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. 2018 May;6(9):e13640.
doi: 10.14814/phy2.13640.

Ultrasound as a Noninvasive Tool for Monitoring Reproductive Physiology in Female Atlantic Salmon (Salmo Salar)

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Free PMC article

Ultrasound as a Noninvasive Tool for Monitoring Reproductive Physiology in Female Atlantic Salmon (Salmo Salar)

Ingun Naeve et al. Physiol Rep. .
Free PMC article

Abstract

Aiming to explore ultrasound technology as a noninvasive method for maturation monitoring, we compared ultrasound observations and measurements in female Atlantic salmon (Salmo salar) during the last year before ovulation with standard, invasive methods such as gonadosomatic index (GSI), gonad histology and sex hormone analysis. Ultrasound measurements of ovaries correlated strongly (R > 0.9, P < 0.01) with ovary weight and GSI, and could be used as a noninvasive tool for GSI estimation. Using ultrasound, we were able to identify females with advanced oocyte development and elevated sex hormone and GSI levels earlier than previously observed. Histological studies confirmed these observations showing oocyte yolk accumulation 10 months before ovulation and 8 months before significant increase in sex hormones. Levels of the sex hormone 11-keto testosterone (11-KT) indicated a new role of this hormone at final maturation in salmon females. We propose the use of ultrasound as an alternative method to traditionally used invasive methods during sexual maturation monitoring in wild and farmed Atlantic salmon broodstock populations. Eliminating sacrifice of valuable broodfish, and reducing handling stress, would improve animal welfare in present-day broodstock management.

Keywords: Animal welfare; endocrinology; histology; reproduction; ultrasound.

Figures

Figure 1
Figure 1
Estimating GSI in Atlantic salmon females from ultrasound measurements. Relationship between real left ovary length and total ovary weight (A) and between ultrasound length and real length of left ovary (B). Linear and exponential models for estimating GSI indirectly by first estimating the total ovary weight and using body weight to calculate GSI (C), or directly from ultrasound length of left ovary (D). Comparison of GSI estimated by linear (E) and exponential (F) method and real GSI of females sampled during the last year before ovulation. Horizontal bars at the top represents changes in environment conditions. Data in E and F are mean ± SEM.
Figure 2
Figure 2
Vitellogenesis in female Atlantic salmon during the last year before ovulation, visualized using ultrasound and histology. Ultrasound (A) and histology (B) of previtellogenic female in September and December 2014, respectively. Ovaries in ultrasound images remain a uniform mass (C) as vitellogenesis has started (D) in some females in Decembler 2014. A growth in ovary area (E) can be observed in ultrasound images as vitellogenesis progresses in February 2015 (F). As some females reach tertiary yolk oocyte stage of vitellogenesis in February 2015, oocytes becomes clearly visible in ultrasound images (G and H). at, atretic oocyte; ca, cortical alveoli stage; in, intenstine; li, liver; mu, muscle; od, oil droplet stage; oo, oocyte; ov, ovary, pn: perinucleolus stage, py: primary yolk oocyte, sy: secondary yolk oocyte, ty: tertiary yolk oocyte. Scalebar in ultrasound images (right side) is 5 cm. Scalebar in all histology slides is 1 mm.
Figure 3
Figure 3
Gonad development of female Atlantic salmon during the last year before ovulation described as area fractions of different oocyte stages in histological sections. The area of oocyte development stages was calculated as percent of total area in sections from 12 to 2 months before ovulation. Horizontal bars at the top represent changes in environment conditions. Data are mean values.
Figure 4
Figure 4
Sex hormone levels in female Atlantic salmon grouped according to dominating oocyte stage area fraction during maturation. Oestradiol (A), testosterone (B), luteinizing hormone (C), 11‐keto testosterone (E) and maturation inducing hormone (F): pre‐vtg; previtellogenic females (n = 21; September 2014–February 2015), primary yolk oocytes (n = 17; November 2014–March 2015), secondary yolk oocytes (n = 14; January–May 2015), tertiary yolk oocytes (n = 44; March–July 2015). Follicle stimulating hormone (D): Pre‐vtg: previtellogenic females (n = 13; September 2014–January 2015), primary yolk oocytes (n = 12; December 2014–March 2015), secondary yolk oocytes (n = 14; January–May 2015), tertiary yolk oocytes (n = 43; March–July 2015). Bars are mean values and S.E.M. The line represents mean ultrasound estimated GSI and S.E.M. GSI was estimated from ovary length using direct exponential approach (Fig. 1D). Letters indicate significant differences in sex hormones, P < 0.05. Asterisks represents significant different USGSI measures.

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