1. Key Points

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The Yokozuna Slickhead is the largest teleost fish (length > 250 cm) that is endemic to the deep sea at depths of over 2000 m.

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The distribution of the Yokozuna Slickhead extends to seamounts far to the south of Suruga Bay.

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The combined use of environmental DNA analyses and baited camera surveys can aid research on large, rare species that cannot be easily studied, including apex predators, and will be useful for monitoring offshore seabed nature conservation areas (marine protected areas) in the future.

2. Overview

Yoshihiro Fujiwara and colleagues of the Research Institute for Global Change at the Japan Agency for Marine–Earth Science and Technology (JAMSTEC) surveyed a deep-sea ecosystem aboard the research vessel KAIMEI in established offshore seabed nature conservation areas in Japanese waters (Fig. 1). By combining environmental DNA (eDNA) analyses and baited camera observations, the research team discovered novel habitats of the Yokozuna Slickhead (Narcetes shonanmaruae) and revealed that this species is the largest teleost fish endemic to the deep sea at depths of over 2000 m in oceans worldwide. In 2020 and 2021, the research team comprehensively surveyed the ecosystems of offshore seabed nature conservation areas designated in 2020 under the Nature Conservation Act in Japan. The goal of this survey was to acquire baseline information for the future monitoring of these protected areas and to establish a survey method for easy monitoring.

To understand the biodiversity of seamounts within offshore seabed nature conservation areas, the research team filtered a large volume of seawater collected from the deep sea using a rosette-type water sampler outfitted with a conductivity, temperature, and depth (CTD) probe and then analyzed the eDNA contained therein. The gene sequence of the Yokozuna Slickhead was detected in the seawater collected at the foot of three seamounts. This large, deep-sea fish was first reported by JAMSTEC researchers in 2021 and is known to be an apex predator in the deepest part of Suruga Bay(press releases dated January 25, 2021). All three seamounts at which the gene sequence for the Yokozuna Slickhead has now been detected were located far to the south of Suruga Bay, the only location from which this species was previously known. To examine the veracity of the eDNA analyses, a baited camera was deployed to the seafloor south of the Genroku seamount — one of the seamounts at which slickhead genes were detected — at a depth of 2091 m. Video footage was captured of a large (length > 250 cm) Yokozuna Slickhead threatening the Pacific Grenadier (Coryphaenoides acrolepis) gathered around the bait and attempting to attack the cage.

This study demonstrates that the combined use of eDNA analyses and baited camera observations allows for the acquisition of ecological information on rare species, such as apex predators, living in the deep sea, which has been challenging using conventional methods. We expect that determining the biodiversity, distribution, and ecology of deep-sea organisms using such a method will promote our understanding of vulnerable marine ecosystems and the impacts of global environmental change upon them. The findings of this study was published in Frontiers in Marine Science on July 1^st, 2022 (JST).

Title:

Detection of the largest deep-sea endemic teleost fish at depths of over 2,000 m through a combination of eDNA metabarcoding and baited camera observations

DOI:

https://doi.org/10.3389/fmars.2022.945758

Authors:

Yoshihiro Fujiwara¹, Shinji Tsuchida¹, Masaru Kawato¹, Kotohiro Masuda², Sakiko Orui Sakaguchi¹, Tetsuya Sado³, Masaki Miya³, Takao Yoshida¹

Affiliation:

1. Research Institute for Global Change (RIGC), Japan Agency for Marine-Earth Science and Technology (JAMSTEC)
2. Institute of Industrial Science, The University of Tokyo
3. Natural History Museum and Institute, Chiba

3. Background

To achieve the Aichi Biodiversity Targets adopted at the tenth meeting of the Conference of the Parties to the Convention on Biological Diversity (CBD–COP10) held in Nagoya, Aichi Prefecture, Japan in October of 2010, four areas were designated as the first offshore seabed nature conservation areas in Japan under the Nature Conservation Act passed on December 3, 2020. With this designation, the proportion of marine protected areas in Japan reached 13.3%, thereby meeting the Aichi target of conserving 10% of marine areas by 2020. Changes in the natural environment due to development and the impacts of conservation on marine protected areas have been highlighted as important issues. While continuous monitoring is necessary to evaluate any changes in the biodiversity of conservation areas, surveys and observations of the deep sea currently require more specialized equipment and knowledge than shallower regions. Therefore, JAMSTEC scientists began monitoring the ecosystems of offshore conservation areas in 2020, first using existing technologies and later developing a novel monitoring technology that can be employed without large-scale research

vessels. To more easily understand the biodiversity of seamounts within offshore conservation areas, the research team collected a large volume of seawater using a rosette-type water sampler equipped with a CTD probe and analyzed the eDNA contained therein, from which the gene sequence of the Yokozuna Slickhead was detected at three of the six seamounts surveyed in 2020 and 2021 (Fig. 1). A baited camera was then deployed at one of the three seamounts to capture video footage of the Yokozuna Slickhead, a large deep-sea fish first reported by JAMSTEC researchers in 2021, and known to be an apex predator in the deep parts of Suruga Bay (press releases dated January 25, 2021).

4. Outcome

From November–December of 2020 and in October of 2021, a rosette-type water sampler with CTD installed on the research vessel KAIMEI, was used to collect a large volume of seawater at the Shoho, Shotoku, Genroku, and An’ei seamounts in the Nishi-Shichito Ridge Marine Protected Area and at the Nikko and Ritto seamounts in the Central and Western Mariana Ridge North Marine Protected Area. A total of 2.6 tons of seawater were filtered through 75 filters (~35 kg of seawater per filter), and eDNA was extracted after filtration. Following gene amplification for the fish nucleotide sequence, the sequence was decoded using next-generation sequencing, and the resultant information was obtained from approximately 7.8 million DNA fragments. Among the seawater samples collected, the gene sequence of the Yokozuna Slickhead was detected in those from a depth of 1961 m at the Shotoku seamount, at 2060 m south of the Genroku seamount, and at 1969 m and 1976 m at the An’ei seamount. At these locations, which were limited to the Nishi-Shichito Ridge, the sequence was detected at depths greater than 1900 m. The proportion of the Yokozuna Slickhead sequence to the total DNA fragments at each of these locations was 0.5–8.9%, with an average of 2.4% of the sequences belonging to this species. Detection of the gene sequence of the Yokozuna Slickhead was limited to the vicinity of the seafloor, and even at the same location, it could not be found in seawater samples collected far away from the seafloor.

A baited camera was deployed to a depth of 2091 m south of Genroku Seamount on October 14, 2021. A single individual of Yokozuna Slickhead came around the bait approximately 5.5 hours after the baited camera landed. The locations where Yokozuna Slickheads were detected by eDNA analysis or baited camera observations had a depth range of 1961–2091 m, temperatures from 1.9–2.0 °C, a salinity of 34.6‰, and oxygen concentrations of 97.6–105.3 µmol·kg^-1. Once the camera was in place, a Yokozuna Slickhead approached, widely opened its mouth twice in a threatening display toward Pacific Grenadier, and left the site after chasing away the gathered fish and attacking the bait cage (Fig. 2). The images revealed that the Yokozuna Slickhead had deep blue eyes and bumpy skin with many parasites. Approximately four minutes after the initial encounter, the same individual appeared in front of the camera and swam away without approaching the bait cage. Based on the size of the cage, the total length of this slickhead was calculated to be 253 cm (standard length: 222 cm).

By combining eDNA analyses and baited camera observations, the research team discovered novel habitats of the Yokozuna Slickhead and recorded it displaying threatening behavior toward another species for the first time. The Yokozuna Slickhead is a rare species and since it was first described in 2021, only six individuals have been collected. The successful detection of such an enigmatic species in the deep-sea regions of the open ocean, where the density of organisms is expected to be very low, indicates that eDNA analysis may be effective for monitoring marine protected areas in the future.

Environmental DNA analysis has been employed in various bodies of water, which has provided many insights regarding biodiversity. However, acquiring ecological information, such as the size, habitat density, sex, maturity, coloration, and behavior of organisms, using eDNA alone remains challenging. Baited camera observations complement eDNA analyses, particularly when studying deep-sea organisms. However, baited cameras can only observe the areas that light can reach, and their survey area is narrower than that of eDNA analysis. The results of this study demonstrate that the combined use of wide-range and spot surveys based on eDNA analysis and baited camera observations, respectively, allows for the acquisition of ecological information on large, rare species from the deep sea that cannot be easily studied, including apex predators.

The survey reported here revealed that the habitat of the Yokozuna Slickhead extends at least to more than 400 km south of Suruga Bay and that it is slightly shallower than the previously known depth range. However, no information on the Yokozuna Slickhead was obtained at the Shoho seamount, which is located between Suruga Bay and the Shotoku seamount, where slickhead genes were detected. Owing to the small number of surveys, it remains unknown whether the distribution of the Yokozuna Slickhead is interrupted around the Shoho seamount. Moreover, no information (genetic or observation) was obtained at the Ritto or Nikko seamounts, which are located south of Nishi-Shichito Ridge, where the species was also detected. In the future, additional surveys should reveal the exact distribution of the Yokozuna Slickhead.

Observing the threatening behavior of the Yokozuna Slickhead toward another species (Pacific Grenadiers) was unexpected. Members of Alepocephalidae, the family that includes the Yokozuna Slickhead, are generally thought to have soft and fragile bodies. Nevertheless, the recorded slickhead threatened the Pacific Grenadiers by opening its mouth wide and chasing them away from the bait cage. Previous studies have shown that the Yokozuna Slickhead feeds on relatively large fish and shows a high trophic position, which is consistent with the threatening behavior observed in this study. Considering its body length (>250 cm), this species is thought to be an apex predator in both Suruga Bay and along the Nishi-Shichito Ridge.

Only seven species of teleost fish that exceed 200 cm in total length are known to live in the deep sea at depths of >2000 m, of which the Yokozuna Slickhead and Giant Grenadier are the only ones that are endemic to the deep sea. Since the slickhead reported in this study exceeded the maximum recorded length of Giant Genadiers, the Yokozuna Slickhead is currently the largest known deep-sea endemic teleost fish from depths of over 2000 m. Adult Giant Grenadiers are also known to occupy a high trophic level and can fill the niche of an apex predator even at depths exceeding 2000 m. Additionally, the distributions of these two species are limited to the North Pacific, suggesting that the energy supply needed to feed such large predators is present at depths of at least 2000 m in this region. Clear spatial partitioning was observed between the two species, with the Yokozuna Slickhead tending to live at greater depths and lower latitudes than the Giant Grenadier (Fig. 3).

The information currently available on deep-sea predators is limited. The Giant Grenadiers exhibited a typical “rattail” form, in which the caudal area narrows toward the posterior. This body type makes Giant Grenadiers slow swimmers and individuals may even be caught in trawl nets. In contrast, the Yokozuna Slickhead is fusiform and has a large caudal fin. All six previously collected individuals of this species were captured using longlines, and none by trawl nets, indicating that they are capable swimmers. According to data from the Ocean Biodiversity Information System — a global database of marine organisms — there are fewer than 10 longline records from depths of more than 2000 m, while there are more than 1000 trawl records at the same depth range. This suggests that the deep-sea surveys conducted thus far have only been capable of collecting fish with poor swimming abilities, and it is likely that large fish with strong swimming abilities, such as the Yokozuna Slickhead, have not been sufficiently collected due to this limitation. In the future, we expect to gain a better understanding of strong-swimming, deep-sea predators worldwide, by combining eDNA analyses and baited camera observations, in addition to longline sampling.

5. Future outlook

The Aichi Biodiversity Targets require each country to designate at least 17% of terrestrial and inland waters and 10% of coastal and marine areas, especially those that are important for biodiversity and ecosystem services, as protected areas by 2020 to halt the global loss of biodiversity. By May of 2021, those nations that are party to the Convention on Biological Diversity have designated 16.64% of terrestrial and 7.74% of marine areas as nature reserves. However, our understanding of biodiversity remains insufficient, even in designated protected areas, and this deficiency is evident especially in offshore areas. The habitats of the Yokozuna Slickhead newly discovered in this study are located in and around offshore seabed nature conservation areas, meaning that the existence of an apex predator in these marine protected areas was previously unknown.

The progression of global environmental changes affects the apex predators of every ecosystem, and changes across their populations are expected to disrupt local food chains, eventually causing catastrophic damage to entire ecosystems. The research team aims to understand the biodiversity present in offshore seabed nature conservation areas, including that of apex predators, based on the results of this study, which should promote technological development to allow for easier monitoring of deep-sea ecosystems. Additionally, JAMSTEC continues to promote research and development that can accurately evaluate the effects of global environmental changes upon these ecosystems.

【Supplemental information】

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Environmental DNA (eDNA) analysis: A research method for decoding eDNA sequences derived from various organisms in water and soil to obtain information on those living where the samples were collected. For example, fish in rivers and along coasts can be studied by extracting eDNA from a liter of water collected in a bucket at a given location. In contrast, a large volume of seawater must be collected to study the deep sea because of the very low concentrations of eDNA present; specialized equipment and knowledge are required to perform and analyze such collections.

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Apex predator: An animal at the top of the ecosystem with no natural predators. Examples include lions and orcas.

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Baited camera: A camera system with bait attached that is deployed to the seafloor in free-fall mode. It is equipped with a current meter in addition to a device that measures environmental factors, such as conductivity (salinity), temperature, and depth, and shows the diversity and biomass of predators that gather around the bait.

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Niche: The position or role of a species within an ecosystem.

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Rosette-type water sampler with CTD: A water sampler combined with a probe consisting of sensors to measure the conductivity (salinity), temperature, and depth (pressure) of seawater.