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23 June 2016 Effects of Cold Winters on the Genetic Diversity of an Estuarine Fish, the Spotted Seatrout
Timothy P. O'Donnell, Stephen A. Arnott, Michael R. Denson, Tanya L. Darden
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Abstract

Spotted Seatrout Cynoscion nebulosus are recreationally important fish that have been harvested in South Carolina for centuries. The Spotted Seatrout in South Carolina suffered substantial declines in estuarine abundance during the cold winters of 2000, 2009, and 2010, when water temperatures dropped below their tolerance threshold. As these population declines may result in genetic bottlenecks and their repetitive occurrence over a short timescale could reduce the population's adaptive potential, we estimated the genetic diversity and effective population size (Ne) of the Charleston Harbor Spotted Seatrout population at six time points related to recent cold winters using a suite of 13 microsatellite markers. Grouping individuals by year-class (fish spawned in the same year) was the most appropriate and effective method for measuring interannual fluctuations in observed and expected heterozygosity and allelic richness, superior to partitioning fish by collection year. The genetic diversity of Spotted Seatrout was significantly influenced by catch per unit effort, although only minor changes were observed and Ne remained high. Short overlapping generations appear to allow Spotted Seatrout to genetically recover during population growth and maintain moderate levels of genetic diversity.

Fish have long been harvested from the world's oceans as a food resource, and in recent years the overexploitation of certain fish stocks has led to severe population declines or fishery collapses (Myers et al. 1995; Hutchings 2000). Although overfishing is a leading cause of declines in many fish populations, climatic variation can also exert a strong influence on fish population dynamics and have effects that are independent of or synergistic with overexploitation (Clark et al. 2003; Harley and Rogers-Bennett 2004; Tolimieri and Levin 2005; Eero et al. 2011). Therefore, fisheries managers need to consider the effects of climate in their regulatory strategies (Perry et al. 2010; Planque et al. 2010). With complex anthropogenic and environmental interactions driving fish population dynamics, informed, science-based management is essential to the recovery of depleted fish stocks (Botsford et al. 1997; Beddington et al. 2007). Thus, it is critical to understand not only the population dynamics of fish stocks but also how significant declines in abundance affect the health and resilience of the remaining individuals within a population.

Spotted Seatrout Cynoscion nebulosus is an estuarine resident that ranges from Cape Cod, Massachusetts, in the western Atlantic Ocean to Campeche, Mexico, in the southern Gulf of Mexico (Welsh and Breder 1923; Tabb 1966). The Spotted Seatrout is an important recreational species throughout its range, and in South Carolina an estimated mean of 212,000 fish (120 metric tons) have been harvested annually from 1981 to 2010 (National Marine Fisheries Service, Fisheries Statistics Division, Silver Spring, Maryland, personal communication). In recent years, below-average estuarine water temperatures during cold winters in South Carolina have caused population declines among Spotted Seatrout (Figures 1, 2); however, Spotted Seatrout have continued to support a strong recreational fishery due to intermittent mild winters and regulatory changes including a decrease in the bag limit in 1998 and an increase in the minimum size limit in 2007. Without prudent management, the repetitive occurrence of cold winters in the past decade may have made it difficult for Spotted Seatrout populations to sustain high numbers in the face of fishing pressure.

FIGURE 1.

Mean daily water temperatures at the Customs House in Charleston Harbor during extremely cold winters and the 15-year average daily water temperatures calculated as the means of all daily water temperatures for those dates from 1996 to 2011.

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FIGURE 2.

Mean CPUE (number per trammel net haul) of Spotted Seatrout in SCDNR's trammel net surveys in the Charleston Harbor system during the first quarter of each year. Open circles indicate sampling years immediately following cold winters; error bars = SEs.

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Spotted Seatrout routinely experience large fluctuations in physical water characteristics, including temperature, salinity, dissolved oxygen, and pH (Hubertz and Cahoon 1999). For the majority of these parameters, Spotted Seatrout show a wide range of physiological tolerances and are likely capable of moving to areas within estuaries that are within their tolerable ranges (Tabb 1966). When severe winter cold fronts move along the southeastern U.S. coast, strong winds and falling air temperatiues promote the mixing of estuarine waters, which can cause a rapid drop in water temperature in the shallow estuarine habitats where Spotted Seatrout are commonly found, including oyster reefs, marsh grass, and tidal creeks. While climate change does predict an overall trend of warming temperatures, models also predict greater temperature variability and extremes as well as an increase in extreme precipitation events (Kharin et al. 2013), which will promote rapid cooling of shallow estuarine waters during the winter months. Low, falling temperatures immobilize Spotted Seatrout, making it difficult for them to escape these shallow-water habitats to find warmwater refugia in deeper areas of the estuary (Tabb 1958). Based on historical environmental data, Spotted Seatrout populations in Florida experience substantial mortality when water temperatures fall below 7.2°C for longer than 24 h (Tabb 1958). Current evaluation of the cold temperature tolerance of Spotted Seatrout in South Carolina indicates that the threshold is actually much lower than 7.2°C; Spotted Seatrout experienced mortality at ~3°C, depending on the length of exposure (Anweiler 2014). While temperature drops of this magnitude are uncommon in deep channels, temperatures in the shallow tidal creeks that Spotted Seatrout commonly inhabit regularly drop below 5°C during extremely cold winters.

A relationship between cold winter events and decreased abundance of Spotted Seatrout in South Carolina has been documented over the past decade. For example, water temperatures in Charleston Harbor were 5.2°C below their average in the winter of 2000–2001 (U.S. Geological Survey 2012; Figure 1), with subseque