Influence of Size, Age, and Spawning Season on Sex Change in Black Sea Bass

A tagging study was conducted off the New Jersey coast to study sex change in Black Sea Bass Centropristis striata as a function of size, age, and spawning season. Throughout 2011–2013, 3,670 fish were measured and 1,498 were tagged from research, charter, and commercial fishing vessels. Of the tagged fish, 437 were recaptured. Size at 50% probability of sex change was 355 mm TL; the proportion of female fish in sexual transition increased with body size from 0.5% at 175–225 mm to 15.7% at 375–425 mm and increased with age from 0.6% at 3 years old to 18.2% at 6 years old. Relatively few females (8 of 107) changed sex during the spawning season, but a larger proportion (8 of 22 females) transitioned between spawning seasons. The proportion of females with transitional gonads was lowest at the start of the spawning season in June (0.2%), slowly increased over the summer, and sharply peaked just after the spawning season in October (9.5%). In addition, a high proportion of young mature fish were male (40% at age 2), which may indicate the presence of primary males. This is the first tagging study to estimate sex change as a function of size, age, and season in a protogynous hermaphroditic fish species. Use of tagging avoids potential problems that are associated with inferring sex change rates from sex ratios based on catch data. Sex change in hermaphroditic fishes can have important implications for fishery management (Alonzo and Mangel 2004; Heppell et al. 2006; Hamilton et al. 2007). The relationship between sex change and size, age, and season is of interest with regard to hermaphroditic species from multiple geographic regions, including tropical (Warner and Swearer 1991; Blaber et al. 1999; DeMartini et al. 2011) and temperate (Benton and Berlinsky 2006; Villegas-Rios et al. 2013) areas. Evidence suggests that harvest may bring about changes in the size at sex change (Warner and Swearer 1991; Hamilton et al. 2007; Götz et al. 2008) and in population sex ratios (Beets and Friedlander 1998; McGovern et al. 1998) and may influence the seasonality of sexual transition (Loke-Smith et al. 2010). These types of shifts in population structure and life history Subject editor: Isaac Wirgin, New York University School of Medicine, Tuxedo © M. M. Provost, O. P. Jensen, and D. L. Berlinsky This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/ licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. The moral rights of the named author(s) have been asserted. *Corresponding author: [email protected] Present address: Department of Wildlife, Fish, and Conservation Biology, University of California Davis, One Shields Avenue, Davis, California 95616, USA. Received March 7, 2016; accepted December 15, 2016 126 Marine and Coastal Fisheries: Dynamics, Management, and Ecosystem Science 9:126–138, 2017 Published with license by the American Fisheries Society ISSN: 1942-5120 online DOI: 10.1080/19425120.2016.1274696 can have profound effects on population dynamics (Alonzo et al. 2008); as a consequence, the effects of fishing on hermaphroditic species present unique challenges for fishery managers. In most fish species, the timing of reproductive events (e.g., differentiation, sex change, and age at maturity) plays an essential role in reproductive success, and these parameters should be considered across a variety of temporal scales (Lowerre-Barbieri et al. 2011). For example, is sex change restricted to specific months or seasons? Do fish transition within the spawning season? The paucity of knowledge on the timing of reproductive events in hermaphroditic fish species is a large hurdle for scientists and managers seeking to anticipate how fish stocks will respond to fishing pressure given their complicated life histories. The Black Sea Bass Centropristis striata is an economically important, protogynous hermaphroditic fish species found along the entire East Coast of the United States. The present study focuses on the northern stock of Black Sea Bass, which is located north of Cape Hatteras, North Carolina. Fishing mortality rates for the northern stock are thought to have been well above sustainable benchmarks from the late 1970s to the early 2000s, at which point they apparently declined to levels associated with maximum sustainable yield (Shepherd 2012). However, this understanding of fishing mortality rates and population dynamics is based on a stock assessment that was rejected as the basis for management by a peer review panel. One of the concerns raised by the review panel was the limited consideration of the protogynous life history of Black Sea Bass within the assessment model (Miller et al. 2011). The panel recommended “. . .research on rate, timing and occurrence of sexchange in this species” (Miller et al. 2011:17). The call for further research into sex change in Black Sea Bass adds to the growing concern over the manner in which stock assessments currently address sex change in hermaphroditic species within U.S. waters (Provost and Jensen 2015). Commercial and recreational fishing seasons overlap with the spawning season (late spring, summer, and early fall), during which Black Sea Bass populate reefs and artificial wrecks near shore. An acoustic tagging study conducted in the Mid-Atlantic Bight during May–September suggested that mature male Black Sea Bass that arrived early to spawning sites maintained larger home ranges than males arriving later in summer (Fabrizio et al. 2014). After the peak spawning season (May–August), when water temperatures drop in late October, adults migrate off the coastline and move southeast toward the continental shelf, where they remain throughout winter until the following spring (Musick and Mercer 1977; Moser and Shepherd 2009). Conditions during the winter period are likely the primary factor determining year-class strength of new Black Sea Bass recruits, as the presence of a strong age-0 year-class during the fall is not always indicative of whether that year-class will be strong during the following spring (i.e., at age 1; Miller et al. 2016). The mating system of Black Sea Bass is not completely known. Most male Black Sea Bass tend to be larger than females, but small males are also observed (Wenner et al. 1986; Wuenschel et al. 2011), possibly suggesting that some individuals develop as “primary” males instead of maturing first as females and then changing sex. Previous studies of Black Sea Bass have used experiments in controlled laboratory settings to understand the social and hormonal controls of sex change. Benton and Berlinsky (2006) manipulated sex ratios in Black Sea Bass held in tanks and found that the presence of large males discouraged females from changing sex in captivity, whereas the removal of males led the largest female in the group to undergo sexual transition within six weeks. For other sequential hermaphrodite species that are located in relatively accessible shallow-water reefs, the social dynamics that facilitate sex change have been observed directly in the species’ natural habitat (e.g., Bluehead Thalassoma bifasciatum: Warner and Swearer 1991; Halfmoon Grouper Epinephelus rivulatus: Mackie 2003). However, for many temperate hermaphroditic fishes, such as seabasses (Serranidae), groupers (Epinephelidae), and some wrasse species (Labridae), populations range over large geographic areas and inhabit deep water, which makes it difficult to perform direct observations and manipulative experiments in the field. Previous studies of these temperate species have estimated transition rates by examining fluctuations in the sex ratio based on catch data by size, age, or season (e.g., Erisman et al. 2010; Mariani et al. 2013). Other studies have used catch data to measure the percentage of transitional fish as a way to approximate the prevalence of sex change in the population (e.g.,Wenner et al. 1986; Brule et al. 2003; Burgos et al. 2007). Unfortunately, the use of catch data to estimate the population sex ratio and size at sex change can be biased for three specific reasons. First, catch data cannot distinguish between two phenomena in protogynous species: (1) fish in sexual transition may be rare in the catch if the process of sex change is rapid (i.e., it is difficult to capture fish “in the act” of transitioning); or (2) sex change may occur in a very small percentage of the population. Either phenomenon would result in low observed rates of transitional individuals unless sampling was conducted frequently throughout the year. Without knowledge of the duration of sexual transition, it is difficult to interpret such observations. Second, catch data can only estimate the size and age of transition if captured individuals are observed in the act of changing sex. It would be nearly impossible to know how many males in the catch had transitioned from females unless histology was used on every captured male to look for the remnants of female tissue that are present in male gonads after transitioning (Lavenda 1949). Catch data provide only a small subset of the data used to estimate the size and age at transition and the seasonality of sex change because the males that have already transitioned cannot be identified. Third, the size and age at transition have been inferred INFLUENCES ON SEX CHANGE IN BLACK SEA BASS 127