Resource utilization by deep-sea sharks at the Le Danois Bank, Cantabrian Sea, north-east Atlantic Ocean

The feeding habits of birdbeak dogfish Deania calcea, velvet belly lantern shark Etmopterus spinax and blackmouth catshark Galeus melastomus at Le Danois Bank, Cantabrian Sea, south Bay of Biscay were studied in relation to their bathymetric distribution. Deep‐sea sharks were collected during two multidisciplinary surveys carried out in October 2003 and April 2004 at the Le Danois Bank. Two different habitats were defined: (1) the top of the bank, ranging from 454 to 642 m depth and covered by fine‐sand sediments with a low percentage of organic matter, and (2) the inner basin located between the bank and the Cantabrian Sea's continental shelf, at depths of 810–1048 m, which was characterized by a high proportion of silt and organic matter. Deania calcea was not present at the top of the bank but was abundant below 642 m, while E. spinax was abundant in the shallower top of the bank but was not found in the deeper inner basin. There was almost no bathymetric overlap between these two deep‐sea shark species. Galeus melastomus was found over the whole depth range. There seemed to be an ontogenetic segregation with depth for this species, however, since 80% of the specimens collected at the top of the bank were < 600 mm total length (L_T) (mean 510 mm L_T), whereas larger individuals (mean 620 mm L_T) inhabited deeper zones. Galeus melastomus exhibited a significantly higher feeding intensity than both E. spinax at the top of the bank and D. calcea in the inner basin. Little dietary overlap between D. calcea and G. melastomus in the inner basin was found, with D. calcea being an ichthyophagous predator while the diet of G. melastomus at these depths was composed of a variety of meso‐bathypelagic shrimps (e.g. Acantephyra pelagica, Pasiphaea spp. and Sergia robusta), cephalopods and fishes. The diets of E. spinax and G. melastomus at the top of the bank showed a high dietary overlap of euphausiids, which represented the main prey taxa for both species. Euphausiids declined in abundance with depth which was reflected in the diet of G. melastomus. The cluster analysis of prey affinities among hauls depicted two major groups, corresponding to the two different habitats (top of the bank and inner basin). Redundancy analysis also indicated top–basin segregation, with euphausiids representing the main prey taxa at the top of the bank and bathypelagic shrimps in the inner basin. Euphausiids and Micromesistius poutassou were key prey within the Le Danois Bank ecosystem since they were positively selected by the three deep‐sea shark species. These results show that the feeding ecology of these predators in Le Danois Bank ecosystem is highly influenced by depth‐related variables, as a result of changes in prey availability. Overall results were analysed in relation to the deep‐sea Le Danois ecosystem structure and functioning.     

A molecular and ecological study of Grillotia (Cestoda: Trypanorhyncha) larval infection in small to mid‐sized benthonic sharks in the Gulf of Naples,Mediterranean Sea

AimTrypanorhyncha cestodes comprise a wide range of heteroxenous parasites infecting elasmobranchs as definitive hosts. Limited data exist on the larval infection of these cestodes and the role of intermediate and paratenic hosts in the life cycle of these parasites. We investigated the factors that determine the occurrence and the level of infection of Grillotia plerocerci in the skeletal muscles of various benthonic sharks and analyzed the parasites through an integrative taxonomic approach.LocationMediterranean Sea.MethodsSharks obtained as bycatch of commercial trawling activities (i.e., Etmopterus spinax, Galeus melastomus, and Scyliorhinus canicula) were used in this study. Data from a limited number of Dalatias licha and Scyliorhinus stellaris were also included. Grillotia plerocerci were molecularly characterized using the partial 28S large subunit rDNA. Boosted regression trees were used to model the relationship between the abundance of infection with both morphological and physiological predictors in each host.ResultsPlerocerci of Grillotia were detected in all shark species except S. stellaris. Host species significantly differed in terms of parasite abundance, with the highest and lowest prevalence and abundance of infection detected in G. melastomus and E. spinax, respectively. The relative influence of the traits involved in explaining the parasite abundance was related to the host size in G. melastomus, while both morphology‐ and physiology‐related traits explained the patterns observed in E. spinax and S. canicula. The 28S rDNA sequences shared an identity of ∼99.40% with a Grillotia species previously found in the Mediterranean Sea. At intraspecific level, two different genotypes were found. A first type was retrieved only from D. licha, whereas a second type was found in G. melastomus, E. spinax, and S. canicula.Main conclusionsPresent results suggest that the two genotypes could be involved in different consumer‐resource systems and confirm most of the examined shark species as transport hosts of Grillotia species for unknown larger top predators.     

Comparing Deep-Sea Fish Fauna between Coral and Non-Coral “Megahabitats” in the Santa Maria di Leuca Cold-Water Coral Province (Mediterranean Sea)

Two experimental longline surveys were carried out in the Santa Maria di Leuca (SML) cold-water coral province (Mediterranean Sea) during May–June and September–October 2010 to investigate the effect of corals on fish assemblages. Two types of “megahabitat” characterized by the virtual absence of fishing were explored. One was characterized by complex topography including mesohabitats with carbonate mounds and corals. The other type of megahabitat, although characterized by complex topographic features, lacks carbonate mounds and corals. The fishing vessel was equipped with a 3,000 m monofilament longline with 500 hooks and snoods of 2.5 m in length. A total of 9 hauls, using about 4,500 hooks, were carried out both in the coral megahabitat and in the non-coral megahabitat during each survey. The fish Leucoraja fullonica and Pteroplatytrygon violacea represent new records for the SML coral province. The coral by-catch was only obtained in the coral megahabitat in about 55% of the stations investigated in both surveys. The total catches and the abundance indices of several species were comparable between the two habitat typologies. The species contributing most to the dissimilarity between the two megahabitat fish assemblages were Pagellus bogaraveo, Galeus melastomus, Etmopterus spinax and Helicolenus dactylopterus for density and P. bogaraveo, Conger conger, Polyprion americanus and G. melastomus for biomass. P. bogaraveo was exclusively collected in the coral megahabitat, whereas C. conger, H. dactylopterus and P. americanus were found with greater abundance in the coral than in the non-coral megahabitat. Differences in the sizes between the two megahabitats were detected in E. spinax, G. melastomus, C. conger and H. dactylopterus. Although these differences most probably related to the presence-absence of corals, both megahabitats investigated play the role of attraction-refuge for deep-sea fish fauna, confirming the important role of the whole SML coral province as a refuge area from fishing.     

First record of the brown lanternshark,Etmopterus unicolor, from the waters around New Zealand, and comparison with the southern lanternshark,E. granulosus

Specimens of the brown lanternshark,Etmopterus unicolor, reported here for the first time from the waters around New Zealand, were caught on bottom longlines. This study compares morphometeric and meristic characters of New Zealand and Japanese specimens ofE. unicolor and New Zealand specimens of the southern lanternshark,E. granulosus. E. unicolor andE. granulosus are clearly distinguishable by the height of the first dorsal fin, number of spiral valves, number of vertebrae, and shape of the dermal denticles and teeth.     

Elasmobranch species richness,fisheries, abundance and size composition in the Azores archipelago (NE Atlantic)

ABSTRACT

Elasmobranchs are a vulnerable resource, more susceptible to overfishing than most teleosts, and their assessment is complicated due to a general lack of information about their fisheries, biology and ecology. This study aimed to analyse all fishery and survey data available for elasmobranchs caught over the past c. 25 years around the Azores (NE Atlantic) to provide a baseline information, which can be used to inform stock assessment and management strategies. Elasmobranch species covered pelagic, benthopelagic and demersal habitats, from shallow to deep-water strata in areas around the islands and seamounts. These species are taken accidentally as by-catch of three main fisheries: swordfish fishery, black scabbardfish fishery and demersal bottom longline fishery. The latter represents one of the most important fishing activities in the Azores, and frequent elasmobranch by-catches include Raja clavata, Galeorhinus galeus, Deania calcea, D. profundorum, Etmopterus pusillus and E. spinax. A slight reduction in the abundance indices of these species was observed, despite the implemented technical measures (e.g. minimum size, zero catch). Little is known about resource dynamics for the Azorean region and no analytical assessments have been conducted. This study highlights the vulnerability to overfishing of these resources and the urgent need to develop management strategies.     

In the intimacy of the darkness: Genetic polyandry in deep-sea luminescent lanternsharks Etmopterus spinax and Etmopterus molleri (Squaliformes,Etmopteridae)

Multiple paternity seems common within elasmobranchs. Focusing on two deep-sea shark species, the velvet belly lanternshark (Etmopterus spinax) and the slendertail lanternshark (Etmopterus molleri) we inferred the paternity in 31 E. spinax litters from Norway (three to 18 embryos per litter) and six E. molleri litters from Japan (three to six embryos), using 21 and 10 specific microsatellites, respectively. At least two E. spinax litters were sired from multiple fathers each, with highly variable paternal skew (1:1 to 9:1). Conversely, no clear signal of genetic polyandry was found in E. molleri.     

A glimpse into the trophic ecology of deep-water sharks in an important crustacean fishing ground

Deep-water sharks are among the most vulnerable deep-water taxa because of their extremely conservative life-history strategies (i.e., late maturation, slow growth, and reproductive rates), yet little is known about their biology and ecology. Thus, this study aimed at investigating the trophic ecology of five deep-water shark species, the birdbeak dogfish (Deania calcea), the arrowhead (D. profundorum), the smooth lanternshark (Etmopterus pusillus), the blackmouth catshark (Galeus melastomus) and the knifetooth dogfish (Scymnodon ringens) sampled onboard a crustacean bottom-trawler off the south-west coast of Portugal. We combined carbon and nitrogen stable isotopes with RNA and DNA (RD) ratios to investigate the main groups of prey assimilated by these species and their nutritional condition, respectively. Stable isotopes revealed overall small interspecific variability in the contribution of different taxonomic groups to sharks' tissues, as well as in the origin of their prey. S. ringens presented higher δ¹⁵N and δ¹³C values than the other species, suggesting reliance on bathyal cephalopods, crustaceans and teleosts; the remaining species likely assimilated bathy-mesopelagic prey. The RD ratios indicated that most of the individuals had an overall adequate nutritional condition and had recently eaten. This information, combined with the fact that stable isotopes indicate that sharks assimilated prey from the local or nearby food webs (including commercially important shrimps), suggests a potential overlap between this fishing area and their foraging grounds, which requires further attention.     

Living naked: first case of lack of skin-related structures in an elasmobranch,the blackmouth catshark (Galeus melastomus)

As far as is known, in this paper the first case of lacking of skin-related structures (epidermis, stratum laxum, dermal denticles and teeth) in a free-swimming elasmobranch, the blackmouth catshark, Galeus melastomus, is reported. The individual was caught by trawl in Sardinian waters (central-western Mediterranean) in July 2019 at a depth of 500 m. Although this kind of morphological abnormality is potentially fatal, the observations suggested that the specimen was in good health and well developed.     

Diet and feeding strategy of blackmouth catshark Galeus melastomus

Diet and feeding strategy of the blackmouth catshark Galeus melastomus in the deep waters of the eastern Ionian Sea were investigated. Sampling was carried out using experimental bottom longline fishing at depths ranging from 300 to 855 m in summer and autumn 2010. Diet variability with fish size, season, area, sex and depth zone was tested and only season was found to significantly affect the diet of the species. Of the 870 stomachs examined, only 1·4% were empty. Cumulative prey curves showed that the sample sizes were adequate to describe the main prey items of the diet for both seasons. Prey identified belonged primarily to three major groups: fishes, cephalopods and dendrobranchiatan and caridean shrimps. In autumn, the above three major groups were found as principal prey, whereas in summer cephalopods followed by fishes were the principal prey and shrimps were found as secondary prey. SIMPER analysis indicated high dissimilarity between seasons and highlighted that Sepiolidae, Myctophidae, fishes, cephalopods, shrimps and other crustaceans contributed to seasonal differences in the diet of G. melastomus. The prey diversity index was higher in autumn than in summer. A high dietary overlap was observed between the two seasons. Galeus melastomus behaved as an opportunistic predator with a variety of unimportant prey in its diet. Feeding strategy indicated that G. melastomus holds a generalist niche with a considerable specialization at the individual level. This strategy seems to be an adaptation to a food‐scarce environment, as typified in deep‐water habitats.     

Metazoan parasite communities and diet of the velvet belly lantern shark Etmopterus spinax (Squaliformes: Etmopteridae): a comparison of two deep‐sea ecosystems

By combining an examination of stomach contents yielding a snapshot of the most recent trophic niche and the structure of parasite communities reflecting a long‐term feeding niche, this study aimed at gaining more comprehensive information on the role of the small‐sized deep‐water velvet belly lantern shark Etmopterus spinax in the local food webs of the Galicia Bank and the canyon and valley system of the Avilés Canyon, which have been both proposed for inclusion in the Natura 2000 network of protected areas. As far as is known, this study provides the first comparative parasite infracommunity data for a deep‐sea shark species. Component parasite communities in E. spinax were relatively rich, whereas the infracommunities were rather depauperate, with similar low diversity at both localities. The significant differences in the composition and structure of both parasite communities and prey assemblages indicate differential effects of the two deep‐sea ecosystems on both long‐term and most recent trophic niches of E. spinax. These results underline the importance of the use of multivariate analyses for the assessment of geographical variation in shark populations based on parasites and diet data.     

The photoreceptor system in the retinae of two dogfishes, Scyliorhinus canicula and Galeus melastomus: possible relationship with depth distribution and predatory lifestyle

The small spotted dogfish Scyliorhinus canicula and the blackmouth dogfish Galeus melastomus, whose depth distributions overlap in the upper part of the slope (c. 500 m depth), where they have access to the same prey community, have well‐developed eyes and a pure‐rod retina with a single layer of photoreceptors. Interspecific differences in rod outer segment length (L_ROS) within retinal regions were found. In the periphery and the retinal centre G. melastomus showed a L_ROS 24 and 30% longer, respectively, than S. canicula and, therefore, a potential for increased sensitivity. In both species longer L_ROS were always found in correspondence with the retinal centre where the ganglion cell topography formed a horizontal meridian that allowed for better discrimination of the horizon in the visual field. In this area L_ROS reached 53·4±4·1μm in S. canicula and 77·1±10·5μm in G. melastomus against 46·3±4·2μm and 61·1±10·1μm in the retinal periphery. No significant differences were recorded in L_ROS and rod density during growth. In both species, a rapid increase of theoretical visual acuity was found to be related to an increase in fish L_T and lens size. Visual acuity ranged between 1·7 and 3 cycles degree^‐1 in S. canicula and 2·4 and 4·2 in G. melastomus. The G. melastomus rod visual pigment showed the characteristic spectral adaptation to vision in deep‐water (λ_max of 481 nm), but was also well placed to detect the bioluminescence of some of its main prey species. In S. canicula the visual pigment absorption (λ_max of 496 nm) was more typical of shallow water living fishes. The opsin sequences of the two visual pigments are discussed and key amino acid sites were identified where sequence changes could be responsible for the spectral absorption differences between the two species. The possible relationship between L^ROS, visual acuity, visual pigment absorption, depth distribution and feeding behaviour are discussed.     

TAXONOMY OF THE PHACUS OSCILLANS (EUGLENACEAE) AND ITS CLOSE RELATIVES—BALANCING MORPHOLOGICAL AND MOLECULAR FEATURES1

The establishment of epitypes (together with emended diagnoses) for seven species of Phacus Dujard. [Phacus oscillans G. A. Klebs, Phacus parvulus G. A. Klebs, Phacus pusillus Lemmerm., Phacus skujae Skvortzov, Phacus inflexus (Kisselew) Pochm., Phacus polytrophos Pochm., and Phacus smulkowskianus (Zakry?) Kusber] was achieved by literature studies, verification of morphological diagnostic features (cell size, cell shape), as well as molecular characters (SSU rDNA). The investigated Phacus species are mostly well distinguished morphologically, with an SSU rDNA interspecific sequence similarity of 95.1%–99.0% and an intraspecific sequence similarity of 99.0%–99.9%. Some of the phylogenetic relationships among the seven species have not been resolved, but the topology obtained indicates their assignment into two sister clades. The first clade is composed of two sister groups (P. parvulus and P. pusillus), while the second constitutes an assemblage of the remaining five species. The relationships between the clades remain unresolved.     

Early development of bioluminescence suggests camouflage by counter‐illumination in the velvet belly lantern shark Etmopterus spinax (Squaloidea: Etmopteridae)

The development of luminous structures and the acquisition of luminescence competence during the ontogeny of the velvet belly lantern shark Etmopterus spinax, a deep‐sea squalid species, were investigated. The sequential appearance of nine different luminous zones during shark embryogenesis were established, and a new terminology for them given. These zones form the complex luminous pattern observed in free‐swimming animals. The organogenesis of photophores (photogenic organs) from the different luminous zones was followed, and photophore maturation was marked by the appearance of green fluorescent vesicles inside the photocytes (photogenic cells). Peroxide‐induced light emissions as well as spontaneous luminescence analysis indicated that the ability of E. spinax to produce light was linked to the presence of these fluorescent vesicles and occured prior to birth. The size of photogenic organs, as well as the percentage of ventral body surface area occupied by the luminous pattern and covered by photophores increased sharply during embryogenesis but remained relatively stable in free‐swimming animals. All these results strongly suggest camouflage by counter‐illumination in juvenile E. spinax.     

Description of epithelial granular cell in catshark spiral intestine: Immunohistochemistry and ultrastructure

We evaluated the histology of the spiral intestine of the blackmouth catshark (Galeus melastomus), a small shark distributed in the eastern Atlantic and Mediterranean Sea basin. Entire digestive tracts of 10 G. melastomus were studied using histochemical, immunohistochemical, and ultrastructural methods. Our studies identified a unique, large granular cell type in the intestinal epithelium. Transmission electron microscopy showed that the epithelial granular cell type made intimate contact, by means of junctional complexes, with adjacent epithelial and mucous cells. Several histochemical staining methods showed that the cytoplasmic granules were strongly eosinophilic. Immunostaining of intestinal sections revealed immunoreactivity of the granular cell to tumor necrosis factor-α (TNF-α) antibody. However, no reactivity to inducible-nitric oxide synthase (i-NOS), interleukin-6 (IL-6), interleukin IL-1β, lysozyme, serotonin 5-HT antibodies was detected.     

Deep‐water fish assemblages in the central‐western Mediterranean (south Sardinian deep‐waters)

This paper explores structure and spatial distribution of fish assemblages in an area of the central‐western Mediterranean Sea (south Sardinian deep‐waters) at depths between 546 and 1598 m. A total of 67 species (12 chondrichthyes and 55 teleosteans) were sampled. Multivariate analysis showed a clear pattern of zonation. Three main assemblages were identified within the vertical range investigated: the first situated in the shallower area between 546 and 699 m, the second group between 720 and 1099 m, and the third between 1145 and 1598 m. Abundance values declined with increasing depth. Highest biomass values were found at depths of 720–1099 m with the presence of larger species such as Galeus melastomus, Mora moro, Trachyrhynchus scabrus and Alepocephalus rostratus. Species richness decreased with depth. The deepest bottoms of the central‐western Mediterranean Sea shelter an ichthyofauna dominated by small to medium‐sized species living in a food‐scarce environment in which some large mobile fishes are widespread.     

The Systematics and Reproductive Biology of the Galeus arae Subspecific Complex (Chondrichthyes: Scyliorhinidae)

Galeus arae is currently classified as a complex of three subspecies (Galeus arae arae, Galeus arae antillensis, and Galeus arae cadenati). Morphometric and meristic analyses, size at maturity, and variation in color patterns, support the recognition of these taxa as distinct species. All species have well-developed nidamental glands and are oviparous. Galeus arae comprises two geographically disjunct populations that are not distinguishable by the characters we examined. A northern population occurs along the east and Gulf coasts of North America from South Carolina to the Mississippi delta, and the northern coast of Cuba to the north-eastern tip of the Yucatan. A southern population occurs along the Caribbean coasts of Honduras, Nicaragua, and Costa Rica, and some neighboring islands. Galeus antillensis occurs on the northern coasts of Hispaniola and Puerto Rico, and off many of the Leeward Islands. Galeus cadenati occurs off the Caribbean coasts of Panama and Colombia. Distributional data suggest that the three species are distributed allopatrically.     

Octopods of the Canary Islands. New records and biogeographic relationships

Two octopod species are reported from the Canary Islands (eastern Atlantic Ocean) for the first time: the deep sea four-horn octopus, Pteroctopus tetracirrhus (Delle Chiaje, 1830) and the gelatinous giant octopus, Haliphron atlanticus Steenstrup, 1861. Both female specimens were caught in Tenerife. Haliphron atlanticus is described from fresh remains found floating close to the southwest coast and the second species, P. tetracirrhus, is described from a specimen captured in a shrimp trap at 200 m depth on the southeastern coast of Tenerife. With these two additions the revised and updated list of octopod species of the Canary Islands now comprises eight families and 18 species, all of them incirrate octopods. The zoogeographic relationships of octopod species from other Atlantic regions, including the Mediterranean Sea, were studied. The likely directions of faunal flows were inferred based on affinity indices, showing that Mauritania could be the most probable source of the octopod species of the Canary Islands and the rest of the Macaronesian archipelagos.     

Redescription of a poorly known acropomatid, <Emphasis Type="Italic">Verilus sordidus</Emphasis> Poey 1860, and comparison with <Emphasis Type="Italic">Neoscombrops atlanticus</Emphasis> Mochizuki and Sano 1984 (Teleostei: Perciformes)

A poorly known acropomatid, Verilus sordidus Poey 1860, is redescribed based on six specimens from the western central Atlantic. We present diagnostic characters to differentiate this species from Neoscombrops atlanticus Mochizuki and Sano 1984, which has been confused with this species, and designate a neotype of V. sordidus. This species is distinguishable from N. atlanticus by the proximal-middle radial of the first anal-fin pterygiophore being slender with no trough or hollow on the anterodorsal portion (vs. hollow in N. atlanticus), several canine teeth posterior to the large canine teeth on either side of the symphysis of the lower jaw (vs. villiform teeth posterior to enlarged canines), and by the modal numbers of pectoral-fin rays, lateral-line scales, and gill rakers on the lower limb of the first arch.     

Photon Hunting in the Twilight Zone: Visual Features of Mesopelagic Bioluminescent Sharks

The mesopelagic zone is a visual scene continuum in which organisms have developed various strategies to optimize photon capture. Here, we used light microscopy, stereology-assisted retinal topographic mapping, spectrophotometry and microspectrophotometry to investigate the visual ecology of deep-sea bioluminescent sharks [four etmopterid species (Etmopterus lucifer, E. splendidus, E. spinax and Trigonognathus kabeyai) and one dalatiid species (Squaliolus aliae)]. We highlighted a novel structure, a translucent area present in the upper eye orbit of Etmopteridae, which might be part of a reference system for counterillumination adjustment or acts as a spectral filter for camouflage breaking, as well as several ocular specialisations such as aphakic gaps and semicircular tapeta previously unknown in elasmobranchs. All species showed pure rod hexagonal mosaics with a high topographic diversity. Retinal specialisations, formed by shallow cell density gradients, may aid in prey detection and reflect lifestyle differences; pelagic species display areae centrales while benthopelagic and benthic species display wide and narrow horizontal streaks, respectively. One species (E. lucifer) displays two areae within its horizontal streak that likely allows detection of conspecifics'' elongated bioluminescent flank markings. Ganglion cell topography reveals less variation with all species showing a temporal area for acute frontal binocular vision. This area is dorsally extended in T. kabeyai, allowing this species to adjust the strike of its peculiar jaws in the ventro-frontal visual field. Etmopterus lucifer showed an additional nasal area matching a high rod density area. Peak spectral sensitivities of the rod visual pigments (λ_max) fall within the range 484–491 nm, allowing these sharks to detect a high proportion of photons present in their habitat. Comparisons with previously published data reveal ocular differences between bioluminescent and non-bioluminescent deep-sea sharks. In particular, bioluminescent sharks possess higher rod densities, which might provide them with improved temporal resolution particularly useful for bioluminescent communication during social interactions.