Atresia of ovarian follicles in fishes, and implications and uses in aquaculture and fisheries

Corriero, Aldo; Zupa, Rosa; Mylonas, Constantinos C.; Passantino, Letizia

doi:10.1111/jfd.13469

Cited by 32 publications

(13 citation statements)

References 279 publications

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“…Rates of atresia during subsequent reproductive cycles may be similarly accounted for (e.g., during subsequent reproductive cycles 17%–67% of individuals expected to spawn may undergo ovarian follicular atresia). This will also ensure that the spawning stock biomass is not biased by the lack of inclusion of the rate of mass ovarian follicular atresia (see Corriero et al, 2021). If the rates of mass ovarian follicular atresia are high in subsequent reproductive cycles and are not incorporated into population models seeking to evaluate recovery or population viability (e.g., Nelson et al, 2021), the spawning stock biomass could be overestimated.…”

Section: Discussionmentioning

confidence: 99%

Reproductive indices and observations of mass ovarian follicular atresia in hatchery‐origin pallid sturgeon

et al. 2022

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The Pallid Sturgeon (Scaphirhynchus albus) Conservation Propagation and Stocking Program began stocking in the Missouri River above Fort Peck Reservoir in 1998 with 1997‐year‐class pallid sturgeon. Within the 1997‐year class, all hatchery‐origin pallid sturgeon females that reached reproductive maturation by 2016 underwent mass ovarian follicular atresia. Using combined historical and contemporary data, we described the spawning periodicity for female and male pallid sturgeon, characterized age‐ and size‐at‐first spawning, and evaluated what proportion of females experience mass ovarian follicular atresia during the first and subsequent reproductive cycles. Pallid sturgeon reached their first reproductive cycle at older ages and larger sizes than described for other populations. Females were functionally and physiologically capable of spawning at 21 years and males at 15 years. Immature pallid sturgeon as old as 20 years were documented. We found that more female pallid sturgeon underwent mass ovarian follicular atresia during the presumed‐first reproductive cycle or known‐first reproductive cycle than females during subsequent reproductive cycles (62.5% compared to 33.3%) indicating that effects related to reproductive maturation may be occurring. Nonetheless, mass ovarian follicular atresia appears to also occur for reasons not related to reproductive maturation. Females had biennial reproductive cycles, and males had annual and biennial reproductive cycles. Population models should account for females undergoing mass ovarian follicular atresia in their first reproductive cycle and subsequent cycles thereby increasing the age at first‐successful spawning and reducing the estimated size of the spawning stock.

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Section: Discussionmentioning

confidence: 99%

Reproductive indices and observations of mass ovarian follicular atresia in hatchery‐origin pallid sturgeon

et al. 2022

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“…Follicular atresia—a degenerative process in oocytes (Valdebenito et al 2011)—plays a key role in the determination of fecundity (Bromage and Cumaranatunga 1988; Tyler and Sumpter 1996; Lubzens et al 2010; Corriero et al 2021). Rainbow Trout are “capital breeders” (Wootton and Smith 2015) and provision offspring by using energy stores accumulated at an earlier time, with 10–30% of the vitellogenic ovarian follicles in the ovary of a female undergoing atresia at any one time (Bromage and Cumaranatunga 1988).…”

Section: Discussionmentioning

confidence: 99%

“…The developing phase is a period of gonad growth prior to entry into the spawning capable phase, when gamete development advances enough such that spawning may occur. For females, partial follicular atresia—the resorption of ovarian follicles—can occur during the developing phase and can be an important determinant of fecundity (Bromage and Cumaranatunga 1988; Bromage et al 1992; Grier et al 2007; Corriero et al 2021). Once fish become spawning capable, outcomes are to (1) successfully undergo oocyte maturation, ovulation, and oviposition; or (2) undergo mass follicular atresia (Figure 1).…”

Section: Methodsmentioning

confidence: 99%

“…An understanding of reproductive dynamics is critical for successful fisheries management (Morgan 2008; Kjesbu 2009; Marshall 2009; Corriero et al 2021) and is commonly integrated into management of harvest fisheries for which information on the reproductive potential (e.g., fecundity) or sex ratios is readily available (Hutchings 2009; Lowerre‐Barbieri et al 2016). However, for populations that support recreational fisheries or that are threatened or endangered, information on reproductive biology can be challenging to obtain.…”

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confidence: 99%

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Population Reproductive Structure of Rainbow Trout Determined by Histology and Advancing Methods to Assign Sex and Assess Spawning Capability

Crossman

Webb

Korman³

et al. 2022

Trans Am Fish Soc

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Rainbow Trout Oncorhynchus mykiss have been intensively studied and gametogenesis has been described, but the use of reproductive indices in field studies has not been widely applied when assessing variability in growth or recruitment dynamics. We integrated descriptions for gametogenesis within the framework of standardized terminology for reproductive development in teleosts to develop sex‐specific criteria for assignment of reproductive phases. We used these descriptions and histological analysis of gonad tissue collected from Rainbow Trout in the Colorado River downstream from Glen Canyon Dam to quantify season‐, size‐, and sex‐specific variation in population reproductive structure. The accuracy of nonlethal methods (manual expression and ultrasonography) was evaluated for assigning sex by comparing estimates with those determined by histology. Rainbow Trout were sampled through an annual spawning cycle from October 2018 to April 2019. Spawning capable males were available across the entire period, with a higher proportion earlier in the season compared to later. Females were spawning capable in October, with a peak in February; by April, they were in the early developing phase, indicating that spawning had ended. Elevated levels of atresia (19% for fall spawners) and evidence for delayed maturation were identified, suggesting energetic limitations on the reproductive potential of the population. For both sexes, the probability of being spawning capable increased with fork length, with minimum sizes of ≥283 mm for females and ≥187 mm for males. Sex assignment using ultrasonography was more accurate (46%) than manual expression of gametes (9%), as only a small proportion of males and females expressed gametes. Probabilities of correct sex assignment using ultrasonography were strongly influenced by reproductive phase, with spawning capable fish (females: 100%; males: 77%) having significantly higher probabilities of correct sex assignment compared to immature fish. Furthermore, probabilities of correct sex assignment increased with fish size and were higher for females than for males. Results provide a framework for quantifying spawning capability and population reproductive structure in ongoing research to better understand the drivers of recruitment variability in aquatic ecosystems.

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“…Abortive maturation, the interruption of maturation often attributed to unfavorable environmental factors that would lead to unsuccessful spawning, has been documented in fish (e.g., Conrath, 2017). Subsequent to the cessation of maturation, the nutrients and cellular components of the developing gametes are mobilized and resorbed through a mass atresia process (Corriero et al, 2021). While follicular atresia is documented in cheloniids (Miller and Limpus, 2003), it remains unknown whether sea turtles might undergo abortive maturation, as do fish.…”

Section: Research Needsmentioning

confidence: 99%

A morphologist, a modeler, and an endocrinologist consider sea turtle sex ratios in a changing climate. Some wine was involved

Heppell

Wyneken²,

Heppell³

2022

Front. Ecol. Evol.

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Because the sex of sea turtles is determined by temperature during embryonic development, many populations are vulnerable to increased bias in primary sex ratios as global temperatures rise. Higher temperatures produce more females, and some populations are already showing years with all-female offspring production. But because sea turtles take decades to mature and have long adult lifespans, these primary sex ratio biases can take years to impact adult sex ratios, and the males from cohorts that are produced during cooler years may compensate for the sex ratio bias if they can breed more frequently and with multiple females. To date, little is known about male sea turtle reproductive behavior, making predictions of sex ratio skew impacts highly speculative. We used data from southern Florida loggerhead sea turtle nests to parameterize a simple population model to explore the effects of an increase in the proportion of female hatchlings over time on population trends, effective population size (Ne), and quasi-extinction probability. We also tested the effects of increasing the frequency of relatively high male production years to simulate potential mitigation strategies. While heuristic rather than predictive, our results expectedly show a rise in nest counts due to the increase in females over time, followed by population decline as males become limiting. Population collapse due to increased female bias will take many decades to occur, but sex ratio skew can have large impacts on Ne, and thus increase the potential for inbreeding. An increase in the frequency of male production years, even just one additional “good male year” per decade, can help mitigate these outcomes if the rate of feminization is not too rapid. Male breeding frequency and mating success are critical drivers of the results and must be prioritized for research.

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Atresia of ovarian follicles in fishes, and implications and uses in aquaculture and fisheries

Cited by 32 publications

References 279 publications

Reproductive indices and observations of mass ovarian follicular atresia in hatchery‐origin pallid sturgeon

Reproductive indices and observations of mass ovarian follicular atresia in hatchery‐origin pallid sturgeon

Population Reproductive Structure of Rainbow Trout Determined by Histology and Advancing Methods to Assign Sex and Assess Spawning Capability

A morphologist, a modeler, and an endocrinologist consider sea turtle sex ratios in a changing climate. Some wine was involved

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