Reproductive life history of sablefish (Anoplopoma fimbria) from the U.S. Washington coast

Abstract

Sablefish (Anoplopoma fimbria) is a marine groundfish that supports valuable fisheries in the North Pacific Ocean and holds promise for marine aquaculture. Limited information is available, however, about its reproductive biology. This study aimed to characterize the complete reproductive cycle, including seasonal changes in gonadal development (macroscopic and histological), plasma sex steroid levels (17β-estradiol -E2-, and 11-ketotestosterone -11KT-), gonadosomatic and hepatosomatic indices (GSI, and HSI), and condition factor (K) of female and male sablefish captured off the Washington coast. Adult fish (209 females, 159 males) were caught by longline monthly from August 2012 to August 2013. Early signs of recruitment of ovarian follicles into secondary growth, indicated by oocytes containing small yolk granules and cortical alveoli, were first observed in March. Oogenesis progressed during spring and summer, and fully vitellogenic follicles were first observed in July. Vitellogenic growth was correlated with increases in plasma E2, GSI, HSI and K. Periovulatory females, indicated by fully-grown oocytes with migrating germinal vesicles and hydrated oocytes, were found from November to February. At this stage, plasma E2 and GSI reached maximal levels. In males, proliferating cysts containing spermatocytes were first observed in April. Testicular development proceeded during spring and summer, a period during which all types of male germ cells were found. The first clusters of spermatozoa appeared in July, concomitant with a 5.2-fold increase in GSI. Spermiating males were observed from November to April; at this time, spermatids were absent or greatly reduced, and testis lobules were filled with spermatozoa. The highest levels of plasma 11KT were found in males at this stage. Postspawning ovaries and testes, and basal steroids levels were found in fish captured from February to April. These results suggest that sablefish in coastal Washington initiate their reproductive cycle in March/April and spawn primarily in January/February.

Fig 1. Map of deep and shallow longline sampling sites off the Washington coast over the Quinault Canyon.

Sampling was performed 40–50 miles northwest of Gray's Harbor, Westport (WA). See S1 Table for exact details of longline depth and location.

Fig 2. Monthly fork length, body weight and age of sablefish collected off the Washington coast.

Fork length (A), body weight (B) and age (C) of female (empty circles) and male (black circles) sablefish. Data are expressed as the mean ± SD. Means not sharing the same letters are significantly different (p<0.05). Male sablefish collected in June were not included in any post-hoc comparisons due to small sample size (n = 2). Asterisks (*) indicate significant differences between males and females within a given month (two-way ANOVA, p<0.05)

Fig 3. Representative photographs of the external appearance and histological sections of sablefish ovaries at onset of secondary growth, early and mid vitellogenic stages.

Onset of secondary growth (A), early vitellogenesis (B) and mid vitellogenesis (C). Detail of an ovarian follicle transitioning to secondary growth is shown in A.1. Abbreviations: yg, yolk granule, ca, cortical alveoli; nu, nucleolus; epn, early perinucleolus follicle; lpn, late perinucleolus follicle; evit, early vitellogenic follicle; fvit, fully vitellogenic follicle. Gonad orientation is anterior portion to the left, posterior to the right. Bars indicate 4 cm in left panels and 500 μm in right panels.

Fig 4. Representative photographs of the external appearance and histological sections of sablefish ovaries at late vitellogenic, periovulatory and postspawning stages.

Late vitellogenesis (A), periovulatory (B) and postspawning (C). Abbreviations: epn, early perinucleolus follicle; lpn, late perinucleolus follicle; fvit, fully vitellogenic follicle; gvm, germinal vesicle migration; ygf, yolk granule fusion; pof, postovulatory follicle. Gonad orientation is anterior portion to the left, posterior to the right. Bars indicate 4 cm in left panels and 500 μm in right panels.

Fig 5. Follicle size-frequency distribution histograms representative of each stage of ovarian development in sablefish.

Ovaries at onset of secondary growth (A), early vitellogenesis (B), mid vitellogenesis (C), late vitellogenesis (D), periovulatory (E) and postspawning (F) are shown. A total of 597, 743, 625, 491, 384, 204 and 559 cross-sectioned follicles were measured at these specific stages, respectively. To facilitate the visualization of the results, follicle size-frequency histograms are divided into four categories: perinucleolar, which includes follicles at the late perinucleolus stage (80–160 μm); early developing, which includes follicles at the onset of secondary growth and early vitellogenesis as they typically overlap in size (160–340 μm); fully vitellogenic, which includes follicles with their cytoplasm completely filled with yolk and lipid globules (340–610 μm); and maturing, which includes follicles showing signs of germinal vesicle migration and yolk globule fusion (610–760 μm).

Fig 6. Monthly proportion of female sablefish at specific reproductive stages and their gonadosomatic index, hepatosomatic index, condition factor and plasma 17β-estradiol levels.

Proportion of female sablefish at specific reproductive stages (A), gonadosomatic index (B), hepatosomatic index (C), condition factor (D) and plasma 17β-estradiol levels (E). In A, the number of females sampled at each month is indicated in parentheses. In B-E, females were divided into specific stages of ovarian development within a month. In B-E, data are represented by box and whisker plots in which the box extends from the 25th to 75th percentile and the line within the box indicates the median; whiskers are determined by the largest and the smallest values. To improve visualization of lower values, plasma levels of 17β-estradiol are shown in a log10-based scale.

Fig 7. Comparison of gonadosomatic index, hepatosomatic index, condition factor and plasma 17β-estradiol at specific stages of ovarian development in sablefish.

Gonadosomatic index (A), hepatosomatic index (B), condition factor (C) and plasma 17β-estradiol (D). The stages of ovarian development include onset of the secondary growth, OSG; early vitellogenesis, EV; mid vitellogenesis, MV; late vitellogenesis, LV; periovulatory, PO; postspawning, PS. Data are represented by box and whisker plots in which the box extends from the 25th to 75th percentile and the line within the box indicates the median; whiskers extend from the 5th to 95th percentile. Shared letters indicate statistical similarities (ANOVA on ranks, p<0.05).

Fig 8. Representative photographs of the external appearance and histological sections of sablefish testes at early, mid and late recrudescence stages.

Early recrudescence (A), mid recrudescence (B) and late recrudescence (C). Detail of cyst containing secondary spermatocytes is shown in A.1. Abbreviations: spg, spermatogonia; spcI, primary spermatocyte; spcII, secondary spermatocyte; spd, spermatid; spz, spermatozoa. Gonad orientation is anterior portion to the left, posterior to the right. Bars indicate 4 cm in left panels and 100 μm in right panels.

Fig 9. Representative photographs of the external appearance and histological sections of sablefish testes at spermiating and postspawning stages.

Spermiating (A) and postspawning (B). Abbreviations: spz, spermatozoa; re-spz, residual spermatozoa. Gonad orientation is anterior portion to the left, posterior to the right. Bars indicate 4 cm in left panels and 100 μm in right panels.

Fig 10. Monthly proportion of male sablefish at specific reproductive stages and their gonadosomatic index, hepatosomatic index, condition factor and 11-ketotestosterone levels.

Proportion of male sablefish at specific reproductive stages (A), gonadosomatic index (B), hepatosomatic index (C), condition factor (D) and 11-ketotestosterone levels (E). In A, the number of males sampled at each month is indicated in parentheses. In B-E, males were divided into specific stages of testicular development within a month. In B-E, data are represented by box and whisker plots in which the box extends from the 25th to 75th percentile and the line within the box indicates the median; whiskers are determined by the largest and the smallest values. In order to improve visualization of lower values, plasma levels of 11-ketotestosterone are shown in a log10-based scale.

Fig 11. Comparison of gonadosomatic index, hepatosomatic index, condition factor and plasma 11-ketotestosterone at specific stages of testicular development in male sablefish.

Gonadosomatic index (A), hepatosomatic index (B), condition factor (C) and plasma 11-ketotestosterone (D). Stages of testicular development include early recrudescence, ER; mid recrudescence, MR; late recrudescence, LR; spermiating, S; postspawning, PS. Data are represented by box and whisker plots in which the box extends from the 25th to 75th percentile and the line within the box indicates the median; whiskers extend from the 5th to 95th percentile. Shared letters indicate statistical similarities (ANOVA on ranks, p<0.05).