S.R. Melancon, R.A. Angus, and K.R. Marion 2013 Southeastern Naturalist Vol. 12, No. 4 684 2013 SOUTHEASTERN NATURALIST 12(4):684–691 Demographic Comparisons Between Reservoir-dwelling and Stream-dwelling Populations of a Threatened Turtle (Sternotherus depressus Tinkle and Webb) Sherry R. Melancon1, Robert A. Angus1, and Ken R. Marion1,* Abstract - Sternotherus depressus (Flattened Musk Turtle) is a federally threatened species endemic to the Black Warrior River drainage in north-central Alabama. Individuals of both stream-dwelling and impoundment-dwelling populations were trapped for comparative demographic analyses. Carapace length was significantly longer for reservoir turtles than for stream turtles. Size-class distributions between the two populations were also significantly different, with reservoir turtle collections biased toward the larger size classes, and presumably older age classes. These results suggest a reduced recruitment in the reservoir population, and raise concerns about long-term population sustainability in impoundment habitats. Introduction Endemic to the Black Warrior River drainage above the Fall Line in northern Alabama, Sternotherus depressus Tinkle and Webb (Flattened Musk Turtle) is a small kinosternid turtle (Dodd 2008, Ernst and Lovich 2009) that prefers small to medium-sized clear streams with alternating riffles and pools, and rocky or sandy substrates (Ernst et al. 1989, Mount 1981). Over the last several decades, the species has declined significantly in abundance and distribution and it is federally listed as threatened under the Endangered Species Act (USFWS 1987). The decline of the Flattened Musk Turtle has been primarily attributed to habitat degradation and fragmentation. Many streams in the Black Warrior basin have been degraded by strip-mining activities for coal, resulting in heavy benthic siltation, elevated metal concentrations and occasionally altered pH levels (USFWS 1987). These changes have also resulted in habitat fragmentation, which can increase vulnerability to disturbance, alter population genetic composition, and increase the possibility of extirpation (Dodd 1990, USFWS 1987). According to Dodd (1990), the Flattened Musk Turtle has disappeared from more than 50% of its estimated historic range, and most remaining populations are fragmented by extensive areas of degraded habitat. An important factor in the loss of preferred habitat and the increase in habitat fragmentation has been stream impoundment (Dodd 1990). While some turtle species adapt and do well in impoundments (Buhlmann et al. 2008, Dodd 1989, Moll and Moll 2004), other species have been negatively impacted, resulting in reduced abundance and altered population structure (Bodie 2001, Buhlmann and Gibbons 1997, Cook and Martin-Lamb 2004, Dickerson et al. 1999, Holland 1991, Jackson 2005, Reese and Welsh 1998a, Vandewalle and Christiansen 1996, Zappalorti and 1Biology Department, University of Alabama at Birmingham, Birmingham, AL 35294- 1170. *Corresponding author - kmarion@uab.edu. 685 S.R. Melancon, R.A. Angus, and K.R. Marion 2013 Southeastern Naturalist Vol. 12, No. 4 Iverson 2006). Further, few turtle species prefer the open waters of deep man-made reservoirs (Buhlmann et al. 2008). Factors that have been cited as having negative impacts on some turtle species due to impoundment of streams include: isolation of populations due to habitat fragmentation (Buhlmann and Gibbons 1997, Dodd 1990); reduction of food sources and feeding habitats (Cook and Martin-Lamb 2004; Moll 1980; Reese and Welsh 1998a, b; Vandewalle and Christiansen 1996); fluctuating water levels and resulting exposure of brumating turtles during winter drawdown (Bodie and Semlitsch 2000a, b; Dickerson et al. 1999; Vandewalle and Christiansen 1996); introduction of competitors, predators, and possible disease vectors (Vannote et al. 1980); reduction of basking habitats and benthic cover (Reese and Welsh 1998a, b; Vandewalle and Christiansen 1996); reduction of sandbars for nesting (Johnson 1992, Tucker et al. 1997); and anthropogenic alteration of the riparian zone (Bodie and Semlitsch 2000a, b; Dodd 1990; Moll 1980; Reese and Welsh 1998b; Zappalorti and Iverson 2006). Over the last fifty to sixty years, several large impoundments have been constructed in the Black Warrior River drainage, including the largest: Lewis Smith Reservoir. Completed in 1961, the reservoir is 56.3 km long, impounds 8579 ha of water at full pool, and has over 800 km of shoreline (Sznajderman 2012). More than 161 km of possible Flattened Musk Turtle stream habitat were inundated during impoundment. However, a number of studies since impoundment have shown that isolated populations of Flattened Musk Turtles continue to persist in Lewis Smith Reservoir, primarily in the impounded arms of the major inflowing streams (Bailey and Bailey 2003, Ernst et al. 1989, Mount 1981). These areas are separated from each other by extensive reaches of deep water with steep, often nearly vertical shorelines that the turtles cannot ascend to leave the water. This relief effectively fragments the reservoir populations due to unsuitable habitat, and the poor swimming ability of these benthic-dwelling turtles (Ernst et al. 1989). Our objective was to compare the population structure of Flattened Musk Turtle populations found in impoundments to those found in nearby streams. Our results may be used to assess the long-term viability of reservoir-dwelling populations of this threatened species. Methods Impoundment-dwelling turtles were trapped in both the Sipsey Fork and Brushy Creek arms of Lewis Smith Reservoir. Trapping sites were located in rocky coves separated from each other by long stretches of deep water and were 4.8–6.4 km below the inflowing stream habitat. Comparative stream turtle populations were trapped in both the Sipsey Fork and Brushy Creek. Trapping sites were located 3.2−4.8 km upstream of any physical impoundment influences. At sunset, we baited wire-mesh funnel-traps (Iverson 1979) with sardines, placed the traps near suitable shoreline cover, and checked them at dawn the following morning. Trapping locations at reservoir sites were reached by boat or by foot from the shoreline. Trapping on streams was performed by wading or shoreline access. Both reservoir and stream S.R. Melancon, R.A. Angus, and K.R. Marion 2013 Southeastern Naturalist Vol. 12, No. 4 686 sites were sampled during the summers of 2005 and 2006. The carapace length (CL) of each captured turtle was measured to the nearest 0.1 mm using dial calipers. Adult turtles were sexed based on tail length and vent location (Buhlmann et al. 2008, Ernst and Lovich 2009). Each turtle was individually identified for other on-going and future studies by injecting a coded passive integrated transponder (PIT) tag into the peritoneal cavity adjacent to the right hind leg before release (Buhlmann and Tuberville 1998). Differences between capture rates were tested for significance by calculating a 95% confidence interval for difference (Sahai and Kurshid 1996). If the confidence interval for the difference included zero, we concluded that the capture rates did not differ significantly at α = 0.05. Differences in carapace lengths between reservoir and stream turtles were tested for significance using the nonparametric Mann- Whitney U test because one of the samples (females collected from the reservoir) was not normally distributed (Lilliefors test: P = 0.020). Since t-tests are robust to departures from normality (Zar 2010), two-sample t-tests were also performed for all comparisons to determine whether any of the conclusions changed. Differences in carapace length distributions between reservoir and stream turtles (both sexes combined) were tested for significance using a two-sample Kolmogorov-Smirnov test. Significance was defined as P ≤ 0.05 for all statistical tests. Results We captured a total of 59 Flattened Musk Turtles (34 males, 24 females, 1 juvenile) at eight reservoir sites during 142 trap-nights, for a catch-per-unit-effort (CPUE) of 0.42. We captured 111 turtles (59 males, 52 females) at eight stream habitat sites during 302 trap-nights for a CPUE of 0.37. The 95% confidence interval for the difference between these two capture rates (-0.075 to 0.171) includes 0, indicating that they do not differ significantly at α = 0.05. The mean carapace length of reservoir turtles was 89.54 mm compared to a mean carapace length of 81.38 mm for stream turtles (Table 1, Fig. 1). There was no significant difference in the carapace length between male and female Flattened Musk Turtles collected from the reservoir (Table 1). All other carapace length comparisons were significant: females from stream sites were Table 1. Size distributions of Flattened Musk Turtles (Sternotherus depressus) according to size and location given as mean carapace lengths (mm) ± 95% confidence limits; sample sizes are in parentheses. The larger U and probability (P) values from Mann-Whitney U tests are shown in the margins of the table. The probabilities, based on a chi-square approximation with 1 d.f., are from Mann-Whitney U tests comparing the rank sums of the data summarized in the same row or column. Males Females U P Reservoir 88.79 ± 3.43 (34) 92.00 ± 2.98 (24) 481.5 0.245 Stream 77.70 ± 2.67 (59) 88.56 ± 2.72 (52) 2193 <0.001 U 1601.5 877 P <0.001 0.005 687 S.R. Melancon, R.A. Angus, and K.R. Marion 2013 Southeastern Naturalist Vol. 12, No. 4 significantly longer than males from stream sites, males from the reservoir were significantly longer than males from stream sites, and females from the reservoir were significantly longer than females from the stream sites (Table 1). When both sexes were combined, there was a significant difference in population size-distributions between stream and reservoir sites (P < 0.001): reservoir turtle collections were proportionally biased toward the larger size classes (Fig. 1). Discussion Results from our trapping efforts suggest that there is no significant difference in the abundance of Flattened Musk Turtles between the reservoir and stream locations we sampled. However, the population-size structures differ significantly between the two habitat types. The mean carapace length was greater in reservoir turtles than in stream turtles. Further, results from our analyses of size-class distributions indicate that the reservoir population has relatively fewer smaller individuals and a relatively greater number of larger, and presumably older, individuals than the stream population. Although factors such as differences in food abundance and water temperatures can affect growth in turtles (Germano and Bury 2009), the differences in mean carapace length and size distributions Figure 1. Size-class distributions of reservoir- and stream-dwelling Flattened Musk Turtles (Sternotherus depressus) as percent of each collection, both sexes combined. Numbers above bars are numbers of individuals captured in each size class. S.R. Melancon, R.A. Angus, and K.R. Marion 2013 Southeastern Naturalist Vol. 12, No. 4 688 between the two habitats strongly suggest that many individuals in the reservoir population are reasonably old. Melancon et al. (2011) have shown that Flattened Musk Turtles grow more slowly than most small kinosternids and, based on von Bertalanffy growth-curve analysis, these turtles can reach ages of 40–60 years. At the time our study was conducted, Lewis Smith Reservoir had been impounded for >40 years. Thus, the larger reservoir individuals likely began life as stream residents. One possible explanation for the differences in demographic characteristics between the two populations is that recruitment and/or survival of younger individuals is low in the relatively “top heavy” reservoir population. The recruitment and/or survival of younger turtles in Lewis Smith Reservoir may be impacted by a number of factors. Food abundance may be reduced in the reservoir. Hatchlings and very young Flattened Musk Turtles are primarily insectivorous (Tinkle 1958), whereas the diet of larger juveniles and adults is 90% mollusks (Marion et al. 1991). Cursory observations by Ernst et al. (1989) and benthic dredges in the current study (data not published) indicate low-density aquatic insect and mollusk populations in Lewis Smith Reservoir. This impoundment also undergoes a winter drawdown, with water levels 3–6 m below the summer pool level (Alabama Power Company 2005). Bodie and Semlitsch (2000a, b), Dickerson et al. (1999), and Vandewalle and Christiansen (1996) have reported that such drawdowns can potentially affect survival in reservoir-dwelling turtles. The impoundment of streams has also eliminated favorable nesting areas used by stream-dwelling turtles (Johnson 1992, Tucker et al. 1997). The greatest population densities of Flattened Musk Turtles occur in streams with a sandy and/or rocky benthic substrate (Ernst et al. 1989, Mount 1981). These streams usually have small areas of exposed sandy banks or sand bars for much of the year. Although Flattened Musk Turtles are adaptable in choosing nest locations, we have found several nests in sandy areas over the years (K.R. Marion, pers. obs.). The lack of such areas in impoundments may negatively impact recruitment success in the reservoir population. Finally, much of the shoreline of Lewis Smith Reservoir has been developed for residential purposes. Numerous authors have noted that the conversion of riparian habitats to human land-use is often deleterious to turtle populations (Bodie and Semlitsch 2000a, b; Dodd 1990; Moll 1980; Reese and Welsh 1998a, b). Zappalorti and Iverson (2006) noted that riparian alteration near springs containing Sternotherus minor minor Agassi (Loggerhead Musk Turtles) likely reduces their populations. The findings in this study suggest that reservoir-dwelling populations of Flattened Musk Turtles, a threatened species, may decline in abundance over the long term, and ultimately, these populations may not be sustainable. This result may be especially significant, because we conducted our study in the upper reaches of Lewis Smith Reservoir, where there is some suitable habitat for Flattened Musk Turtles, and not in the extensive lower reaches of the impoundment, where the water is very deep and the shorelines are nearly vertical. Few, if any, Flattened Musk Turtles are likely to have persisted in the lower reaches subsequent to impoundment. We note that our conclusions on recruitment are based on size distributions only, and analyses 689 S.R. Melancon, R.A. Angus, and K.R. Marion 2013 Southeastern Naturalist Vol. 12, No. 4 of other measures may yield different results. Germano and Bury (2009), working with Actinemys marmorata Baird and Girard (Western Pond Turtle), cautioned against reliance on size alone as a measure of population structure or trends in turtle populations because local differences in a number of resource and physiological factors could have major influences on turtle demography. More studies are needed to characterize the population status, recruitment, and size-class distributions of the Flattened Musk Turtle population in the Lewis Smith Reservoir, AL, in order to better assess the population’s long-term prospects for success. 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