies of deep-sea fish metabolism are not possible as these fish are typically killed during recovery to the surface. As these species are important members of deep-sea communities, the lack of these data represents a significant limitation to our understanding of the functioning of this ecosystem. An autonomous fish respirometer vehicle was developed in order to measure the oxygen consumption of deep-sea fish in situ. This new lander allows measurements to be made without handling or stressing the animals and without the logistical problems and great cost of submersible operations. The design, operation, and measurement methodology are described and preliminary data for Coryphaenoides armatus at 4000 m are presented. These Atlantic data appear to confirm the low metabolic rate measured in this species when compared to other gadid species.

In situ investigation of burst swimming and muscle performance in the deep-sea fish Antimora rostrata (Gunther, 1878)

The few existing measurements of deep-sea fish physiology consistently indicate reduced basal metabolism and metabolic power. A possible explanation for this is the reduction in selective pressure for burst activity capacity due to a reduction in the frequency and duration of predator-prey interactions in the sparsely distributed fish community and continuous darkness. Video recordings of stimulated fast-starts in deep-sea fish were obtained by a lander vehicle and analysed to give the swimming velocities, accelerations, and inertial power requirements of fast-start swimming in Antimora rostrata. With a mean peak velocity of 0.7 m s(-1), and white muscle power output of only 17.0 W kg(-1). A. rostrata is a slow moving fish, but no slower than shallow-water fishes at the same temperature.