Fran Saborido-Rey

A Standardized Terminology for Describing Reproductive Development in Fishes

Abstract As the number of fish reproduction studies has proliferated, so has the number of gonadal classification schemes and terms. This has made it difficult for both scientists and resource managers to communicate and for comparisons to be made among studies. We propose the adoption of a simple, universal terminology for the phases in the reproductive cycle, which can be applied to all male and female elasmobranch and teleost fishes. These phases were chosen because they define key milestones in the reproductive cycle; the phases include immature, developing, spawning capable, regressing, and regenerating. Although the temporal sequence of events during gamete development in each phase may vary among species, each phase has specific histological and physiological markers and is conceptually universal. The immature phase can occur only once. The developing phase signals entry into the gonadotropin-dependent stage of oogenesis and spermatogenesis and ultimately results in gonadal growth. The spawning capable phase includes (1) those fish with gamete development that is sufficiently advanced to allow for spawning within the current reproductive cycle and (2) batch-spawning females that show signs of previous spawns (i.e., postovulatory follicle complex) and that are also capable of additional spawns during the current cycle. Within the spawning capable phase, an actively spawning subphase is defined that corresponds to hydration and ovulation in females and spermiation in males. The regressing phase indicates completion of the reproductive cycle and, for many fish, completion of the spawning season. Fish in the regenerating phase are sexually mature but reproductively inactive. Species-specific histological criteria or classes can be incorporated within each of the universal phases, allowing for more specific divisions (subphases) while preserving the overall reproductive terminology for comparative purposes. This terminology can easily be modified for fishes with alternate reproductive strategies, such as hermaphrodites (addition of a transition phase) and livebearers (addition of a gestation phase).

Reproductive timing in marine fishes: variability, temporal scales, and methods

Abstract Reproductive timing can be defined as the temporal pattern of reproduction over a lifetime. Although reproductive timing is highly variable in marine fishes, certain traits are universal, including sexual maturity, undergoing one or more reproductive cycles, participating in one or more spawning events within a reproductive cycle, release of eggs or offspring, aging, and death. These traits commonly occur at four temporal scales: lifetime, annual, intraseasonal, and diel. It has long been known that reproductive timing affects reproductive success, especially in terms of the onset of sexual maturity and the match or mismatch between seasonal spawning and offspring survival. However, a comprehensive understanding of variability in reproductive timing over species, populations, and temporal scales is lacking. In addition, there is a need to assess how variability in reproductive timing affects a populations resilience. Because natural selection occurs at the individual level, this necessitates an understanding of within-population (i.e., individual) variability in reproductive timing and how fishing may impact it through age truncation and size-specific selectivity or fisheries-induced evolution. In this paper, we review the temporal aspects of reproductive strategies and the four most-studied reproductive timing characteristics in fishes: sexual maturity, spawning seasonality, spawning frequency, and diel periodicity. For each characteristic, we synthesize how it has traditionally been measured, advances in understanding the underlying physiology, its role in equilibriumbased fish population dynamics, and its importance to reproductive success. We then provide a review of emerging methodology—with an emphasis on ovarian histology—to improve our ability to assess variability in reproductive timing both among populations and within populations.

Emerging issues and methodological advances in fisheries reproductive biology

Abstract Although incorporating detailed reproductive data into all stock assessments is not a practical goal, the need to understand how reproductive biology affects population productivity is being increasingly recognized. More research focused on reproductive biology—coupled with a shift towards a resilience perspective in fisheries science—is resulting in challenges to many long-held assumptions; the emergence of important new issues; and identification of the need to improve data and methods used in reproductive studies. Typically, data for reproductive studies are based on an assessment of gonadal development, which is most accurately evaluated with histology. This special section of Marine and Coastal Fisheries contains contributions from a workshop on the gonadal histology of fishes that was held in Cadiz, Spain, during June 2009. These papers cover a wide range of species and reproductive topics while introducing improved and new histological techniques. In this introduction, we address the following needs: (1) to employ standardization, thereby improving our ability to conduct comparative studies; (2) to better understand patterns of gonadal development and spawning events over time; and (3) to move beyond the spawning stock biomass paradigm. We identify the contributions of special section papers to these topics and conclude by suggesting needs for future research and integration of reproductive data into both conceptual and quantitative models to better understand how reproductive performance affects population dynamics.

Digestive enzymes in marine species. II. Amylase activities in gut from seabream (Sparus aurata), turbot (Scophthalmus maximus) and redfish (Sebastes mentella)

Abstract The amylase activity of the digestive tract of three carnivorous fish species (Sparus aurata, Scophthalmus maximus and Sebastes mentella) has been studied. The activity of seabream and turbot showed its maximum at neutral pH (7.0–7.5); meanwhile, the activity of redfish had an optimum pH at 4.5-5.0. The t° function ranged between 35 and 45°C for the three species. The Arrhenius plots of the intestinal activities of seabream and turbot showed breakpoints at temperatures close to those of their physiological activities. High saline concentrations inhibited the activity of seabream and turbot and activated the activity of redfish. Seabream activity was absolutely dependent on calcium ions. On the contrary, redfish activity was only detected in the absence of this metal. Studies carried out by using several effectors suggested that the activities found in these three species are different. Considering our results from a point of view of the environmental conditions of these species, it might be concluded that enzymatic digestion of dietary carbohydrates proceeds at very low rate. Physiological implications are discussed.

The use of Histological Techniques to Study the Reproductive Biology of the Hermaphroditic Mediterranean Fishes Coris julis, Serranus scriba, and Diplodus annularis

Abstract The usefulness and importance of histological techniques in reproductive studies have been widely discussed for gonochoristic fish species. In the case of hermaphroditic fishes, histology is a particularly important tool for the proper identification of sexual pattern (i.e., sequential, simultaneous, or nonfunctional hermaphroditism). We used a histological approach to describe hermaphroditism, dynamics of follicle development, and spawning patterns in three species from the northwestern Mediterranean Sea (Balearic Islands, Spain): the Mediterranean rainbow wrasse Coris julis (sequential hermaphrodite), painted comber Serranus scriba (simultaneous hermaphrodite), and annular sea bream Diplodus annularis (nonfunctional hermaphrodite). Development of secondary growth follicles was asynchronous in all three species, and similar peaks in spawning activity occurred between May and July. However, notable differences in sexual cycle and egg production were found. For the painted comber, hydrated follicles were present in ovarian tissue almost every day during the peak of the spawning season, suggesting daily spawning and increasing the chances of autofertilization unless a mechanism to avoid this action is present in this species. Intersexual Mediterranean rainbow wrasses were identified, and the size and age at sex change were estimated to be 132 mm total length and 4 years, respectively. Previous investigators have concluded that the annular sea bream is a protandric hermaphrodite, but our results indicate nonfunctional hermaphroditism. These three species are of little commercial interest and are considered to be bycatch by the artisanal fleet, but they are vulnerable to the impacts of some recreational angling activities. Currently, no specific management plan has been developed for these species. We address the importance of describing sexual pattern and its implications for future conservation efforts.

Endocrine alteration and other biochemical responses in juvenile turbot exposed to the Prestige fuel oil

Juvenile turbot (Scophthalmus maximus) were exposed to different concentrations of the Prestige fuel oil through the diet. The effects on hepatic biotransformation enzymes, namely, 7-ethoxyresorufin O-deethylase (EROD), catalase, and phase II activities - UDP-glucuronosyltransferases (UGT) and cytosolic sulfotransferases (SULT) -, were monitored after 42-day exposure. Additionally, potential alterations on the endocrine system of juvenile turbot were assessed by measuring circulating levels of testosterone and 17beta-estradiol in plasma, together with gonadal P450 aromatase activity and the glucuronidation of testosterone by liver microsomal fractions. Fluorescent aromatic compounds (FACs) in bile were determined as an indicator of exposure to polycyclic aromatic hydrocarbons (PAHs). EROD activity increased in a dose dependent manner, and a positive correlation between levels of FACs in bile and EROD activity was observed. A significant increase in UGT activity was observed in fish exposed to medium and high fuel doses, whereas SULT cytosolic activity was not responsive to exposure. Exposure to the Prestige fuel oil sharply reduced circulating levels of testosterone in plasma. The obtained results suggest the ability of the Prestige fuel oil to alter hepatic biotransformation enzymes and to disrupt endogenous hormone levels in juvenile turbot, with unknown consequences in terms of sexual differentiation and reproduction.

Comparison of demographic and direct methods to calculate probabilistic maturation reaction norms for Flemish Cap cod (Gadus morhua)

Age and length at maturation have declined in many fish populations and this has been hypothesized to be a genetic change caused by high fishing mortality. Probabilistic Maturation Reaction Norms (PMRNs) have been used as a tool to gain a better understanding of the possible genetic nature of these changes. The demographic and direct methods are two ways to calculate PMRNs. The data requirements are more often met for the demographic method than for the direct method which requires the identification of recruit spawners. However, the demographic method relies on more assumptions than the direct method, typically assuming equality of growth and mortality rates for immature and mature individuals within an age class. This study provides the first direct comparison of demographic and direct methods and shows that both methods produce comparable results. Differences between methods are hypothesized to be owed to possible differences in growth rate between mature and immature individuals in Flemish Cap cod.

Female reproductive biology of the bluemouth Helicolenus dactylopterus dactylopterus: spawning and fecundity

The bluemouth Helicolenus dactylopterus dactylopterus is a zygoparous species that spawns multiple batches of embryos enclosed within a gelatinous matrix. Oocyte development is asynchronous, and the recruitment of secondary growth oocytes occurs continuously during the developing phase, but stops before the start of the first spawning (i.e. fecundity is determinate). The number of developing oocytes can be estimated as a function of the total length of the fish, its ovary mass and its gonado-somatic index. Only at the onset of spawning, when potential fecundity is determined, does condition also have a significant effect. The low levels of atresia detected during most of the spawning season show that this mechanism does not substantially affect the process. There is variability both in the spawning interval (with a mean of 2 days) and in the number of embryos comprising every single batch (up to 37,000). Expected effect of fisheries on the reproductive traits of this deep-sea species is also discussed.

Review of the population structure and ecology of S. mentella in the Irminger sea and adjacent waters

Significant controversies exist over the three types of Sebastes mentella found in the Irminger Sea and adjacent waters. Preliminary genetic studies have given evidence for the existence of three distinct groups, characterized using several molecular genetic markers. The biological or ecological significance of these between-group differences has, however, not been evaluated. In the present paper, we review the life cycle of S. mentella in this area, based on published data. Spawning of S. mentella in the Irminger Sea takes place in a single area above Reykjanes Ridge. The larvae drift towards East Greenland from where they are carried to West Greenland (NAFO Subareas 0+1). Later they return to East Greenland where the main nursery area has been identified. There is evidence for a migration of juvenile fish from the nursery area into the open Irminger Sea, where many different cohorts spawn. We also compare these ecological data with the genetic results and we conclude that the observed genetic differences can be derived from possible genetic drift, selection or mostly from temporal variation (age dependency). which has also been reported for other species with as high longevity as S. mentella. We conclude that S. mentella in the Irminger Sea and adjacent waters comprises one single population.

Ontogenetic allometry of the bluemouth, Helicolenus dactylopterus dactylopterus (Teleostei: Scorpaenidae), in the Northeast Atlantic and Mediterranean based on geometric morphometrics

The bluemouth, Helicolenus dactylopterus, is a deep-sea scorpionfish widely distributed in the Atlantic Ocean and the Mediterranean. It is a common by-catch associated to many demersal fisheries. However, there is little information about the stock structure, stock dynamics and life history parameters of the bluemouth. From the perspective of stock identification, it is important to study growth in fish populations to better understand the possible morphological differences among populations and when and why do they arise. Thus, the aim of this study was to determine the growth (allometric) trajectories of shape for several bluemouth populations in Northeast Atlantic and Mediterranean using landmark-based geometric morphometric techniques. In this study, ontogenetic allometry was present in all of the bluemouth samples. Ontogenetic shape changes were most evident in the head and pectoral area, affecting the position of the snout, preopercular spines and pectoral fins, but changes in body depth and length were also important. However, the degree to which these ontogenetic shape changes were present in bluemouth from each of the studied areas was different, indicating that their growth trajectories are not homogeneous. The importance of this finding for size-correction of the shape variables in morphometric studies for stock identification is also discussed.