Secondary sexual characters, energy use, senescence, and the cost of reproduction in sockeye salmon

Reproductive development and energy stores were characterized for sockeye salmon (Oncorhynchus nerka) maturing in the wild (Pick Creek, Bristol Bay, Alaska). Between freshwater entry and the start of spawning, ovaries increased in mass by 87.1% and secondary sexual characters increased in linear dimension by 13.0–47.4%. Between the start of spawning and death, secondary sexual characters decreased in relative size by 3.3–12.7%. Mass-specific somatic energy declined from freshwater entry (6.7% fat, 20.6% protein, 6.6 kJ·g–1) to the start of spawning (1.6% fat, 18.0% protein, 4.5 kJ·g–1) and finally to death (0.1% fat, 14.4% protein, 2.9 kJ·g–1). Stored fat appeared to be used primarily for upriver migration and egg production, whereas stored protein appeared to be used primarily for the development of secondary sexual characters and metabolism during spawning. Most development of secondary sexual characters occurred late in maturation, perhaps to forestall deterioration of muscle tissue. Relative to populations with long freshwater migrations, Bristol Bay sockeye salmon stored less fat before entering fresh water and used less fat before death. The total energy cost of reproduction (freshwater entry until death, including gonad investment) was 74.1% for females and 66.1% for males, higher than levels typically reported for iteroparous salmonids. Résumé : Le développement du système reproducteur et les réserves énergétiques ont été étudiés chez le Saumon rouge (Oncorhynchus nerka) au cours de la maturation, en nature (Pick Creek, baie de Bristol, Alaska). Entre le moment de leur en eau douce et le début de la fraye, la masse ovarienne des saumons augmente de 87,1% et leurs caractères sexuels secondaires augmentent de 13,0–47,4% dans leur dimension linéaire. Entre le début de la fraye et la mort, la taille relative des caractères sexuels secondaires diminue de 3,3–12,7%. L’énergie somatique spécifique à la masse diminue depuis l’entrée en eau douce (6,7% de graisses, 20,6% de protéines, 6,6 kJ⋅g–1), jusqu’au début de la fraye (1,6% de graisses, 18,0% de protéines, 4,5 kJ⋅g–1) et finalement jusqu’à la mort (0,1% de graisses, 14,4% de protéines, 2,9 kJ⋅g–1). Les graisses de réserve semblent utilisées surtout au cours de la migration vers l’amont et servent à la production d’oeufs, alors que les réserves de protéines sont utilisées surtout à la production des caractères sexuels secondaires et au métabolisme durant la fraye. La plupart des caractères sexuels secondaires apparaissent tard au cours de la maturation, peut-être pour retarder la détérioration du tissu musculaire. Comparativement aux populations qui font de longues migrations en eau douce, les Saumons rouges de la baie de Bristol accumulent moins de graisses avant leur entrée en eau douce et en utilisent moins jusqu’à leur mort. Le coût énergétique total de la reproduction (de l’entrée en eau douce jusqu’à la mort, en comptant le coût de formation des gonades) a été évalué à 74,1% chez les femelles et à 66,1% chez les mâles, valeurs plus élevées que celles qui prévalent généralement chez les salmonidés itéropares. [Traduit par la Rédaction] 1675 Hendry and Berg Introduction The most taxing period of life for many organisms is reproduction, when resources are diverted from procuring food and into tasks necessary for successful breeding. As a result, energetic constraints are often associated with reproduction, and these constraints are particularly evident in species with low energy intake and high energy expenditure during breeding. Sockeye salmon (Oncorhynchus nerka) migrate long distances from feeding areas in the open ocean to their natal spawning sites in streams or lakes (Burgner 1991). Females develop large gonads (about 25% of their body mass; Hendry et al. 1999) and engage in vigorous competition for access to spawning sites (Foote 1990). Males undergo extensive morphological changes (Davidson 1935) and fight incessantly for access to spawning females (Quinn et al. 1996). Feeding ceases at entry into fresh water, often several months before spawning commences (capital breeding), and all fish die after a single spawning season (semelparous). Given severe limitations on available energy and conflicting demands for that energy, natural selection should tend to optimize patterns of reproductive development and energy allocation. We investigated these patterns in the context of five specific objectives. Our first objective was to document the temporal sequence of development for secondary sexual characters, traits that typically differ between the sexes and influence “the advantage which certain individuals have over other 1663 Can. J. Zool. 77: 1663–1675 (1999) © 1999 NRC Canada Received December 15, 1998. Accepted July 12, 1999. A.P. Hendry.1 School of Fisheries, University of Washington, Box 357980, Seattle, WA 98195-7980, U.S.A. O.K. Berg. Department of Zoology, Norwegian University of Science and Technology, NTNU, 7034 Trondheim, Norway. 1Author to whom all correspondence should be sent at the following address: Department of Zoology, University of British Columbia, 6270 University Boulevard, Vancouver, BC V6T 1Z4, Canada (e-mail: [email protected]). J:\cjz\cjz77\cjz-11\Z99-158.vp Friday, January 14, 2000 9:48:43 AM Color profile: Disabled Composite Default screen