H. Murua, F. Saborido-Rey, Tomkiewicz, P. King and R. Rideout Female Reproductive Strategies of Marine Fish Species of the North Atlantic H. Murua, F. Saborido-Rey, Tomkiewicz, P. King and R. Rideout

INTRODUCTION Most of the North Atlantic marine fish resources are overexploited, outside safe biological limits, or even collapsed with weak or not signal of recovering. One of the basic goals of fisheries management is to conserve sufficient reproductive potential of a stock to allow for sustainable exploitation. To understand the reproductive potential of a stock, the reproductive strategy and ecology must be well understood; this will also define the sampling strategy. Histology is the best way to study many of the reproductive proccess (maturation, oocyte development, atresia and follicular degeneration).

INTRODUCTION Our aim is to classify the reproductive strategy of common commercially exploited fish species of the North Atlantic updating the contribution to the NAFO Working Group on Reproductive Potential (Murua and Saborido-Rey, 2003). We used the reproductive traits that differed most among species studied Breeding opportunity - Semelparous / Iteroparous Ovarian organization based on oocyte development Synchronous Group synchronous / Asynchronous development Fecundity type according to oocyte recruitment Determinate / Indeterminate Spawning pattern – Total spawners / Batch spawners Reproductive characteristics not considered: Gender system (Gonochoristic/hermaphroditic), mating system (promiscuous/polygamous), type of fertilization (external/internal), embryonic development (oviparity/viviparity), parental care (present or absent), spawning site preparation (yes or no). With regard to breeding opportunities: SEMELPAROUS - spawn only once in their life time and die shortly afterwards ITEROPAROUS - capable of producing offspring in successive annual or seasonal cycles

Ovarian organization General characteristics of teleost oogenesis Organization of developing oocytes in the ovary: - Synchronous - Group-synchronous - Asynchronous Reproductive cycle and maturation stages Source of discussion

Types of ovarian organization SYNCHRONUS OOCYTE DEVELOPMENT: All oocytes, once formed, grow and ovulate from the ovary in unison - replenishment of cohorts by proceeding ones does not take place during ripening and spawning No oocytes in primary growth stage OOCYTE DIAMETER PERCENTAGE Size frequency distribution of a hypothetical synchronous spawner

Types of ovarian organization GROUP SYNCHRONUS OOCYTE DEVELOPMENT: At least two populations of oocytes can be distinguished at the same time during ripening and spawning - a fairly synchronous population of larger oocytes (defined as a clutch) and a more heterogeneous population of smaller oocytes from which the clutch is recruited Oocytes in primary growth stage Hydrated oocytes PERCENTAGE OOCYTE DIAMETER Size frequency distribution of a hypothetical group-synchronous spawner

Types of ovarian organization ASYNCHRONUS OOCYTE DEVELOPMENT: Successive cohorts of oocytes in different stages of development can be distinguished in ovaries of ripening and spawning females Ripe and reripening females Spawning females with hydrated eggs PERCENTAGE OOCYTE DIAMETER Size frequency distribution of a hypothetical asynchronus spawner

Fecundity types DETERMINATE FECUNDITY: Potential annual fecundity is fixed prior the spawning period and after correcting for atretic losses, the total number of eggs spawned per female in a year is called the realised annual fecundity (Hunter et al., 1992). INDETERMINATE FECUNDITY: Potential annual fecundity is not fixed before the onset of spawning. In such species, previtellogenic oocytes can develop and be recruited into the yolked oocyte stcok at any time during the spawning season (de novo vitellogenesis) (Hunter and Goldberg, 1980).

Determinate fecundity and realised egg production RIPENING PRE-SPAWNING SPAWNING STAGES END OF SPAWNING RECRUITMENT VITELLOGENESIS MATURATION ATRESIA POTENTIAL FECUNDITY ATRESIA: should be highlighted that normally determinate fish species could be high during pre-sapwning and spawning in order to adjust realised fecundity from much higher potential fecundity. EGG PRODUCTION TOTAL REALISED FECUNDITY The total realised egg production corresponds to the potential fecundity corrected for atretic losses

Indeterminate fecundity and realised egg production RIPENING PRE-SPAWNING SPAWNING STAGES END OF SPAWNING RECRUITMENT VITELLOGENESIS MATURATION ATRESIA ATRESIA: should be highlighted that normally in indeterminate fish species is rather low in spawning fishes whereas is very high at the end of spawning season (resorption of remaining vitellogenic oocytes) SUCCESSIVE EGG PRODUCTION TOTAL REALISED FECUNDITY The total realised egg production corresponds to potential batch fecundity times number of batches corrected for atretic losses

Reproductive cycle and maturation stages Ripening or Re-ripening IMMATURE Spawning Active Partly spent Spent MATURE Recovering / Resting Skipped spawning Inactive

Mass atresia (previtellogenic)

Mass atresia (vitellogenic) 6 10 63% atretic oocytes

DETERMINATE FECUNDITY INDETERMINATE FECUNDITY CHARACTERISTIC INDETERMINATE FECUNDITY PRESENT PRESENCE OR ABSENCE OF A HIATUS BETWEEN YOLKED AN UNYOLKED OOCYTES IN THE OOCYTE SIZE FREQUENCY DISTRIBUTION IN OVARIES PASSING THROUGH DIFFERENT DEVELOPMENTAL PHASES IN THE MAIN SPAWNING SEASON ABSENT DECREASE EVOLUTION OF NUMBER OF VITELLOGENIC OOCYTES ALONG THE MAIN SPAWNING SEASON CONSTANT INCREASE EVOLUTION OF THE MEAN DIAMETER OF THE ADVANCED VITELLOGENIC OOCYTES IN THE STANDING STOCK ALONG THE SPAWNING SEASON DURING THE SPAWNING SEASON EVOLUTION OF THE LEVELS OF ATRESIA DURING SPAWNING SEASON AND THE END OF THE SPAWNING SEASON GENERALIZED AT THE END OF SPAWNING SEASON THE PERCENTAGE OF SMALL OOCYTES (CA, EARLY VITELLOGENIC) TRHOUGHOUT THE SPAWNING SEASON

Spawning Pattern TOTAL SPAWNERS: The recruited oocytes are ripened, hydrated and ovulated as a clutch and the eggs are spawned in a unique event or over a shorter period of time but as part of a single event BATCH SPAWNERS: Ripe oocytes which arise from successive cohorts of ripening oocytes (asynchronous development) or a pool of yolked oocytes (synchrounous or group-synchronous development) enter final maturation in clutches and are spawned as successive batches of hydrated eggs at several days intervals

Reproductive strategies Examples Spawning pattern Fecundity type Ovarian organization Breeding oportunity Total spawner Determinate Synchronous Semelparous Pacific salmons (Oncorhincus spp.) Capelin (Mallotus villosus) Lamprey (Petromyzontiformes) Eel (Anguilla anguilla)?? Total spawner Determinate Group synchronous Iteroparous Cod (Gadus morhua) Haddock (Melanogrammus aeglefinus) Saithe / Pollock (Pollachius virens) Whiting (Merlangus merlangus) Roughhead grenadier (Macrourus berglax) Roundnose grenadier (Coryphaenoides rupestris) Yellowtail flounder (Limanda ferruginea) Greenland halibut (Reinhardtius hippoglossoides) Atlantic halibut (Hippoglossus hippoglossus) American plaice (Hippoglossoides platessoides) Dab (Limanda limanda) Plaice (Pleuronectes platessa) Winter flounder (Pseudopleuronectes americanus) Turbot (Psetta maxima) Lemon sole (Microstomus kitt) Megrim (Lepidorhombus whiffiagonis) Bass (Dicentrarchus labrax) Redfishes (Sebastes spp.) Monkfishes (Lophius spp.) Atlantic Salmon (Salmo salar) Sea trout(Salmo trutta) Herring (Clupea harengus) Elasmobranchs Batch spawner Batch spawner Determinate Asynchronous Atlantic Mackerel (Scomber scombrus) Sole (Solea solea) Indeterminate Anchovies (Engraulis spp.) Sprat (Sprattus sprattus) European hake (Merluccius merluccius) Blue whiting (Micromesistius poutassou) Chub mackerel (Scomber japonicus) Horse mackerel (Trachurus trachurus) Yellowfin tuna (Thunnus albacares) Pilchard (Sardina pilchardus) Atlantic swordfish (Xiphias gladius)