Identification of multiple nursery habitats of skates in the eastern Bering Sea

The use of more than a single nursery habitat type is examined for oviparous elasmobranchs using data summarized from studies conducted on the Alaska skate Bathyraja parmifera and the Aleutian skate Bathyraja aleutica in the eastern Bering Sea. The eastern Bering Sea skate species use two discrete areas as nurseries, one for egg deposition and a second for newly emergent juveniles. Egg deposition sites were located along the outer shelf and upper slope near canyons in the eastern Bering Sea. Newly emergent juveniles were found along the outer and middle shelf for B. parmifera and deep‐slope for B. aleutica, suggesting that habitat used by newly emergent juvenile skates is distinct from habitat used for egg deposition and embryo development. In reviewing many studies on oviparous elasmobranchs, similar patterns emerge of habitat use during their early life history. To distinguish these distinct habitats, appropriate terminology is proposed. Egg case nursery is suggested for areas of egg deposition and juvenile nursery is suggested for areas where juveniles aggregate after emergence. Criteria to describe each habitat type are outlined.     

Age and growth of big skate (Raja binoculata) and longnose skate (R. rhina) in the Gulf of Alaska

In 2003, big skates, Raja binoculata, and longnose skates, Raja rhina, were the target of a commercial fishery around Kodiak Island in the Gulf of Alaska (GOA) for the first time. The sudden development of a fishery for these species prompted the need for improved life history information to better inform fishery managers. Due to the selective nature of the skate fishery, mostly larger individuals were captured. Back-calculation from skate vertebral measurements was used to estimate size-at-age for younger skates. Because back-calculated age-length data within individuals were highly correlated, bootstrap resampling methods were used to test for differences between male and female growth curves. Results from bootstrapping indicated that differences between male and female growth were statistically significant for both species. This investigation indicates that growth of big skates in the GOA (max size 178 cm total length, max age 15 years) is similar to that in California, but different from that in British Columbia. For longnose skates, our GOA results agree with those reported in British Columbia, but were considerably older (max size 130 cm, max age 25 years) than those reported in California, which may not be surprising because longnose skates in the present study were generally larger. This life history information suggests that both big and longnose skates are at risk of unsustainable exploitation by targeted fisheries.     

Life‐history traits of the long‐nosed skate Dipturus oxyrinchus

This work investigates life‐history traits of the long‐nosed skate Dipturus oxyrinchus, which is a common by‐catch in Sardinian waters. The reproductive variables were analysed from 979 specimens sampled during scientific and commercial hauls. Females (10·4–117·5 cm total length, L_T) attained larger sizes than males (14·5–99·5 cm L_T). To evaluate age and growth, a sub‐sample of 130 individuals (76 females and 54 males) were used. The age was estimated by annuli counts of sectioned vertebral centra. Four models were used for the length‐at‐age data: the von Bertalanffy, the exponential, the Gompertz and the logistic functions. According to the Akaike's information criterion, the Gompertz model seemed to provide the best fitting curve (L_∞ mean ± s.e. : 127·55 ± 4·90 cm, k: 0·14 ± 0·09, IP: 3·97 ± 0·90 years). The oldest female and male were aged 17 (115·5 cm L_T) and 15 years (96·0 cm L_T), respectively. Lengths at maturity were 103·5 cm for females and 91·0 cm for males, corresponding to 90% of the maximum observed length in both sexes. The monthly distribution of maturity stages highlighted an extended reproductive cycle, with spawning females and active males being present almost throughout the year, as confirmed by the gonado‐somatic index. Ovarian fecundity reached a maximum of 26 yolked follicles with a mean ± s.e. size of 19·7 ± 6·5 mm.     

Seamount egg‐laying grounds of the deep‐water skate Bathyraja richardsoni

Highly localized concentrations of elasmobranch egg capsules of the deep‐water skate Bathyraja richardsoni were discovered during the first remotely operated vehicle (ROV) survey of the Hebrides Terrace Seamount in the Rockall Trough, north‐east Atlantic Ocean. Conductivity–temperature–depth profiling indicated that the eggs were bathed in a specific environmental niche of well‐oxygenated waters between 4·20 and 4·55° C, and salinity 34·95–35·06, on a coarse to fine‐grained sandy seabed on the seamount's eastern flank, whereas a second type of egg capsule (possibly belonging to the skate Dipturus sp.) was recorded exclusively amongst the reef‐building stony coral Solenosmilia variabilis. The depths of both egg‐laying habitats (1489–1580 m) provide a de facto refuge from fisheries mortality for younger life stages of these skates.     

Southern African skate biodiversity and distribution

The skates (Family Rajidae) have 12 genera and possibly 28 species off southern Africa (southern Angola, Namibia, South Africa and Mozambique). The geographic and bathymetric distribution and the taxonomic composition of the southern African skate fauna are analysed and the distribution mapped. The southern African skate fauna is best known off the temperate west coast of South Africa from the intertidal to approximately 1,200 meters, but poorly known below 1,200 m and sketchily known in warm-temperate and tropical parts of the area. Southern African skates of the temperate continental shelves above 100 m are not diverse and regularly include one species of the genus Dipturus, one species of Leucoraja, two species of Raja (including R. straeleni, the most abundant skate in southern African waters) and the giant skate Rostroraja alba. All of these skates are ‘shelf overlap’ species that range onto the outer shelves and uppermost slopes, and none are confined to inshore environments. Skate diversity increases on the outer shelves and upper slopes. At least half of the skate species are endemic to the southern African region; other species also occur off East or West Africa, a few extend to European waters, and records of one species, Amblyraja taaf, appear to be of strays from nearby sub-Antarctic seas. The genus Bathyraja and softnose skate group (Arhynchobatinae) are surprisingly limited (a single species) in deep-water off southern Africa (unlike other regions including the Antarctic), and almost all of southern African skates are members of the Rajinae. Amongst rajines, the tribes Amblyrajini (Amblyraja, two species, Leucoraja, two species, and Rajella, five species) Rajini (Dipturus, six species, Okamejei, one species, Raja, two species, and Rostroraja, one species), and Anacanthobatini (Anacanthobatis, two species, and Cruriraja, three species) predominate, while Gurgesiellini has a species of Neoraja and possibly two of Malacoraja.     

Reanalysis of long‐term surveys on the ecology and biology of mud skate (Rhinoraja taranetzi Dolganov, 1985) in the northwestern Pacific (1993–2002)

Based on data sampled in 1992–2002, the occurrence, spatial distribution, bathymetry, bottom temperatures preferences, size composition, feeding, and some features of reproductive biology of mud skate Rhinoraja taranetzi in the Pacific waters off the northern Kuril Islands and southeastern Kamchatka are considered. Throughout the year, the mud skate was most abundant in the central part of the study area, from the coast of Onekotan Island to the southern tip of Kamchatka peninsula. The proportion of this species in bottom trawl catches in different seasons has changed slightly. However, maximum catch occurred in September–December. In April–May mud skates occupied shallower depths (mean 230–270 m), moving deeper in the summer period (mean 340–390 m). In December–March the skate occurred at lower bottom temperatures (mean 0.8–1.6°C) whereas the rest of the year it inhabited warmer waters with mean bottom temperatures of 2.5–3.1°C. Throughout the year decreasing body weight with depth was observed, indicating that adult and juvenile mud skates inhabit different depths. Total length of mud skates in catches ranged from 17 to 70 cm with a mean of 51.71 cm. Relation between total length (TL, cm) and body weight (W, g) was: W = 0.0029TL^3.1614 (r² = 0.978). Males were more abundant among small skates (<30 cm) only, whereas females predominated among larger skates (>30 cm) comprising about 70% in 60–70 cm length class. Female mud skates were longer and heavier than males (mean length 56.9 vs 51.2 cm and mean weight 1206 vs 807 g, respectively). This species is considered to be benthophagous, consuming mostly amphipods (34.9% by weight), polychaete worms (27.6%), decapod crustaceans (12.7%), and fishery discards (13.9%). Small skates (20–40 cm) fed mostly on amphipods (85.4%); medium‐sized (40–60 cm) ate amphipods (40.2%), polychaetes (29.1%) and decapods (19.3%); the largest individuals (>60 cm) consumed fishery offal (27.9%) and less amphipods (26.6%) and polychaetes (27.7%). Preliminary data on the maturation of the species in the western Bering Sea showed that males and females become mature at lengths above 61 cm TL.     

Chondrichthyan egg cases from the south-west Atlantic Ocean

Egg cases of 21 oviparous chondrichthyan species from the south-west Atlantic Ocean are described and compared. The catshark Schroederichthys bivius has a cigar-shaped egg case with curled tendrils only at the posterior end. Egg cases of the elephant fish Callorhinchus callorynchus are spindle-shaped with anterior and posterior tubular extensions and lateral flanges. The skate Amblyraja doellojuradoi presents medium-sized egg cases (71 mm in length) with a lateral keel extending to the first portion of the horns. The endemic skate species of the genus Atlantoraja have medium to large egg cases (69-104 mm in length) and present relatively large posterior horns. Egg cases of the genus Bathyraja have a medium size, 75-98 mm in length, and are characterized by a very similar morphology, a relatively smooth to rough surface case and posterior horns strongly curved inwards. Egg cases of the genera Dipturus and Zearaja are very large, 115-230 mm in length, and have a well-developed posterior apron. Despite the problematical identification of skates at species level, the egg capsules of the endemic genus Psammobatis are easily diagnosed; the capsules are small (25-53 mm in length), those of Psammobatis rutrum being the smallest known to date in the world. Egg cases of Rioraja agassizi have a medium size, 61-68 mm in length, relatively straight sides, a smooth surface and silky attachment fibres placed in the lateral keel next to each horn. Those of the genus Sympterygia are small to medium sized, 51-86 mm in length, and display the thickest lateral keel and the longest posterior horns among the skates of the world. Egg cases can be a useful tool for identifying species and egg-laying areas; therefore, a provisional key for the south-west Atlantic Ocean chondrichthyan capsules is presented.     

Observations on the electric organ discharge of two skate species (Chondrichthyes: Rajidae) and its relationship to behaviour

Synopsis The electric organ discharge (EOD) of the little skate,Raja erinacea and winter skate,R. ocellata was recorded both from isolated individuals and from small groups using methods that allowed for the identification of individuals producing EODs. Pulse duration, train lengh, frequency, and pulse patterns are characterized and correlated with behaviour. The two species,R. erinacea andR. ocellata, were found to have characteristically different EOD pulse durations of 70 ms and 217 ms respectively. Isolated skates rarely discharged whereas groups of skates were found to discharge regularly. The EOD was evoked by tactile prodding, physical contact with other skates and electrical stimulation. Skates also discharged reflexively in response to an artificially induced head-positive DC stimulus, sine wave and monopolar square pulses. During approach and contact, skates responded to each other with interacting EOD displays. EOD interaction and pulse duration differences between other species suggest a possible intra-specific communication function of the EOD inRaja.     

Embryonic development of the axial column in the little skate,Leucoraja erinacea

The morphological patterns and molecular mechanisms of vertebral column development are well understood in bony fishes (osteichthyans). However, vertebral column morphology in elasmobranch chondrichthyans (e.g., sharks and skates) differs from that of osteichthyans, and its development has not been extensively studied. Here, we characterize vertebral development in an elasmobranch fish, the little skate, Leucoraja erinacea , using microCT, paraffin histology, and whole‐mount skeletal preparations. Vertebral development begins with the condensation of mesenchyme, first around the notochord, and subsequently around the neural tube and caudal artery and vein. Mesenchyme surrounding the notochord differentiates into a continuous sheath of spindle‐shaped cells, which forms the precursor to the mineralized areolar calcification of the centrum. Mesenchyme around the neural tube and caudal artery/vein becomes united by a population of mesenchymal cells that condenses lateral to the sheath of spindle‐shaped cells, with this mesenchymal complex eventually differentiating into the hyaline cartilage of the future neural arches, hemal arches, and outer centrum. The initially continuous layers of areolar tissue and outer hyaline cartilage eventually subdivide into discrete centra and arches, with the notochord constricted in the center of each vertebra by a late‐forming “inner layer” of hyaline cartilage, and by a ring of areolar calcification located medial to the outer vertebral cartilage. The vertebrae of elasmobranchs are distinct among vertebrates, both in terms of their composition (i.e., with centra consisting of up to three tissues layers—an inner cartilage layer, a calcified areolar ring, and an outer layer of hyaline cartilage), and their mode of development (i.e., the subdivision of arch and outer centrum cartilage from an initially continuous layer of hyaline cartilage). Given the evident variation in patterns of vertebral construction, broad taxon sampling, and comparative developmental analyses are required to understand the diversity of mechanisms at work in the developing axial skeleton of vertebrates. J. Morphol. 278:300–320, 2017. © 2017 Wiley Periodicals, Inc.     

Using biological variables and reproductive strategy of the undulate ray Raja undulata to evaluate productivity and susceptibility to exploitation

The present work provides a detailed analysis of the reproductive strategy of the undulate ray Raja undulata in Portuguese mainland waters. The species was found mostly between 30 and 40 m deep on sandy bottoms. Egg‐laying sites were observed in the north, centre and south‐west regions, mainly at depths below 30 m. The peak of the reproductive season occurred from December to May. Asynchrony between reproductively active females and males appeared to occur, although most adult males were capable of reproducing throughout the year. The estimated length at 50% maturity was 86·2 cm (8·7 years) and 76·8 cm (7·6 years) total length for females and males, respectively. The maximum potential fecundity was estimated to be 69·8 follicles per female per reproductive season, which are released in 4·7 batches of 15 follicles. The life‐history and demographic parameters of R. undulata are similar to those of other skate species, while the potential rate of population increase (0·49) is above the published values for other elasmobranch species. With these new findings, this study makes an important contribution to the understanding of the life history of R. undulata, and provides a first evaluation of the productivity and susceptibility of the species to exploitation.     

In situ observations of a possible skate nursery off the western Antarctic Peninsula

A dense aggregation of skate egg cases was imaged during a photographic survey of the sea floor along the western Antarctic Peninsula in November 2013. Egg cases were noted in a narrow band between 394 and 443 m depth. Although some skate species in other oceans are known to utilize restricted areas to deposit eggs in great numbers, such nurseries have not been described in the Southern Ocean.     

Age,growth, and age at sexual maturity of the commercially landed skate species,Dipturus chinensis (Basilewsky, 1855), in the northern East China Sea

Age, growth, and age at sexual maturity of the polkadot skate Dipturus chinensis, in the northern East China Sea were determined for a total of 614 specimens collected from April 2009 to December 2014. Vertebral centrum analysis was used to calculate the age of the skates. Annual band deposition was determined by marginal increment analysis. The von Bertalanffy growth model was fitted to the observed length‐at‐age data for each sex (males, L_∞ = 76.8, k = 0.109, t₀ = ?1.28; females, L_∞ = 83.1, k = 0.103, t₀ = ?1.20). Growth patterns of females and males were similar until the age of 6; thereafter, females grew larger than males. Maximum age recorded was 13 years for males and 15 years for females. Age at 50% sexual maturity was 8.22 years for males and 9.39 years for females. These results indicate that D. chinensis is slow growing, relatively long‐lived, and late maturing, and therefore vulnerable to exploitation.     

First confirmed complete incubation of a flapper skate (Dipturus intermedius) egg in captivity

An egg of the critically endangered flapper skate Dipturus intermedius was successfully incubated to hatching in captivity in what is believed to be a first for the species. Water conditions (temperature, salinity, flow rate) were recorded, with mean water temperatures ranging from a monthly mean of 8.3 ± 1.2 to 13.2 ± 0.3°C and salinity from a monthly mean of 30.5 ± 1.2 to 36.6 ± 2.3 ppt. Hatching occurred after 534 days, suggesting that flapper skate eggs take c. 5700 growing degree-days to incubate to hatching. The egg's prolonged embryonic development raises concerns about flapper skate eggs' vulnerability to anthropogenic disturbance.     

The first confirmed cases of full albinism in rajid species

Three albino skate specimens (Rajidae) were captured from the North Sea and English Channel between 2008 and 2011. Using DNA barcoding (COI gene) and morphometric analyses, species were identified as a spotted ray Raja montagui, a blonde ray Raja brachyura and a thornback ray Raja clavata. This finding represents the first record of full albinism (a lack of skin and retinal pigmentation) in rajid species.     

Skate Bathyraja spp. egg predation in the eastern Bering Sea

Predation on skate eggs by snails was examined for three skate species at seven nursery sites in three regions (north, middle and south) of the eastern Bering Sea. Mean predation levels were 6·46% for the Alaska skate Bathyraja parmifera , 2·65% for the Aleutian skate Bathyraja aleutica and 22·25% for the Bering skate Bathyraja interrupta . Predation levels were significantly higher at the middle and north sites than the south sites for all species combined. Predation levels decreased with increasing egg-case densities at all nursery sites, and the highest predation levels occurred where egg-case densities were very low. Predated egg-case density increased with increasing snail densities across all nursery sites examined. The Oregon triton Fusitriton oregonensis was the most abundant snail species at all nursery sites and displayed ability to drill holes in the egg case of B. parmifera. Holes left by predatory snails in egg cases of B. parmifera were significantly larger, and of different shape at the middle site compared to the south site. Holes in B. parmifera were also significantly larger than those in egg cases of B. interrupta across all sites examined. Egg cases of B. aleutica possess surface spines that cover the egg case and may inhibit predation by snails at a greater rate than that of the B. parmifera and B. interrupta , which have a smoother egg-case surface.     

Size at maturity and egg capsules of the softnose skates Bathyraja brachyurops (Fowler, 1910) and Bathyraja macloviana (Norman, 1937) (Elasmobranchii: Rajidae) in the SW Atlantic (37°00'–39°30'S)

The softnose skates Bathyraja brachyurops and Bathyraja macloviana represent an important portion of the skate catches of the Uruguayan trawling fleet in the southwestern Atlantic. From March to October 2004, specimens of these species were collected at 75–200 m depth range in the area situated between latitudes 37°00'–39°30'S. For B. brachyurops , total length at which 50% of the specimens were retained by the gear was 68.0 cm for both sexes; T _L50 was estimated at 65.4 cm for males and 67.0 cm for females. For B. macloviana, total length at which 50% of the specimens were retained was 56.0–57.0 cm for both sexes; T _L50 was estimated at 53.5 cm for males and 52.0 cm for females. Egg capsule length varied from 79–91 mm in B. brachyurops and 69–75.5 mm in B. macloviana . In both species, capsules displayed striated surfaces and similar gross morphology, although egg capsules of B. macloviana had more robust anterior horns and a smaller size than those of B. brachyurops . Egg capsules of the latter also exhibited microscopical prickles. Capsule edges were laterally keeled with a groove along the keel, and a straight and transverse velum was present in the egg capsules of both species.     

Food habits of the longnose skate, <Emphasis Type="Italic">Raja rhina</Emphasis> (Jordan and Gilbert, 1880), in central California waters

Feeding studies can provide researchers with important insights towards understanding potential fishery impacts on marine systems. Raja rhina is one of the most common elasmobranch species landed in central and northern California demersal fisheries, yet life history information is extremely limited for this species and aspects of its diet are unknown. Specimens of R. rhina were collected between September, 2002 and August, 2003 from fisheries-independent trawl surveys. Percent Index of Relative Importance values indicated that the five most important prey items in 618 stomachs of R. rhina were unidentified teleosts (31.6% IRI), unidentified shrimps (19.6% IRI), unidentified euphausiids (10.9% IRI), Crangonidae (7.4% IRI), and Neocrangon resima (6.0% IRI). There were significant dietary shifts with increasing skate total length and with increasing depths. Smaller skates ate small crustaceans and larger skates ate larger fishes and cephalopods. With increasing depths, diet included bentho-pelagic teleosts and more cephalopods and euphausiids. The findings of this study are consistent with previous researchers that report similar diet shifts in skate species with size and depth.     

Embryo developmental events and the egg case of the Aleutian skate Bathyraja aleutica (Gilbert) and the Alaska skate Bathyraja parmifera (Bean)

Embryo development events were correlated with egg-case changes for the Aleutian skate Bathyraja aleutica and the Alaska skate Bathyraja parmifera . Yolk absorption underwent two phases: that of steady absorption during early development and that of rapid yolk absorption during the final development stages. Total length ( L _T) for 50% of the pre-hatching embryos egg-case jelly disappearance was 92·04 mm (range 81–102 mm) and 99·36 mm (range 81–100 mm) for B. aleutica and B. parmifera , respectively, allowing the inner chamber to open to seawater flow. The tail filament underwent three phases of growth: rapid elongation during early development (<100 mm embryo L _T), stasis of tail filament length during the remainder of embryo development and rapid absorption soon after hatching. Complete tail filament development coincided with the disappearance of egg-case jelly. Clasper buds first developed at embryos >70 mm L _T for both species and the sex ratio was 1:1 well before hatching. Egg cases that were devoid of an ova or developing embryo were c. 5·0 and 6·5% of the egg cases examined for B. aleutica and B. parmifera , respectively. Measurements showed that egg cases containing only egg jelly were smaller in both width and length than those possessing an ova. Embryo stages were punctuated with distinct events that correlated with egg case changes controlling the internal environment of the developing embryo.     

Almost a century of oblivion: Integrative taxonomy allows the resurrection of the longnose skate Zearaja brevicaudata (Marini, 1933) (Rajiformes; Rajidae)

Zearaja chilensis has been reported from Southern Brazil in the Southwest Atlantic (SWA) to northern Chile in the Southeast Pacific (SEP), and it was listed as vulnerable by the IUCN. Recent molecular studies have called into question the conspecificity between specimens from these opposite coasts of South America, which can have implications for the conservation status of the species. To verify the identity of specimens identified as Z. chilensis, 47 individuals from SWA and 22 from SEP were examined. By comparing external morphology, spinulation pattern, clasper, egg cases, and mitochondrial cytochrome c oxidase I (COI) sequence data, differences between groups were found. Adults from SWA presented longer snout length and shorter tail than those from SEP. Dermal denticles were restricted to the rostral area in SWA skates, whereas in SEP skates most of the dorsal surface was covered with denticles. Marked differences in the morphology of several components of clasper were noticeable. Egg cases of SWA skates had thinner lateral keels than those of SEP. Molecular analysis revealed two well-defined cohesive clusters, corresponding to SWA and SEP specimens, respectively. Average K2P distance between groups was 3.4%, higher than expected for intraspecific differences, and sequences were assigned to different BINs. These integrative approaches strongly support that specimens from SWA known as Z. chilensis correspond to a different nominal species than those from SEP. Herein, Z. brevicaudata (Marini 1933) is resurrected from synonymy with Z. chilensis.