Histological Analysis Reveals Larger Size at Maturity for Southern Flounder with Implications for Biological Reference Points

For fish stocks managed using biological reference points based upon spawning biomass, it is critical to have accurate maturity schedules. We investigated sizeand age-dependent patterns in maturity for southern flounder Paralichthys lethostigma, a flatfish supporting valuable coastal fisheries in North Carolina and throughout its range. We evaluated both macroscopic and histological methods over two consecutive reproductive seasons. Histological analyses revealed that maturity occurred at larger sizes and older ages than previously estimated. Length at 50% maturity (L50) was estimated at 408 mm total length (TL), which was more than 60 mm larger than currently assumed, and was relatively stable between study years. We found that only 44% of age-1 southern flounder were mature compared with an estimated 74% in an earlier study. We suspect that most of the differences in maturity timing of southern flounder between our findings and previous studies stem from macroscopic assignment error. During this study, only 61% of fish staged macroscopically as developing were found to be mature based on histological analysis. Assuming incorrectly that all of these fish were mature would have resulted in an L50 of 375 mm TL, which is closer to previous estimates. Analysis of spawning stock biomass per recruit demonstrated that biological reference points (e.g., FSPR) could be affected considerably by shifting maturity schedules, and the effects could be magnified at larger sizes at entry and higher harvest rates. Given the life history strategy of southern flounder and the lack of a developed offshore fishery or sampling program, which combine to prevent access to fish on the spawning grounds, it is probably most judicious to routinely analyze reproductive tissue samples histologically to ensure accurate information on the timing of maturity. The influence of individual reproductive biology on the productivity and resilience of fish stocks has received much recent attention (Kjesbu 2009; Lowerre-Barbieri et al. 2011a). Basic information on the timing and extent of reproductive output such as spawning seasonality and fecundity can refine estimates of stock production and biological reference points (Marshall 2009). More specifically, an accurate understanding of the timing of maturity is essential for effective fisheries management (King and McFarlane 2003). The size and age at which fish become mature is a critical element of a species’ life history (Roff 1982; Dieckmann and Heino 2007), and variation in fish Subject editor: Susan Lowerre-Barbieri, Florida Fish and Wildlife Research Institute, St. Petersburg *Corresponding author: [email protected] Received April 6, 2012; accepted July 28, 2012 maturity scheduling can directly affect annual and lifetime reproductive output. Due to resource limitations, many contemporary biological sampling programs still use traditional approaches to assign individual fish to maturity stages based on macroscopic features of the gonads. Unfortunately, macroscopically based maturity assignments often lack agreement with histological assessments of maturity, which can contribute to erroneous conclusions about the status of the stock (Saborido-Rey and Junquera 1998; Tomkiewicz et al. 2003; Costa 2009; Ferreri et al. 2009). For instance, Vitale et al. (2006) revealed that 628 D ow nl oa de d by [U ni ve rs ity o f N or th C ar ol in a W ilm in gt on ] a t 1 3: 37 0 4 D ec em be r 2 01 2 HISTOLOGICAL ANALYSIS OF SOUTHERN FLOUNDER 629 the use of macroscopic staging alone overestimated female spawning-stock biomass in Atlantic cod Gadus morhua in the Kattegat by up to 35%. These results highlight the need for more routine application of histological analyses (e.g., West 1990) that require more time and expense, but yield the most accurate reproductive information (Hilge 1977; Hunter and Macewicz 1985; Murua and Saborido-Rey 2003). Southern flounder Paralichthys lethostigma occur in estuarine and marine waters of the U.S. southern Atlantic Ocean and the Gulf of Mexico, supporting valuable commercial and recreational fisheries throughout their range (Gilbert 1986). Southern flounder are spawned offshore and settle in shallow estuarine and freshwater habitats during late winter and early spring (Wenner et al. 1990; Lowe et al. 2011). Juveniles grow quickly (0.35–1.5 mm/d; Fitzhugh et al. 1996) and some individuals may recruit to commercial and recreational fisheries before reaching age 1. Southern flounder are sexually dimorphic, and females attain larger sizes and contribute disproportionately to fishery landings. Immature southern flounder remain in estuarine habitats for about 2 years or until they mature, at which time they migrate offshore to spawn. The prevailing view maintains that, after spawning, southern flounder return to estuaries, although the fraction of fish returning and the extent of nearshore habitat use have recently been questioned (Wenner et al. 1990; Watterson and Alexander 2004; Taylor et al. 2008). In North Carolina, southern flounder has been the most valuable finfish resource for much of the past two decades (North Carolina Division of Marine Fisheries [NCDMF] commercial harvest statistics 1991–2010; http://portal.ncdenr.org/web/ mf/marine-fisheries-catch-statistics). Currently, the North Carolina stock is considered to be “depleted” due to a long period of elevated harvest rates beginning in the early 1990s. The initial fishery management plan (NCDMF 2005) established several new harvest restrictions in an attempt to lessen the impact on the stock by reducing fishing mortality rates. However, recent findings indicate that fishing mortality rates may still be higher than management targets, at least in the river-based gill-net segment of the fishery (Smith et al. 2009). Indeed, the most recent stock assessment determined that the stock remains both overfished (spawning-stock biomass [SSB] below target) and is undergoing overfishing (fishing mortality [F] above target) (TakadeHeumacher and Batsavage 2009). Observations by Smith and Scharf (2010) also revealed that the commercial gill-net harvest comprised mostly young (primarily age 1) fish, many of which were probably immature. Sizeand age-based maturity schedules for female southern flounder were first estimated for North Carolina fish captured during the mid-1990s by Monaghan and Armstrong (2000). Their findings resulted in an estimated L50 (length at which 50% of females are mature) of 345 mm, and that 18.1% and 73.5% of age-0 and age-1 fish, respectively, were mature. However, all but 2 of 19 running-ripe females collected in ocean waters were greater than 414 mm, and age-1 females failed to demonstrate a defined peak in their gonadosomatic index (GSI) during late fall, which was observed for age-2 and older fish (Monaghan and Armstrong 2000). More recent studies have provided new evidence suggesting that maturation of southern flounder may occur at larger sizes and older ages. Smith and Scharf (2010) examined a small number (n = 31) of southern flounder gonads histologically and estimated that only 56.6% of age-1 females were mature, with no observations of mature age-0 fish. Taylor et al. (2008) found that many southern flounder demonstrated chemical signatures in their otoliths consistent with estuarine residency until just before the deposition of the third annulus (i.e., age-2 fish about to turn age 3), suggesting delayed participation in offshore spawning. Here, we used histology to estimate the size and age at maturity for southern flounder from estuarine waters throughout North Carolina. We compared histologically validated maturity estimates to those generated using only existing macroscopic criteria, and we examined seasonal and size-dependent patterns in GSI as an indicator of maturity. Last, we explored the impact of variable maturity schedules on estimates of southern flounder spawning stock biomass and management reference points.