Age-modulated variation in reproductive development of female Pacific Ocean perch (Sebastes alutus) in waters off Oregon

We investigated the maturity of female Pacific ocean perch (Sebastes alutus) in waters off Oregon. Visual and histological methods produced similar results during the months of December to March; however, neither method provided reliable determinations of reproductive maturity in other months. Evidence of abortive maturation, characterized by mass atresia of the developing class of oocytes, was observed in 7.1% of the fish sampled during December to March, with a strong age-related decline in prevalence. Fish older than 18 (N = 73) showed no evidence of abortive maturation regardless of size, further supporting the higher reproductive value of older rockfishes. Abortive maturation was associated with adolescence (age 5-9 years), but was also observed in post-adolescent fish, especially in 2001 samples. Rates of abortive maturation varied between the years 2001 and 2003, suggesting an environmental influence on successful egg development in younger fish. Pacific ocean perch off Oregon were 50% mature at a length of about 31 cm and an age of six, two years younger than assumed in recent stock assessment models for the West Coast population. Introduction The age and length at maturity for female fish is a critical parameter in many stock assessment models. For example, Clark (1991) and Lunsford (1999) have shown that changes in the age at 50% maturity (A50), espe2 Hannah and Parker—Variation in Reproductive Development cially in relation to the median age of fishery recruitment, can have a strong influence on estimated target fishing rates. Target fishing rates are used by the Pacific Fishery Management Council (PFMC) to manage most groundfish stocks (Clark 1991, PFMC 2000). One example of a target fishing rate would be F40%, the fishing mortality rate that would reduce spawning stock biomass per recruit to 40% of the unexploited level. The importance of errors in estimating the median age of female maturity was illustrated by Lunsford’s (1999) study of maturity of Pacific ocean perch (Sebastes alutus), where a shift in the estimated median age of maturity for female fish from 7.5 to 10.5 years decreased the F40% value from 0.110 to 0.076, a decrease of 31%. Correct estimation of target fishing rates is especially critical for U.S. West Coast rockfish (Sebastes spp.) stocks, as they are considered to be some of the least resilient (Leaman 1991, Clark 2002). For many species of rockfish, especially those found on the upper continental slope, age and length at 50% maturity (L50) are not well established (Love et al. 2002). Some information on L50 has been gathered for most slope rockfish species over the last several decades (Westrheim 1975, Wyllie Echeverria 1987, Barss 1989). These early studies, however, either did not collect age data (Westrheim 1975, Barss 1989), or they based ages on surface readings rather than the more accurate “break and burn” technique (Chilton and Beamish 1982, Wyllie Echeverria 1987). For some West Coast rockfish species, including Pacific ocean perch, the most extensive maturity data available have been from samples collected during the triennial National Marine Fisheries Service summer abundance surveys (Hamel et al. 2003). These data cover a wide geographic range and generally include a wide size range of fish, unlike commercial fishery samples that often lack adequate numbers of smaller, immature fish. However, these data are also based on a simple visual assessment of maturity, so they suffer from a different, but potentially serious, problem. In summer, maturity status of ovaries from winter spawning species like Pacific ocean perch can be very difficult to determine accurately—ovaries of mature, “resting” fish are macroscopically identical to ovaries of immature fish (Wallace and Selman 1981). The problem is best addressed by collecting a wide size range of fish during seasonal time periods when visual maturity determinations are more accurate. However, even within an optimal sampling period, the possibility remains that visual assessment of female rockfish maturity could be an inaccurate assessment of actual or “functional” maturity, meaning the successful production of larvae. Nichol and Pikitch (1994) evaluated maturity of darkblotched rockfish (S. crameri) microscopically and found that some ovaries with evidence of vitellogenesis also showed mass atresia and resorption of oocytes. Their findings underscore the importance of using histological evidence of maturity over visual assessment, as the difference between a funcBiology, Assessment, and Management of North Pacific Rockfishes tionally immature and a functionally mature individual can depend on attributes visible only microscopically, even during the period of reproductive growth. The primary objective of this study was to collect maturity samples from female Pacific ocean perch and evaluate the benefits of using histological sections to determine maturity as opposed to visual assessment. An additional objective was to develop age and length at maturity data specific to U.S. West Coast Pacific ocean perch that could be used in stock assessment. Maternal age has been suggested as a potentially important predictor of reproductive success in rockfish (Leaman 1988, Berkeley et al. 2004). However, supporting data for individual species are very limited. Recent studies of larval quality in black rockfish (Berkeley et al. 2004) suggest a maternal-age effect on larval survival. A third objective of this study was to evaluate the effect of maternal size and age on reproductive success and the seasonal timing of ovarian development in Pacific ocean perch. Methods Maturity data for female Pacific ocean perch were collected from two sources, dockside sampling of Oregon’s commercial fishery landings and chartered research trawl trips. Each fish was measured (cm fork length). An ovary was removed and assigned a macroscopic maturity stage (Table 1) following the criteria of Westrheim (1975). Only experienced samplers were used to assign macroscopic maturity stages to minimize errors in visual staging. One ovary was then preserved from each female fish for histological examination, except for fish with an unambiguous maturity status, such as those with developed larvae or recently spent ovaries. Sagittal otoliths were removed for subsequent age determination. Ages were determined using the break and burn technique (Chilton and Beamish 1982). Table 1. Visual maturity stages and descriptions for rockfish ovaries from Westrheim (1975). Stage Condition Description 1 Immature Small, translucent 2 Maturing Small, yellow, translucent or opaque 3 Mature Large, yellow, opaque 4 Fertilized Large, orange-yellow, translucent 5 Ripe Large, translucent yellow or gray, with black dots (contain embryos or larvae) 6 Spent Large, flaccid, red. A few larvae may be present 7 Resting Moderate size, firm, red-gray, some with black blotches Hannah and Parker—Variation in Reproductive Development Ovaries were collected from all female fish that were not visually assigned stage 4 (fertilized eggs), 5 (eyed larvae) or 6 (recently spent). Ovaries in these three stages were considered to be unequivocally mature. Ovaries were preserved in 10% buffered formalin, and later transferred to 70% ethanol for storage. Tissue samples from the midsection of the ovary were then embedded in paraffin, sectioned at 5 μm, and stained with Harris’s hematoxylin and eosin Y (West 1990). We measured the diameter of the five largest, spherical, non-atretic oocytes in each stained thin-section with an ocular micrometer (100 ×) and calculated a mean maximum oocyte diameter (MMOD) for each sample (West 1990). MMOD was compared for mature and immature fish to determine the appropriate period to evaluate samples to determine maturity. The samples were classified as mature or immature based on the presence or absence of vitellogenin, post-ovulatory follicles, and level of atresia. If the majority of the developing class of oocytes was atretic, maturation was considered abortive and the individual was considered functionally immature. The accuracy of visual examination of ovaries was then evaluated by comparing the maturity status from visual examination with status determined from histological sections. Logistic regression was used to fit sigmoid length-maturity and agematurity curves to microscopically verified maturity data. The model fitted had the general form,