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First published online December 16, 2008
Journal of Experimental Biology 212, 56-70 (2009)
Published by The Company of Biologists 2009
doi: 10.1242/jeb.021352
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Activity of the pituitary–gonadal axis is increased prior to the onset of spawning migration of chum salmon

Takeshi A. Onuma1,2,*, Shunpei Sato3, Hiroshi Katsumata2, Keita Makino2, WeiWei Hu2, Aya Jodo2, Nancy D. Davis4, Jon T. Dickey5, Masatoshi Ban3, Hironori Ando1, Masa-aki Fukuwaka6, Tomonori Azumaya6, Penny Swanson5 and Akihisa Urano2

1 Graduate School of Bioresource and Bioenvironmental Sciences, Kyushu University, Fukuoka 812-8581, Japan
2 Section of Biological Sciences, Graduate School of Life Sciences, Hokkaido University, Sapporo 060-0810, Japan
3 National Salmon Resources Center, Fisheries Research Agency, Sapporo 062-0922, Japan
4 School of Aquatic and Fishery Sciences, University of Washington, Seattle, WA 98195, USA
5 Northwest Fisheries Science Center, NOAA Fisheries, Seattle, WA 99164, USA
6 Hokkaido National Fisheries Research Institute, Fisheries Research Agency, Kushiro 085-0802, Japan


Figure 1
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  		Fig. 1. Offshore, coastal and freshwater sampling locations where chum salmon were collected. (A) Sampling locations for immature and maturing chum salmon in the Gulf of Alaska, the central Bering Sea and the NW Pacific Ocean. In summer, chum salmon were caught in the Bering Sea along and near 180° longitude during cruises of the RV Wakatake-maru in 2001–2003, and at locations in the NW Pacific Ocean at 154°59'E during the cruise of the RV Hokusei-maru in 2001 (circles). In autumn, fish were caught in the central Bering Sea during cruises of the RV Kaiyo-maru in September 2001–2003 (open squares). In winter, chum salmon were caught at stations in the Gulf of Alaska during cruises of the RV Kaiyo-maru in February 2006 (filled squares). (B) Sampling locations for pre-spawning chum salmon in September–October, 2001–2003 in SW and FW in Hokkaido, Japan. a: Esashi on the NE coast; b,c: Ishikari Bay; d: Ishikari River estuary; e: midway between the coast and the hatchery; f: fish wheel located 4 km downstream from the hatchery; and g: the hatchery at the Chitose Field Station.

 

Figure 2
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  		Fig. 2. Frequency distributions of the gonadosomatic index (GSI) for pre-migratory male and female chum salmon in the central Bering Sea, 2001–2003. The GSIs were determined from fish caught during summer (June and July, upper panel) and autumn (September, lower panel). Fitted curves were obtained using a Gaussian distribution with multiple peaks. The ages of fish were estimated from their scales. Data collected during summer show a sizable component of fish with a high GSI, whereas fish with a high GSI are nearly absent in September.

 

Figure 3
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  		Fig. 3. (A) Amount of glycoprotein {alpha}2 (GP{alpha}2) mRNA, (B) follicle-stimulating hormone β (FSHβ) mRNA and (C) FSH in the pituitaries of chum salmon in the central Bering Sea and the NW Pacific Ocean, 2001–2003. Fish were divided into immature fish and maturing adult I and II on the basis of histological observation of the gonads. Value are means ± s.e.m. Significant differences among groups are indicated with different letters (P<0.05 one-way ANOVA and Tukey's test). See Table 1 for the number of fish.

 

Figure 4
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  		Fig. 4. (A) Amount of luteinizing hormone β (LHβ) mRNA and (B) LH in the pituitaries of chum salmon in the central Bering Sea and the NW Pacific Ocean, 2001–2003. Fish were divided into immature fish and maturing adult I and II, as shown in the inset in Fig. 3. Values are means ± s.e.m. Significant differences among groups are identified with different letters (P<0.05 one-way ANOVA and Tukey's test). See Table 1 for the number of fish.

 

Figure 5
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  		Fig. 5. Plasma levels of follicle-stimulating hormone (FSH), testosterone (T), 11-ketotestosterone (11KT) and estradiol (E2) in chum salmon in the central Bering Sea and the NW Pacific Ocean, 2001–2003. Fish were divided into immature fish and maturing adult I and II, as shown in the inset in Fig. 3. Values are means ± s.e.m. n.d., not determined. Significant differences among groups are identified with different letters (P<0.05 one-way ANOVA and Tukey's test). See Table 1 for the number of fish.

 

Figure 6
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  		Fig. 6. Scatter plots showing the correlation between the gonadosomatic index (GSI) and the pituitary contents of follicle-stimulating hormone (FSH) and luteinizing hormone (LH) in pre-migratory male and female chum salmon in the central Bering Sea, 2002-2003. Clade A is made up of Japanese populations and clade B is a mixture of Russian, North American and Japanese populations. The maturing adults with increased FSH and LH were observed in both clades.

 

Figure 7
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  		Fig. 7. Activity of the pituitary–gonadal axis (PG axis) in winter chum salmon in the Gulf of Alaska in terms of (A) the amounts of glycoprotein {alpha}2 (GP{alpha}2), follicle-stimulating hormone β (FSHβ) and luteinizing hormone (LHβ) mRNAs, FSH and LH in the pituitary and (B) the plasma level of FSH, testosterone (T), 11-ketotestosterone (11KT) and estradiol (E2). Fish were collected in February 2006, and divided into immature fish and maturing adult I on the basis of histological features of the gonads. Samples from the winter chum salmon were assayed together with those from the maturing Bering fish in 2003 (N=5 in each sex) for comparison of data with the summer fish in the Bering Sea. Value are means ± s.e.m. See Table 1 for the number of fish.

 

Figure 8
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  		Fig. 8. Changes in the levels of gonadotropin (GTH) subunit mRNAs in the pituitary, and pituitary and plasma levels of follicle-stimulating hormone FSH and luteinizing hormone LH during upstream migration in 2002. Pre-spawning and mature adults were collected along their homing pathway from the coast to the hatchery, as shown in Fig. 1B. Fish near or at the hatchery almost completed final maturation, so that they were considered as mature adults. Furthermore, data are compared with those from maturing adult I in the Bering Sea. Date of sampling and the number of fish are shown in Table 4. Value are means ± s.e.m. n.a., not applicable. Significant differences among sampling points are identified with different letters (P<0.05 one-way ANOVA and Tukey's test). Asterisks indicate significant difference (P<0.05) when compared with the maturing adult 1 in the central Bering Sea.

 

Figure 9
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  		Fig. 9. Changes in plasma levels of testosterone (T), 11-ketotestosterone (11KT), estradiol (E2) and 17{alpha}-20β-dihydroxy-4-pregnen-3-one (DHP) during upstream migration in 2002. Pre-spawning and mature adults were collected along their homing pathway from the coast to the hatchery, as shown in Fig. 1B. Fish at or near the hatchery almost completed final maturation, so that they were considered as mature adults. Furthermore, data are compared with those from maturing adult I in the Bering Sea. Date of sampling and the number of fish are shown in Table 4. Value are means ± s.e.m. Significant differences among sampling points are identified with different letters (P<0.05 one-way ANOVA and Tukey's test). Asterisks indicate significant difference (P<0.05) when compared with the maturing adult 1 in the central Bering Sea.

 

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