Introduction 51Terminology 51Types of spawning omission 56Identifying spawning omission 57 External appearance of gonads 58 Gonad indices 59 Histology 59 Importance of sampling time 61 Causes of spawning omission 62 Non-annual spawning as an adaptive trait: trade-offs between reproduction and survival 64 Significance to fisheries science 66Abstract It is often assumed that iteroparous fishes spawn annually once reaching sexual maturity, but this is not always the case. This paper reviews available information on skipped spawning in female teleost fishes. All instances of non-annual spawning are described as one of three types (retaining, reabsorbing, resting), depending on where in the normal spawning cycle development has been interrupted. Retaining ripe eggs is caused by conditions experienced during the spawning season (fish density, mate availability, pollution), whereas failure to start vitellogenesis (resting) or the breakdown of all oocytes that enter into vitellogenesis (reabsorbing) is caused by factors experienced prior to the spawning season (primarily temperature and poor nutrition). It is speculated that the relative shortage of data on non-annual spawning may be because of difficulties in identifying non-reproductive individuals.In an attempt to rectify this situation, the criteria needed to identify females undergoing the three forms of spawning omission are presented in terms of external appearance of gonads, gonad indices, and histological analysis. The energy saved by not spawning in a poor year may lead to increased survival and the probability of spawning in subsequent years. As the cumulative number of progeny gained by surviving to spawn in multiple subsequent years outweighs the number of progeny lost by not spawning in a given single year, occasional omission of spawning may constitute an adaptive trait in long-lived iteroparous fishes.
The traditional view of iteroparity in fishes is one of an annual reproductive cycle that culminates each year in spawning. More recently, a more flexible view of fish reproduction has been adopted, including the potential for mature fish to skip spawning. Here, we review the abundance of recent research on skipped spawning, covering a broad range of fishes with diverse life history strategies. Evidence for skipped spawning has been collected by use of traditional histological techniques as well as modern technological advances, such as satellite tags and the ability to track fish movements based on elemental and isotope signatures. Skipped spawning is most commonly attributed to deficient diet and poor nutritional condition. Advances made in this field of study in recent years include descriptions of hormonal changes that precede and perhaps initiate skipped spawning, the development of life history models that incorporate the potential for skipped spawning, and estimates of the degree to which skipped spawning influences the reproductive potential of fish populations. In addition to summarizing this new research, we attempt to advance current knowledge by (1) providing the first review discussion of skipped spawning in males, (2) exploring skipped spawning in anadromous fishes by using the Atlantic salmon Salmo salar as an example, and (3) discussing the potential for and difficulties in identifying skipped spawning in species with indeterminate fecundity.
Atlantic cod Gadus morhua were collected from Smith Sound, Newfoundland in January 1999. Visual examination of females (n=150) and males (n=126) revealed that some large fish (42-79 cm) had underdeveloped gonads. Histological examination of underdeveloped ovaries indicated that the majority of these females were undergoing mass resorption of oocytes and would not have spawned in 1999. Fish in this condition included females that were aborting their first attempt at maturation and females that had spawned the previous year but were failing to re-ripen. Somatic and liver condition were significantly lower (P<0·05) for fish undergoing mass oocyte resorption than ripening females, suggesting that the interruption in the maturation cycle may have been related to insufficient nutrient storage. In males, testes of some adult fish were considered to be non-reproductive as they showed no signs of ripening and probably would not have spawned in 1999. Liver condition was significantly higher (P<0·05) for non-reproductive males than those that were ripening. Disruptions in male and female reproductive cycles may also have been related to water temperatures that were too cold (0-0·5 C) for successful gamete development. Immature gametes (perinucleolar oocytes in females; spermatogonia in males) showed no signs of breakdown in non-reproductive individuals, suggesting that they retained the potential to develop and spawn gametes in
Paternal effects on haddock Melanogrammus aeglefinus early life history traits were examined by crossing eggs and sperm in a nested design and analysing the progeny at 0, 5 and 10 days posthatch (dph). The proportion of the variance in early life history traits that was due to paternity was significant for hatching success, larval standard length, myotome height, jaw length and yolk size, but not eye diameter or yolk utilization efficiency. Some morphological traits were influenced more by paternity than maternity. The findings suggest that the importance of males in the early life history success of marine fishes be reconsidered. # 2004 The Fisheries Society of the British Isles
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