Bárbara Serra-Pereira

Molecular markers reveal spatially segregated cryptic species in a critically endangered fish, the common skate (Dipturus batis).

Many sharks and skates are particularly vulnerable to overfishing because of their large size, slow growth, late maturity and low fecundity. In Europe dramatic population declines have taken place in common skate (Dipturus batis L.), one of the largest demersal fish in regional shelf seas, leading to extirpations from substantial parts of its former range. Here we report the discovery of cryptic species in common skate collected from the northeast Atlantic continental shelf. Data from nuclear microsatellite markers indicated two clearly distinct clades and phylogenetic analysis of mitochondrial DNA sequences demonstrated monophyly of each one of them. Capture locations showed evidence of strong spatial segregation, with one taxon occurring mainly in waters off the southern British Isles and around Rockall, while the other was restricted to more northerly shelf waters. These apparently cryptic species showed overlapping substrate and depth preferences, but distributional limits were closely related to temperature gradients, potentially indicating thermal limits to their distributions. This discovery of hidden diversity within a large, critically endangered marine vertebrate demonstrates how marine biodiversity can be underestimated, even in such a relatively well-studied and heavily exploited region.

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.

The use of caudal thorns for ageing Raja undulata from the Portuguese continental shelf, with comments on its reproductive cycle

The present study focuses on age estimation, with reproductive information contributing to the better understanding of the growth and the biology of Raja undulata. In the age and growth study, two calcified structures were used: caudal thorns and central vertebra. Results of readings showed that there were no significant differences in age estimates between the two structures. Both von Bertalanffy and Gompertz growth models were fitted to size-at-age data by sex and geographical area. No significant differences were found between sexes for the two models but significant differences were found between geographical areas (P = 0.05). The Gompertz growth function was selected as the best model to describe R. undulata growth because it presented the best fit and the most reasonable biological estimates. Reproductive analysis indicates one annual breeding season for R. undulata. The differences found in the estimates of length at first maturity between geographical areas (TL50% = 838 mm in Peniche and 762 mm in Algarve for females and TL50% = 781 mm in Peniche and 736 mm in Algarve for males), together with the regional differences found between growth parameters estimates (P = 0.05), may reflect the existence of different local populations of R. undulata on the Portuguese continental shelf.

The development of the oviducal gland in the Rajid thornback ray, Raja clavata

The reproductive processes of chondrichthyans are complex. Knowledge of the development and maturation of the oviducal gland is vital for understanding the reproductive biology of a species. This study represents the first contribution of this subject for skates. In the oviparous thornback ray, Raja clavata, oviducal gland development begins early in the developing stage with the formation of gland tubules and the distinct lamellae of each zone: club, papillary, baffle and terminal. Oviducal development is complete by the end of the developing stage when the storage and secretion of products is evident within the gland tubules of each zone. Periodic acid-Schiff and alcian blue histological staining showed that the secretory mucous cells of the club and papillary zones produce neutral and sulfated acid mucins. The last row of gland tubules of the papillary zone stains intensely for sulfated acid mucins. The baffle zone, which is responsible for the production of the egg capsule, represented 60–80% of the glandular zone of the oviducal gland. Sperm bundles were observed in the deeper recesses of the baffle zone during the maturation process, and during capsule extrusion, sperm were detected near the lumen. The terminal zone was composed of two types of gland tubules: serous (producing protein fibres) and mucous glands (producing sulfated acid mucins).

Maturation of the Gonads and Reproductive Tracts of the Thornback Ray Raja clavata, with Comments on the Development of a Standardized Reproductive Terminology for Oviparous Elasmobranchs

Abstract There is a need for a unified terminology to describe reproductive phase assignment across fish taxa, regardless of the reproductive strategy involved. Reproductive terminology already adopted for teleosts has been applied to oviparous elasmobranchs of both sexes. A historical review of the terminologies used by previous authors and how these correspond to the new terminology is presented. Five reproductive phases are considered: immature, developing, spawning capable (which includes an actively spawning subphase), regressing, and regenerating. By using an oviparous elasmobranch, the thornback ray Raja clavata, as an example, the different phases are described based on both macroscopic and microscopic features of the reproductive tract, including the ovaries, oviducal glands, and uterus in females and the testes, claspers, and sperm ducts in males. The regressing phase was observed in females, but the regenerating phase was not; neither of these two phases was observed in males. Records from other species suggest that all five reproductive phases can be found in oviparous elasmobranchs, depending on the reproductive strategy of the species.

A tale of two seas: contrasting patterns of population structure in the small-spotted catshark across Europe

Elasmobranchs represent important components of marine ecosystems, but they can be vulnerable to overexploitation. This has driven investigations into the population genetic structure of large-bodied pelagic sharks, but relatively little is known of population structure in smaller demersal taxa, which are perhaps more representative of the biodiversity of the group. This study explores spatial population genetic structure of the small-spotted catshark (Scyliorhinus canicula), across European seas. The results show significant genetic differences among most of the Mediterranean sample collections, but no significant structure among Atlantic shelf areas. The data suggest the Mediterranean populations are likely to have persisted in a stable and structured environment during Pleistocene sea-level changes. Conversely, the Northeast Atlantic populations would have experienced major changes in habitat availability during glacial cycles, driving patterns of population reduction and expansion. The data also provide evidence of male-biased dispersal and female philopatry over large spatial scales, implying complex sex-determined differences in the behaviour of elasmobranchs. On the basis of this evidence, we suggest that patterns of connectivity are determined by trends of past habitat stability that provides opportunity for local adaptation in species exhibiting philopatric behaviour, implying that resilience of populations to fisheries and other stressors may differ across the range of species.

Resolving taxonomic uncertainty in vulnerable elasmobranchs: are the Madeira skate (Raja maderensis) and the thornback ray (Raja clavata) distinct species?

Skates and rays constitute the most speciose group of chondrichthyan fishes, yet are characterised by remarkable levels of morphological and ecological conservatism. They can be challenging to identify, which makes monitoring species compositions for fisheries management purposes problematic. Owing to their slow growth and low fecundity, skates are vulnerable to exploitation and species exhibiting endemism or limited ranges are considered to be the most at risk. The Madeira skate Raja maderensis is endemic and classified as ‘Data Deficient’ by the IUCN, yet its taxonomic distinctiveness from the morphologically similar and more wide-ranging thornback ray Raja clavata is unresolved. This study evaluated the sequence divergence of both the variable control region and cytochrome oxidase I ‘DNA barcode’ gene of the mitochondrial genome to elucidate the genetic differentiation of specimens identified as R. maderensis and R. clavata collected across much of their geographic ranges. Genetic evidence was insufficient to support the different species designations. However regardless of putative species identification, individuals occupying waters around the Azores and North African Seamounts represent an evolutionarily significant unit worthy of special consideration for conservation management.

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.

How is the morphology of the oviducal gland and of the resulting egg capsule associated with the egg laying habitats of Rajidae species

Egg capsules of Rajidae species vary in size, shape and adornments. These differences can be used as a taxonomic tool to differentiate species. Furthermore, since egg capsule external morphology is adapted to the environment where they are laid, it can be used make inferences on egg-laying grounds. In the present study, oviducal glands and egg capsules of seven species of skates (Leucoraja naevus, Raja brachyura, Raja montagui, Raja microocellata, Raja miraletus, Raja clavata and Raja undulata) are described and compared, and a taxonomic key developed. The resulting taxonomic key constitute a useful tool to identify skate species inhabiting Portuguese continental waters and, therefore, to improve our knowledge of egg laying habitatsproviding useful information for conservation and management.

Reproductive biology of cuckoo ray Leucoraja naevus

The present study is the first to provide data on the reproductive biology of cuckoo ray Leucoraja naevus in Portuguese continental waters. No difference in size at maturity was detected between sexes, which was estimated as 56 cm total length. Spawning occurs all year round, but maximum activity was during winter months. Maximum fecundity is c. 63 eggs female(-1) year(-1). Encapsulated eggs are released in batches, nine in total with a mean number of seven extruded eggs in each batch.