Etmopterus Research Articles

One-year extra-uterine life support for viviparous shark embryos: first technological application to mid-term embryos

Shark-specific artificial uterine fluid is a recently developed material suitable for maintaining viviparous shark embryos outside the maternal body. Previous studies confirmed that this fluid greatly extends the captive maintenance period of the embryonic slendertail lantern shark (Etmopterus molleri) from <1 week to several months. Its application, however, has been limited to late-term embryos. This study reports the first application of this fluid on mid-term embryos with long external gill filaments. The incubation was found to be successful, with the embryos growing to their natural birth size after 1 year. A high mortality of mid-term embryos was observed during incubation due to pressure ulcers. This indicates that not only appropriate chemical environment but also appropriate physical environment is critical for the stable maintenance of mid-term embryos.

Heavy metal concentrations in sharks, rays and chimaeras from the western Mediterranean Sea

The potential bioaccumulation of pollutants, such as heavy metals, may pose a threat to the western Mediterranean chondrichthyans and human consumers. Therefore, the first extensive assessment of cadmium (Cd), lead (Pb), and copper (Cu) concentrations in the muscle tissue of 17 species of sharks, rays, and chimaeras in this region was conducted via Microwave Assisted Extraction (MAE) and Graphite Furnace Atomic Absorption Spectrometry (GFAAS). Significant differences between species were observed, particularly related to the rabbit fish (Chimaera monstrosa) and the velvet belly lantern shark (Etmopterus spinax), which exceeded the European Union (EU) Commission Regulation 2023/915 threshold of Cd. Overall, heavy metal concentrations correlated negatively with size and trophic level but positively with depth. Although the consumption of these species may entail minimal risk to adult humans, caution is advised, especially for children. These findings are important due to the widespread consumption of chondrichthyans in many western Mediterranean regions.

Successful delivery of viviparous lantern shark from an artificial uterus and the self-production of lantern shark luciferin.

Our recent success in the long-term maintenance of lantern shark embryos in artificial uterine systems has provided a novel option for the medical treatment of premature embryos for captive viviparous elasmobranchs. The remaining issue with this system is that the embryos cannot survive the abrupt change in the chemical environment from artificial uterine fluid (AUF) to seawater during delivery. To overcome this issue, the present study developed a new protocol for seawater adaptation, which is characterized by a long-term and stepwise shift from AUF to seawater prior to delivery. This protocol was employed successfully, and the specimen survived for more than seven months after delivery, the longest captive record of the species. During the experiment, we unexpectedly detected bioluminescence of the embryonic lantern shark in the artificial uterus. This observation indicates that lantern sharks can produce luciferin, a substance for bioluminescence. This contradicts the recent hypothesis that lantern sharks lack the ability to produce luciferin and use luciferin obtained from food sources.

First Recorded Occurrence of the Parasitic Barnacle (Anelasma squalicola) on a Greenland Shark (Somniosus microcephalus) in the Canadian Arctic.

A solitary Anelasma squalicola specimen was collected from the cloaca of a Greenland shark (Somniosus microcephalus), the first time this association has been recorded. The specimen's identity was confirmed through morphological and genetic assessment (mitochondrial markers: COI and control region). Anelasma squalicola is a species typically associated with deep-sea lantern sharks (Etmopteridae) and, until the present observation, had never been observed at a sexually mature size in the absence of a mating partner. Given the reported negative effects of this parasite on its hosts, monitoring Greenland sharks for additional cases is recommended.

First records of the blurred lantern shark Etmopterus bigelowi from the Cayman Islands, Western Atlantic

The genus Etmopterus is the most speciose group of small bodied deep-sea sharks found throughout the tropical and subtropical Western Atlantic. Despite exhibiting a global distribution at the genus-level, the blurred lantern shark (Etempoterus bigelowi) is known only from a few records in the Western and Southern Atlantic Ocean. Through in-situ video observations using deep-sea landers, we provide two new locality records of the blurred lantern shark from the deep waters off the Cayman Islands, Caribbean Sea. Three unique individuals were recorded across two separate deployments between 653m – 668m. These observations provide the first records of this species in the Caribbean Sea, adding to the minimal knowledge of the species’ distribution throughout the Western Atlantic Ocean.

Issue Cover (May 2023)

Front cover: Cover image: Reconstruction of the internal structures and the mandibular arch of a blackbelly lanternshark, Etmopterus lucifer based on micro-CT images. See M.A. Staggl and colleagues, 'Head anatomy of a lantern shark wet-collection specimen (Chondrichthyes: Etmopteridae)', this issue.

Head anatomy of a lantern shark wet-collection specimen (Chondrichthyes: Etmopteridae).

In this study, we apply a two-step (untreated and soft tissue stained) diffusible iodine-based contrast-enhanced micro-computed tomography array to a wet-collection Lantern Shark specimen of Etmopterus lucifer. The focus of our scanning approach is the head anatomy. The unstained CT data allow the imaging of mineralized (skeletal) tissue, while results for soft tissue were achieved after staining for 120 h in a 1% ethanolic iodine solution. Three-dimensional visualization after the segmentation of hard as well as soft tissue reveals new details of tissue organization and allows us to draw conclusions on the significance of organs in their function. Outstanding are the ampullae of Lorenzini for electroreception, which appear as the dominant sense along with the olfactory system. Corresponding brain areas of these sensory organs are significantly enlarged as well and likely reflect adaptations to the lantern sharks' deep-sea habitat. While electroreception supports the capture of living prey, the enlarged olfactory system can guide the scavenging of these opportunistic feeders. Compared to other approaches based on the manual dissection of similar species, CT scanning is superior in some but not all aspects. For example, fenestrae of the cranial nerves within the chondrocranium cannot be identified reflecting the limitations of the method, however, CT scanning is less invasive, and the staining is mostly reversible and can be rinsed out.

Taxonomic Identification of Two Poorly Known Lantern Shark Species Based on Mitochondrial DNA From Wet-Collection Paratypes

Etmopteridae (lantern sharks) is the most species-rich family of sharks, comprising more than 50 species. Many species are described from few individuals, and re-collection of specimens is often hindered by the remoteness of their sampling sites. For taxonomic studies, comparative morphological analysis of type specimens housed in natural history collections has been the main source of evidence. In contrast, DNA sequence information has rarely been used. Most lantern shark collection specimens, including the types, were formalin fixed before long-term storage in ethanol solutions. The DNA damage caused by both fixation and preservation of specimens has excluded these specimens from DNA sequence-based phylogenetic analyses so far. However, recent advances in the field of ancient DNA have allowed recovery of wet-collection specimen DNA sequence data. Here we analyse archival mitochondrial DNA sequences, obtained using ancient DNA approaches, of two wet-collection lantern shark paratype specimens, namely Etmopterus litvinovi and E. pycnolepis, for which the type series represent the only known individuals. Target capture of mitochondrial markers from single-stranded DNA libraries allows for phylogenetic placement of both species. Our results suggest synonymy of E. benchleyi with E. litvinovi but support the species status of E. pycnolepis. This revised taxonomy is helpful for future conservation and management efforts, as our results indicate a larger distribution range of E. litvinovi. This study further demonstrates the importance of wet-collection type specimens as genetic resource for taxonomic research.

First recorded case of leucism in the velvet belly lantern sharkEtmopterus spinax(Squaliformes: Etmopteridae)

The capture of a female specimen of the velvet belly lantern shark Etmopterus spinax with abnormal skin coloration is reported. The specimen was captured off northern Spain (Bay of Biscay, North-eastern Atlantic) in 2021 by bottom trawling. The lack of dermal melanophores combined with a normal retinal pigmentation, lead us to considerate the specimen as leucistic. This is the first case of leucism in E. spinax and the second record of colour aberration in the family Etmopteridae. A comprehensive updated review of published literature on albinism and leucism in chondrichthyans is also provided.

Five-Month Incubation of Viviparous Deep-Water Shark Embryos in Artificial Uterine Fluid

In this study, we developed an extra-uterine life-support system (artificial uterus) for viviparous elasmobranchs. Using this system, we maintained two embryonic specimens of the slendertail lantern shark (Etmopterus molleri) for approximately 5 months, the longest published record of the captive maintenance of the embryos of this species. This system is characterized by the use of a urea-containing artificial incubation fluid, of which the salinity and osmotic pressure are approximately equivalent to those of shark blood plasma. We hypothesized that this fluid reduces the salinity gradient between embryonic blood plasma and the environmental fluid, which thereby contributes to countering the low osmoregulatory capacity of viviparous shark embryos. However, the incubated specimens subsequently died during the process of seawater adaptation following “artificial birth.” Accordingly, information pertaining to uterine chemical dynamics throughout the gestation period is necessary for the design of a more effective incubation system. This technique will be relevant and may find application in conservation breeding at public aquaria in the future.

Diet consistency but large-scale isotopic variations in a deep-sea shark: The case of the velvet belly lantern shark, Etmopterus spinax, in the northeastern Atlantic region and Mediterranean Sea

Deep-sea elasmobranchs are commonly reported as bycatch of deep-sea fisheries and their subsequent loss has been highlighted as a long-running concern to the ecosystem ecological functioning. To understand the possible consequences of their removal, information on basic ecological traits, such as diet and foraging strategies, is needed. Such aspects have been widely studied through stomach content analysis but the lack of long-term dietary information requires other tools to be used such as stable isotopes. This study examines nitrogen and carbon isotope compositions of the velvet belly lantern shark, Etmopterus spinax, one of the most impacted shark species in northeastern Atlantic fisheries as a result of accidental catches. E. spinax was sampled at four different locations, characterized by contrasting oceanographic and ecological conditions: the western Mediterranean Sea (near the Balearic Islands), the southern Iberian upwelling system, Rockall Trough and southwestern Norwegian fjords. Stomach content analysis revealed similar prey species among sites, with a diet dominated by Euphausiacea (mostly Meganyctiphanes norvegica) and an ontogenetic shift towards small teleost fishes, cephalopods or other crustaceans. Despite these similarities, muscle stable isotope compositions differed across sampled locations. Rather than clear dietary differences, the contrasted isotopic values are likely to reflect differences in environmental settings and biogeochemical processes affecting nutrient dynamics at the base of the food webs.

First record of the parasitic barnacle Anelasma squalicola Darwin, 1852 (Pollicipedomorpha: Pollicipedidae) in the Eastern Pacific Ocean and a new host report: Etmopterus benchleyi Vsquez, Ebert amp; Long, 2015 (Squaliformes: Etmopteridae).

Anelasma squalicola is a parasitic barnacle of members of the deep-water shark families Etmopteridae, Pentanchidae and Scyliorhinidae. We report the first published confirmation of this species in the Eastern Pacific Ocean, based on material collected off Costa Rica, its first record as a parasite of the Ninja lantern shark, Etmopterus benchley (Etmopteridae), and a new size record for the host. The information presented herein expands the knowledge (distribution and host usage) of this enigmatic species.

Ecophysiological effects of mercury bioaccumulation and biochemical stress in the deep-water mesopredator Etmopterus spinax (Elasmobranchii; Etmopteridae)

Mercury (Hg) is a non-essential metal that can have toxic effects on the fitness of organisms and tends to bioaccumulate with age and to biomagnify in higher trophic levels. Few studies have assessed oxidative stress and neurotoxicity in deep-water sharks. This study evaluated early ontogenetic changes and physiological effects (antioxidant defences, oxidative damage, aerobic metabolism and neurotransmission functions) of Hg accumulation in the white muscle and brain tissues of the velvet belly lantern shark Etmopterus spinax from the southern Iberian coast (NE Atlantic). Results suggested that the low mercury concentrations observed may induce acute effects in E. spinax before they reach sexual maturity. We found different Hg concentrations in E. spinax: [Hg] males > [Hg] females; [Hg] muscle > [Hg] brain. Females appeared to have higher redox capability translated into higher activities and levels of antioxidant defences than males. However, higher levels of oxidative damage were also observed in females. Whilst the mechanisms underlying these effects remain unknown, these results suggest differences in mercury accumulation between tissues and sex, and potentially deleterious effects on oxidative stress status and neurophysiology of E. spinax, potentially impairing swimming performance and reproduction, which could subsequently impact on the health of both individuals and population.

Etmopterus lantern sharks use coelenterazine as the substrate for their luciferin-luciferase bioluminescence system

The lantern shark genus Etmopterus contains approximately 40 species of deep-sea bioluminescent cartilaginous fishes. They emit blue light mainly from the ventral body surface. The biological functions of this bioluminescence have been discussed based on the luminescence patterns, but the bioluminescence mechanism remains uncertain. In this study, we detected both coelenterazine and coelenterazine-dependent luciferase activity in the ventral photophore tissue of Etmopterus molleri. The results suggested that bioluminescence in lantern sharks is produced using coelenterazine as the substrate for the luciferin-luciferase reaction, as some luminous bony fishes.

Mitochondrial DNA sequencing of a wet-collection syntype demonstrates the importance of type material as genetic resource for lantern shark taxonomy (Chondrichthyes: Etmopteridae).

After initial detection of target archival DNA of a 116-year-old syntype specimen of the smooth lantern shark, Etmopterus pusillus, in a single-stranded DNA library, we shotgun-sequenced additional 9 million reads from this same DNA library. Sequencing reads were used for extracting mitochondrial sequence information for analyses of mitochondrial DNA characteristics and reconstruction of the mitochondrial genome. The archival DNA is highly fragmented. A total of 4599 mitochondrial reads were available for the genome reconstruction using an iterative mapping approach. The resulting genome sequence has 12 times coverage and a length of 16 741 bp. All 37 vertebrate mitochondrial loci plus the control region were identified and annotated. The mitochondrial NADH2 gene was subsequently used to place the syntype haplotype in a network comprising multiple E. pusillus samples from various distant localities as well as sequences from a morphological similar species, the shortfin smooth lantern shark Etmopterus joungi. Results confirm the almost global distribution of E. pusillus and suggest E. joungi to be a junior synonym of E. pusillus. As mitochondrial DNA often represents the only available reference information in non-model organisms, this study illustrates the importance of mitochondrial DNA from an aged, wet collection type specimen for taxonomy.

A matter of size: the population structure of the smallest known living shark, Etmopterus perryi (Springer & Burgess,1985), from deep waters off the Colombian Caribbean coast.

The dwarf lanternshark (Etmopterus perryi) is the smallest known described shark, and practically no information has been available on this species since first described in the mid-1980s. Therefore, the aim of this work is to describe, for the first time, the population structure regarding dwarf lanternshark in the Colombian Caribbean Sea. During deep-water research surveys conducted along the Colombian Caribbean coast, 87 stations were sampled using the swept area method. A total of 153 dwarf lanternshark individuals were caught in depths ranging from 230 to 530 m. This information was used to describe the size structures, morphological measurements including length-at-weight relationship, length at maturity in females and the spatial distribution of mean length and biomass of the species. The lengths of individuals ranged from 78.02 to 289.00 mm total length (TL), which is a new record of maximum length for this species. The spatial distribution of mean lengths and biomass distributions show high abundances and high relative mean lengths in the northeast area off Santa Marta and the area northwest of Riohacha. The mean biomass density in the whole prospected area was 5.52 kg km-2 . Length at 50% maturity in females was estimated in 203 mm TL (95% C.I.: 190-214 mm). Deep-water elasmobranch species, such as the dwarf lantern shark, are expected to show extremely low resilience to fishing exploitation, even when they are not targeted by commercial fishing. Therefore, the information reported in this study can serve as a baseline upon which management measurements can be proposed for the conservation of this shark species.

Bottom temperature warming and its impact on demersal fish off the Pacific coast of northeastern Japan

Global climate change occurs not only at the ocean surface but also at the ocean bottom, which is the main habitat of demersal fish. To clarify the current status of bottom temperature warming off the Pacific coast of northeastern Japan, we examined gridded bottom temperature fields from 2003 to 2019. These fields were created by a newly developed gridding method using flexible Gaussian filter weighting with time, distance, and depth. Spatially averaged bottom temperature had a strong, significant warming trend of 0.083 to 0.115°C yr-1 in depth zones of 150-300 m, indicating bottom temperature warming. Corresponding to the warming, increases in landing amounts were found for warm-water species such as searobin in the middle region of our study area (37°50’-39°N). Seasonal catch amounts suggest that ribbon fish and swimming crab recently began to overwinter and reproduce in the area. The distribution shifts of non-target species in fisheries were also analyzed using bottom otter trawl survey data from the area from 2003 to 2019. Northward distribution shifts and increases in density were observed in blackbelly lantern shark and bighand grenadier, indicating that bottom temperature warming led to habitat expansion. Conversely, darkfin sculpin and jelly eelpout shifted northward with decreasing density, suggesting that bottom temperature warming had a negative effect on them. Deepsea bonefish shifted deeper into colder waters with increasing density and mean body weight. Thus, changes and responses of demersal fish to bottom temperature warming in the area were revealed.

Intraspecific dental variations in the deep-sea shark Etmopterus spinax and their significance in the fossil record

An important character on several taxonomic levels for shark identification is the tooth morphology. Sharks show a variety of highly specialized dentitions reflecting adaptations to their feeding habits. Intraspecific variation of tooth morphology such as sexual or ontogenetic dimorphism is poorly known in many species, even though tooth morphology plays a decisive role in the characterization of the fossil record of sharks, which comprises mostly fossil teeth. Here we analyzed the dentition of 40 jaws of the Velvet Belly Lantern Shark Etmopterus spinax and identified ontogenetic and sexual dimorphic characters such as total number of teeth, number of upper teeth, cusplet numbers in upper jaw teeth and width of lower jaw teeth. Dimorphic characters may reduce intraspecific competition for food, as E. spinax segregates by sex and size and may allow for identifying the male sex. The lower jaw tooth height, a sexually non-dimorphic character, was used to re-calculate the total length of specimens, which represents the first such approach for a squaliform shark. Results derived from the extant E. spinax are subsequently applied to fossil Etmopterus sp. teeth (Miocene) to gain individual information such as sex or size, but also characterize the extinct population from the excavation site by a size distribution profile in comparison to data from extant populations. This approach indicates the presence of multiple ontogenetic stages in the extinct population.

Kuzey Kıbrıs'ın Derin Denizlerinde Kadife Karınlı Fener Köpekbalığının Etmopterus spinax (Linnaeus, 1758) Yeni Kaydı

Lantern sharks are small shark species that can be seen at depths between 70 and 2000 meters. Due to their luminescent characteristics, they have been called “Lantern shark”. In total eleven specimens of the velvet belly lantern shark, Etmopterus spinax (Linnaeus, 1758), were caught in the deep seas of Northern Cyprus by using a bottom trawl. Sampling was carried out using 13 trawling operations. The collected samples were placed in 4% formalin and stored at the Museum of the Systematic, Faculty of Fisheries, Mersin University, (catalogue number: MEUFC-18-11-082). As a sampling area, the depths between 274 and 641 m were selected. Other cartilaginous fish caught during sampling except E. spinax were Galeus melastomus (1 individual), Squalus acanthias (4 individuals), Scyliorhinus canicula (85 individuals). E. spinax made up 10.89% of all cartilaginous fishes which were caught. Species identification for all fishes caught is made with the help of morphological features.

Feeding habits of four sympatric sharks in two deep-water fishery areas of the western Mediterranean Sea

The study of the feeding ecology of marine predators is crucial to understanding their ecological roles and advancing our knowledge of marine ecosystem functioning, especially in highly human-impacted areas. Here, we examined the trophic ecology of three abundant demersal sharks, the velvet belly lantern shark Etmopterus spinax, the blackmouth catshark Galeus melastomus and the small-spotted catshark Scyliorhinus canicula, and the rare kitefin shark Dalatias licha of the western Mediterranean Sea. Data were obtained from two deep-water areas with different degrees of human impact: a fishery restricted area (FRA) in the Gulf of Lions and a highly human-impacted area in the Catalan Sea (non-FRA). We combined analyses of individual stomach contents and stable isotope values from different individuals of each shark species. Our results revealed that D. licha is a predator located higher up on the food web, while G. melastomus, E. spinax and S. canicula are located in lower trophic positions. These results confirm that shark species play important and, most likely, complementary roles as predators in the western Mediterranean Sea. Results also revealed that despite some differences in the diet of the shark species, as revealed by the stomach contents, in the long term (isotopic results) the four species showed similar diet habits and similar trophic relationships in both FRA and non-FRA. This may be due to the fact that despite the fishing regulations in the FRA area, the population of the prey species probably do not vary between the two areas.Overall, this study provides new insights into the trophic ecology of these sharks and contributes to an understanding of their ecological roles within the community.