Standardized diet compositions and trophic levels of skates (Chondrichthyes: Rajiformes: Rajoidei)

Skates by virtue of their abundance and widespread occurrence appear to play an influential role in the food webs of demersal marine communities. However, few quantitative dietary studies have been conducted on this elasmobranch group. Therefore, to better understand the ecological role of skates, standardized diet compositions and trophic level (TL) values were calculated from quantitative studies, and compared within and among skate and shark taxa. Prey items were grouped into 11 general categories to facilitate standardized diet composition and TL calculations. Trophic level values were calculated for 60 skate species with TL estimates ranging from 3.48 to 4.22 (mean TL = 3.80 ± 0.02 SE). Standardized diet composition results revealed that decapods and fishes were the main prey taxa of most skate species followed by amphipods and polychaetes. Correspondingly, cluster analysis of diet composition data revealed four major trophic guilds, each dominated by one of these prey groups. Fish and decapod guilds were dominant comprising 39 of 48 species analyzed. Analysis of skate families revealed that the Arhynchobatidae and Rajidae had similar TL values of 3.86 and 3.79 (t-test, P = 0.27), respectively. The Anacanthobatidae were represented by a single species, Cruriraja parcomaculata, with a TL of 3.53. Statistical comparison of TL values calculated for five genera (Bathyraja, Leucoraja, Raja, Rajella, Rhinoraja) revealed a significant difference between Bathyraja and Rajella (t-test, P = 0.03). A positive correlation was observed between TL and total length (L _T) with larger skates (e.g. >100 cm L _T) tending to have a higher calculated TL value (>3.9). Skates were found to occupy TLs similar to those of several co-occurring demersal shark families including the Scyliorhinidae, Squatinidae, and Triakidae. Results from this study support recent assertions that skates utilize similar resources to those of other upper trophic-level marine predators, e.g. seabirds, marine mammals, and sharks. These preliminary findings will hopefully encourage future research into the trophic relationships and ecological impact of these interesting and important demersal predators.     

Zoogeography and relationships of Australasian skates (Chondrichthyes: Rajidae)

Aim To investigate distributional patterns and derivation of skates in the Australasian realm. Location Australasia. Methods Genus‐group skate taxa were defined for this region for the first time and new systematic information, as well as bathymetric and geographical data, used to identify distribution patterns. Results The extant skate fauna of Australasia (Australia, New Zealand, New Caledonia and adjacent subAntarctic dependencies) is highly diverse and endemic with sixty‐two species from twelve currently recognized, nominal genus‐group taxa. These include the hardnose skate (rajin) groups Anacanthobatis, Amblyraja, Dipturus, Okamejei, Rajella and Leucoraja, and softnose skate (arhynchobatin) genera Arhynchobatis, Bathyraja, Insentiraja, Irolita, Pavoraja and Notoraja. Additional new and currently unrecognized nominal taxa of both specific and supraspecific ranks also occur in the region. The subfamily Arhynchobatinae is particularly speciose in Australasia, and the New Zealand/New Caledonian fauna is dominated by undescribed supraspecific taxa and species. The Australian fauna, although well represented by arhynchobatins, is dominated by Dipturus‐like skates and shows little overlap in species composition with the fauna of New Zealand and New Caledonia. Similarly, these faunas exhibit no overlap with the polar faunas of the Australian subAntarctic dependencies (Heard and Macdonald Islands) to the south. Skates appear to be absent from the Macquarie Ridge at the southern margin of the New Zealand Plateau. Their absence off New Guinea probably reflects inadequate sampling and the subsequent poor knowledge of that region's deepwater fish fauna. Main conclusions Skates appear to have existed in the eastern, Australasian sector of Gondwana before fragmentation in the late Cretaceous. The extant fauna appears to be derived from elements of Gondwanan origin, dispersal from the eastern and western Tethys Sea, and intraregional vicariance speciation.     

Electric organs in skates: Variation and phylogenetic significance (Chondrichthyes: Rajoidei)

A total of 63 species of skates (Chondrichthyes: Rajoidei) were surveyed, along with three species of the outgroup (Chondrichtyes: Rhinobatoidei) for electric organs along the sides of the tail. All skate specimens examined possessed what appeared to be functional electric organs, and the three species of the outgroup lacked evidence of electric organs. The electric organs were tail-positive and arranged into horizontal columns divided by transverse septa. The electrocytes varied considerably within and among supraspecific taxa (subgenera and genera), but they could be broadly classified into cup-shape, modified cup-shape, intermediate-shape, and disc-shape cells, provided that the distinction was partially based on position of the electrocytes within their connective tissue chambers. The survey, in part, corroborates a phylogenetic hypothesis of skates and in some respects further resolves the hypothesis. The supraspecific taxa Atlantoraja and Rioraja have similar derived-type electrocytes, as do the five supraspecific taxa of Rajini, and Cruriraja and Anacanthobatis, and to a lesser extent the supraspecific taxa Arhynchobatis, Psammobatis, and Sympterygia, and the supraspecific taxa Notoraja, Pavoraja, and Pseudoraja, corroborating the hypothesis. The supraspecific taxa Amblyraja, Rajella, Leucoraja, Breviraja, and Dactylobatus were unresolved in the phylogenetic hypothesis, but the electrocyte survey suggested that Leucoraja, Breviraja, and Dactylobatus were derived with respect to Amblyraja and Rajella. © 1994 Wiley-Liss, Inc.     

Development of molecular and morphological markers to improve species-specific monitoring and systematics of Northeast Atlantic and Mediterranean skates (Rajiformes)

The Northeast Atlantic and Mediterranean skates (Rajidae) showed remarkable species diversity but with high morphological and ecological conservatism. Since skates are particularly vulnerable to the bottom trawl fishery, species-specific demographic surveys as well as studies defining life history and evolutionary traits are important in prioritising conservation programs. However, the identification of juveniles and adults of some species may be difficult using referenced guidelines and identification keys. Therefore, we attempt to develop markers for species identification through the parallel analysis of a 16S rDNA gene sequence and of several morphological characters on 135 individuals collected by trawl surveys in the Adriatic Sea and putatively assigned to six taxa. Species-specific haplotypes were defined for Raja miraletus, Raja montagui, Dipturus oxyrinchus, since a solid accordance between species boundaries and well-differentiated haplotypes was observed. Comparative analysis of 16S rDNA sequences allowed the identification of three juvenile specimens of Leucoraja circularis, a species that rarely occurs in the Adriatic Sea. On the contrary, morphological traits and haplotype distribution were largely discordant in Raja asterias and R. clavata. While all putative R. clavata individuals showed a unique haplotype (H-CLA), only 8 of 30 putative R. asterias individuals possessed a second weakly divergent haplotype (H-AST). The remaining 22 R. asterias carried the H-CLA. The multivariate analyses of morphometric and meristic characters in putative R. clavata and R. asterias revealed the clustering of individuals regardless of haplotypes. However, a bimodal distribution of R. asterias and R. clavata samples would suggest that two separated taxa might exist, both sharing the two 16S rDNA haplotypes. The haplotype distribution appeared to be significantly correlated only to the standardised disc length/total length (DL/TL) variation. Three alternative explanations may support this scenario: (i) an incomplete lineage sorting process in two morphologically yet distinct taxa; (ii) a recent hybridisation between the two taxa; (iii) the two taxa are morphologically plastic species and all considered morphological characters may be misleading in discriminating between them at all maturity stages, except for the DL/TL. However, further analyses on larger data sets and using molecular key markers (i.e. nuclear genes) will be needed to definitely resolve the status of these taxa. Molecular relationships among rajid taxa are largely consistent with systematics based on internal and external anatomical features. This multidisciplinary study contributed to defining the pattern of species diversity and abundance of rajids in the Adriatic Sea.     

Survey of the variation in alar and malar thorns in skates: Phylogenetic implications (Chondrichthyes: Rajoidei)

A total of 62 species, representing 24 of the 28 supraspecific taxa of skates, was surveyed for the presence, distribution, and structure of alar and malar thorns. The survey revealed that alar thorns are almost universally present in mature male skates, and that malar thorns are of two types that may have separate origins. The location and orientation of alar thorns differed in two major clades of skates (groups I and II). They were either exposed on the disc with the crown oriented obliquely to the long axis of the base or imbedded in slits in the integument and oriented parallel to the long axis of the base. Group I possessed the former type of thorns and, with several exceptions, group II possessed the latter type. Group I either lacked malar thorns or possessed malar thorns that were most likely derived from generalized placoid scales. Group II possessed, with several exceptions, malar thorns derived from enlarged placoid scales. Within group I the supraspecific taxa Atlantoraja and Rioraja possessed unique alar thorns that were reclined laterally and associated with lateral grooves in the integument. Within group II the supraspecific taxa Anacanthobatis, Cruriraja, Dipturus, Okamejei, Raja, the North Pacific Assemblage, and the Amphi-American Assemblage had a large barb on the distal section of the crown of the alar thorn that suggests that these taxa form a clade. The crown of the alar thorns of the latter five supraspecific taxa was undulatory, thus supporting their monophyletic status. Another assemblage within group II had ridges that ran most of the length of the crown of the alar thorns corroborating their monophyletic status. The survey also suggested that variation of integumentary grooves associated with the alar thorns in Bathyraja, and presence or absence of malar thorns in Psammobatis, may be phylogenetically informative. © 1996 Wiley-Liss, Inc.     

Clasper morphology of skates of the tribe Riorajini (Chondrichthyes: Rajiformes: Arhynchobatidae) and its systematic significance

Claspers of adult specimens of the skate tribe Riorajini, family Arhynchobatidae, comprising Atlantoraja and Rioraja , are described, compared, and systematically reinterpreted based on material collected off southeastern and southern Brazil. For the first time the external components and musculature of the clasper of members of this tribe are described and related to internal (skeletal) structures. The component pecten is present in all species of Atlantoraja but absent in Rioraja . The new external component grip , an autapomorphy of A. cyclophora fully developed in adults, is described. Rioraja presents dorsal terminals 1 and 2, ventral marginal distally extended and ventral terminal cartilages. Dorsal terminals 1 and 2, ventral marginal distally extended, accessory terminals 2 and 3, and ventral terminal cartilages occur in Atlantoraja . A new interpretation of the ventral marginal distally extended is discussed. The dorsal terminal 1 of Atlantoraja has an inverted U shape but is triangular in Rioraja . The accessory terminal 2 cartilage is reported for the first time in Atlantoraja cyclophora . The accessory terminal 3 is present only in A. platana and A. cyclophora , and absent in Rioraja and A. castelnaui . Many of our findings concerning the clasper skeleton do not agree with previous interpretations. The arrangement, distribution and systematic significance of many of the terminal clasper components are discussed among rajoids.     

Preface: Biology of skates

Synopsis Skates have become a concern in recent years due to the preponderance of these elasmobranchs that are caught as bycatch or as a directed fishery. This has raised concern because skates have life history characteristics that may make them vulnerable to over-exploitation. It was due to this increasing awareness and concern about these batoids that prompted us to organize an international symposium on the “Biology of Skates”. The aims and goals of the symposium were to bring together an international group of researchers to meet, discuss, perhaps develop collaborations, and present their most recent findings. The symposium was held over two days, on 13–14 July, 2006, in conjunction with the 22nd annual meeting of the American Elasmobranch Society in New Orleans, LA. A total of 31 authors from four countries contributed 16 papers that appear in this special issue. The papers are broadly arranged into four separate categories: systematics and biogeography, diet and feeding ecology, reproductive biology, and age and growth. To the best of our knowledge this is the first dedicated book on the biology of skates. We hope that readers will find this issue of interest and that it helps encourage and stimulate future research into these fascinating fishes.     

Sexual dimorphism of external morphological characters in some deepwater skates (Rajidae,Rajiformes, Chondrichthyes) of the North Atlantic

Our studies of the external morphology of five species of deepwater skates (Amblyraja jenseni, Bathyraja pallida, B. richardsoni, Rajella bigelowi, and R. kukujevi) showed that their males and females differ significantly in 9 characters in the first species, 14 characters in the second, 11 characters in the third and fourth, and 10 characters in the fifth. Sexual differences occur most frequently in the length of the first gill slit (in four species out of five), the length of the nasal curtain, the mouth width, and the length of the third gill slit (in three species out of five), the width and length of the disc, the length of the first and second dorsal fin bases, the tail height at the tip of the ventral fin, the length of the fifth gill slit, the distance between the first and fifth gill slits, the interspiracular distance, the preanal length, distance from the tip of the snout to the maximum disc width, and the interorbital distance (in two species out of five).     

Raja koreana, a new species of skate (Elasmobranchii, Rajoidei) from Korea

A new rajid species,Raja koreana, is described from a single adult female specimen, 735 mm in total length, collected off the southwestern coast of the Korean Peninsula. AlthoughR. koreana is included in the group of species characterized by the scapulocoracoid lacking an anterior bridge and having the postventral fenestra expanded, it is unique among the latter in possessing: pectoral girdle propterygium not extending to snout tip; rostral shaft of neurocranium narrow and thick, unsegmented base with filamentous cartilage; snout fleshy; pores of ampullae of Lorenzini densely distributed over much of ventral surface to behind cloaca; most thorns on tail directed anteriorly; tail short; a pair of longitudinally elongated black blotches on middle of dorsal surface of disc when fresh; a pair of black blotches (grayish at center) posteriorly on pectoral fins; ventral surface of dise uniformly blackish-brown, except for areas around pores.     

DNA barcoding of the northern Northeast Atlantic skates (Chondrichthyes,Rajiformes), with remarks on the widely distributed starry ray

The skate fauna in the northern Northeast (NE) Atlantic is poorly investigated, and misidentifications are common. Here, ‘DNA barcoding’ was used to analyse 105 specimens of 15 species previously reported from the area to investigate the occurrence of species. Of these 15 species, three were new to the region and confirmed with voucher specimens. Three previously reported taxa were not obtained from the study area, providing a total number of 12 skate species for the northern NE Atlantic. Only one specimen of the critically endangered Dipturus batis complex was found. It occurs frequently in the literature and commercial fisheries catch records, and we argue that the vast majority of these are misidentifications. Due to striking differences in Amblyraja radiata life history parameters across the North Atlantic, cryptic species diversity has previously been suspected. A total of 80 A. radiata cytochrome c oxidase subunit I sequences from across the North Atlantic were sampled, and the highest fixation index (F_ST) was found when maximising geographical distance (F_ST = 0.133). A lower index was found when grouped according to life history (F_ST = 0.067). These results are not strongly supportive for the occurrence of cryptic species.     

DNA barcoding of Canada's skates

DNA-based identifications have been employed across broad taxonomic ranges and provide an especially useful tool in cases where external identification may be problematic. This study explored the utility of DNA barcoding in resolving skate species found in Atlantic Canadian waters. Most species were clearly resolved, expanding the utility for such identification on a taxonomically problematic group. Notably, one genus (Amblyraja) contained three of four species whose distributions do not overlap that could not be readily identified with this method. On the other hand, two common and partially sympatric species (Little and Winter skates) were readily identifiable. There were several instances of inconsistency between the voucher identification and the DNA sequence data. In some cases, these were at the intrageneric level among species acknowledged to be prone to misidentification. However, several instances of intergeneric discrepancies were also identified, suggesting either evidence of past introgressive hybridization or misidentification of vouchered specimens across broader taxonomic ranges. Such occurrences highlight the importance of retaining vouchered specimens for subsequent re-examination in the light of conflicting DNA evidence.     

Abnormal hermaphroditism in the multispine skate Bathyraja multispinis (Chondrichthyes, Rajidae)

A hermaphroditic individual of the multispine skate, Bathyraja multispinis , caught on the Argentinean continental shelf, is described. This is the first record of hermaphroditism in the genus Bathyraja and one of the very few hermaphroditic specimens reported in the Rajidae.     

Body plan convergence in the evolution of skates and rays (Chondrichthyes: Batoidea)

Skates, rays and allies (Batoidea) comprise more than half of the species diversity and much of the morphological disparity among chondrichthyan fishes, the sister group to all other jawed vertebrates. While batoids are morphologically well characterized and have an excellent fossil record, there is currently no consensus on the interrelationships of family-level taxa. Here we construct a resolved, robust and time-calibrated batoid phylogeny using mitochondrial genomes, nuclear genes, and fossils, sampling densely across taxa. Data partitioning schemes, biases in the sequence data, and the relative informativeness of each fossil are explored. The molecular phylogeny is largely congruent with morphology crownward in the tree, but the branching orders of major batoid groups are mostly novel. Body plan convergence appears to be widespread in batoids. A depressed, rounded pectoral disk supported to the snout tip by fin radials, common to skates and stingrays, is indicated to have been derived independently by each group, while the long, spiny rostrum of sawfishes similarly appears to be convergent with that of sawsharks, which are not batoids. The major extant batoid lineages are inferred to have arisen relatively rapidly from the Late Triassic into the Jurassic, with long stems followed by subsequent radiations in each group around the Cretaceous/Tertiary boundary. The fossil record indicates that batoids were affected with disproportionate severity by the end-Cretaceous extinction event.     

Molecular barcoding of skates (Chondrichthyes: Rajidae) from the southern Northeast Atlantic

Serra‐Pereira, B., Moura, T., Griffiths, A. M., Gordo, L. S. & Figueiredo, I. (2010). Molecular barcoding of skates (Chondrichthyes: Rajidae) from the southern Northeast Atlantic. —Zoologica Scripta, 40, 76–84. Due to their vulnerability to fishing pressure, many species of skate (Rajidae) in the Northeast Atlantic are undergoing declines in abundance. The assessment of stock status and subsequent proposal of management measures are often complicated by high levels of species diversity and endemism, coupled with morphological and ecological conservatism, which makes distinguishing between species difficult. To improve the identification of skates and investigate the phylogenetic position of endemic species the cytochrome c oxidase subunit I (COI) was sequenced in 12 species (Dipturus oxyrinchus, Leucoraja naevus, Leucoraja circularis, Neoraja iberica, Raja brachyura, Raja clavata, Raja maderensis, Raja microocellata, Raja miraletus, Raja montagui, Raja undulata, Rostroraja alba) inhabiting the Portuguese waters. Based on sequence divergence R. maderensis and R. clavata only differ by 1% of the 652 bp COI sequence, questioning the recognition of R. maderensis (considered to be endemic to Madeira and the Azores), as a reproductively isolated species. Otherwise, there was clear phylogenetic support for the different genera and all the remaining species, although the genetic divergence was low compared to other chordates. In particular, COI analysis allowed clear identification of the morphologically similar species R. brachyura and R. montagui.     

A morphological analysis of the ampullae of Lorenzini in selected skates (Pisces,Rajoidei)

A comparison of the ampullae of Lorenzini among 40 species of skates (Rajoidei) demonstrates a close relationship between inferred electroreceptive capabilities and feeding mechanisms. Three general lines of morphological modifications are noted. (1) Whereas the majority of ampullary pores are located on the ventral surface of the dorsoventrally flattened body, the relative proportion of ventral pores is significantly lower on species inhabiting aphotic waters. (2) The ventral pores on more piscivorous species are distributed over a larger portion of body surface than they are on those species that feed primarily on invertebrates. Ventral pores in this latter group are more noticeably concentrated around the mouth and their densities on the adult are inversely related to the overall mobility of preferred prey species. (3) The size of each ampulla and the number of alveoli associated with it are directly related to the habitat depth occupied by each species. Shallow-water species have smaller ampullae with fewer alveoli than deeper-dwelling (> 1,000 m) species. The general distribution of ampullary pores on deep dwelling rajoids appears to compensate for reduced visual input, whereas their relative densities are a measure of the system's resolution and reflect major differences in feeding strategies. The increased ampullary size and complexity observed in deep-sea rajoids provides mechanisms to increase both the sensitivity and signal-to-noise ratios.     

Walking in skates (Chondrichthyes, Rajidae): anatomy, behaviour and analogies to tetrapod locomotion

Pelvic fin walking in skates is common. However, the structure and function of pelvic fins have not been analysed. Pelvic fins of skates of the genus Psammobatis and Rioraja agassizi are externally divided into an anterior leg-like lobe and a posterior fin-like lobe. Internally, the anterior lobes are supported by a compound radial, a proximal radial and distal radials that resemble a thigh, a calf and a foot, respectively, and three associated radials arising from the pelvic girdle. A highly developed radial condyle on the pelvic girdle enables broad 'limb' movements. The muscular arrangement of the anterior lobes is formed by protractor, retractor, flexor and extensor muscles, clearly departing from the generalized fin muscle arrangement of elasmobranchs. Walking is composed of propulsion and recovery phases. A backward movement of the compound radial in the horizontal plane characterizes the propulsive phase. The proximal radial connects vertically the compoundradial with the foot-like distal radials, which are anchored on the bottom. During the recovery phase, the foot-like structure is lifted off the bottom and the entire limb-like anterior lobe is moved forwards for starting a new cycle. Walking in skates resembles the ancestral tetrapod sprawling locomotion seen in many salamanders and lizards. Pelvic fin anatomy and walking behaviour in skates and hemiscylliid sharksare compared. Ecological and evolutionary implications of walking locomotion in skates are also discussed.  © 2002 The Linnean Society of London, Biological Journal of the Linnean Society , 2002, 77 , 35–41.     

Possible occurrence of character displacement in the sympatric skates Raja erinacea and R. ocellata (Pisces: Rajidae)

Synopsis Raja erinacea and R. ocellata are sibling species which are positively correlated with each other by occurrence and numerical abundance. In sympatry the species undergo interactive segregation; R. erinacea feeds on a higher percentage of epifauna and R. ocellata feeds on a higher percentage of infauna.An isolated allopatric population of R. ocellata occurs in the Gulf of St. Lawrence which is phenotypically intermediate between the sympatric populations of R. erinacea and R. ocellata in characters related to feeding e.g. size, number of tooth rows in the upper jaw, and shape of the upper jaw. It appears probable that the allopatric population represents the morphological state of R. ocellata before it became sympatric with R. erinacea; divergence in size, number of tooth rows, and shape of the upper jaw between the two species developed after establishment of sympatry. These divergences in character traits, related to feeding, reduced competition between the two sympatric species and permitted the present wide overlap in their ranges.Character displacement is evidently rare in demersal fishes inhabiting the flat and soft bottoms of the northwestern Atlantic because the three other pairs of sibling species that occur there are parapatrically distributed and thus would not compete for resources. Raja erinacea and R. ocellata may have been restrained from establishing parapatry by another species pair of skates (R. senta and R. radiata) which have a complementary distribution and similar feeding habits of R. erinacea and R. ocellata but which occur in deeper water.     

Description of egg capsules of Rasptail Skate Rostroraja velezi (Chondrichthyes: Rajiformes: Rajidae) from northern Peru

Environmental Biology of Fishes - Nine egg capsules of the Rasptail Skate (Rostroraja velezi) were collected from their southernmost distributional range in northern Peruvian waters for their...