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Growth of the Flattened Musk Turtle, Sternotherus depressus Tinkle and Webb
Sherry R. Melancon, Robert A. Angus, and Ken R. Marion

Southeastern Naturalist, Volume 10, Issue 3 (2011): 399–408

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2011 SOUTHEASTERN NATURALIST 10(3):399–408 Growth of the Flattened Musk Turtle, Sternotherus depressus Tinkle and Webb Sherry R. Melancon1, Robert A. Angus1, and Ken R. Marion1,* Abstract - Sternotherus depressus (Flattened Musk Turtle) is a threatened endemic of the Black Warrior River basin in northern Alabama. Carapace lengths taken from recaptures of turtles individually marked over an 18-year period were used to generate von Bertalanffy growth curves for both sexes. Females grew faster than males early in life and reached estimated asymptotic size at a younger age. Size-at-sexual-maturity data from previous studies indicate that males reach maturity in 10–12 years, while females mature at 12–15 years. Compared to a spring-dwelling Florida population of S. minor (Loggerhead Musk Turtle), the Flattened Musk Turtle has a slower growth rate, a greater age at maturity, and a smaller asymptotic size. These differing life-history characteristics likely reflect cooler water temperatures and reduced food availability in Flattened Musk Turtle habitats. Introduction Sternotherus depressus Tinkle and Webb (Flattened Musk Turtle) is a small aquatic kinosternid turtle endemic to the Black Warrior River drainage above the Fall Line in northern Alabama (Ernst and Lovich 2009). The turtle prefers clear, shallow streams with a rocky or sandy substrate. The species is federally listed as threatened under the Endangered Species Act, primarily because of strip-mining activities for coal, which have degraded many streams in the Black Warrior basin (USFWS 1987). According to Dodd (1990), the Flattened Musk Turtle has disappeared from more than 50% of its former range, and most remaining populations are fragmented by extensive areas of degraded habitat. However, some moderate-sized populations still exist in a few locations (Holmes and Marion 2004). As with many long-lived species, age determination, life span, growth rates, and sex-specific growth patterns are difficult to ascertain through direct observations or short-term studies. Knowledge of such parameters may be important in the conservation of declining or threatened species or in management for their recovery. In this study, we examine aspects of the growth of the Flattened Musk Turtle. Annual rings on epidermal scutes have often been used to estimate the age of young turtles, but they become indistinct and increasingly unreliable in older individuals (Germano and Bury 1998). The von Bertalanffy growth equation has often been used to generate growth curves for several groups of vertebrates using data from individuals of known age (e.g., Huang et al. 2008). Due to the inability to obtain reliable age estimates in some organisms, such as older turtles, 1Biology Department, University of Alabama at Birmingham, Birmingham, AL 35294- 1170. *Corresponding author - 400 Southeastern Naturalist Vol. 10, No. 3 an alternative method of determining growth patterns was devised. The von Bertalanffy growth equation was rearranged by Fabens (1965) into a form that uses growth intervals. The interval form of the equation permits the estimation of growth parameters using capture-recapture data from animals of unknown age. Frazer et al. (1990) used a natural population of Trachemys scripta Schoepff (Pond Slider) to compare a von Bertalanffy growth equation using known age data to Fabens’ derivative method under the assumption that no ages were known. The study concluded that there were no significant differences in the values of any of the estimated parameters. In order to use Fabens’ derivative method, a measurement at the time of initial capture and at the time of recapture, and the time interval between measurements, are required. Fabens’ derivative equation has been used to construct growth curves for a number of turtle species, including Caretta caretta L. (Loggerhead Sea Turtle; Casale et al. 2009, Frazer and Ehrhart 1985), Chelonia mydas L. (Green Sea Turtle; Frazer and Ehrhart 1985, Green 1993), Emydoidea blandingii Holbrook (Blanding’s Turtle; Huang et al. 2008), Gopherus polyphemus Daudin (Gopher Tortoise; Aresco and Guyer 1999), Sternotherus minor Agassiz (Loggerhead Musk Turtle; Cox et al. 1991), Terrapene carolina L. (Eastern Box Turtle; Dodd and Dreslik 2008), and Trachemys scripta Schoepff (Pond Slider; Frazer et al. 1990). Although the von Bertalanffy growth model cannot be used to estimate the age of an individual turtle with a high degree of precision, it is useful in the absence of more reliable methods for estimating the approximate age of a turtle of a given sex and carapace length. Additionally, analysis of von Bertalanffy growth curves can reveal useful information about the differential life-history strategies which may be employed by males and females of a species. An alternative growth model, the Gompertz model, has been used to estimate growth patterns in some turtles (Cox et al. 1991). Gompertz curves were generated in the initial phases of this study, but the fits were very poor; therefore, only the von Bertalanffy model was used in our analysis. Methods Study areas and data collection Carapace length records of individually marked Flattened Musk Turtles from several mark–recapture studies previously conducted on Sipsey Fork and Brushy Creek in Winston County, AL were combined with recapture data from the current study to determine growth intervals and instantaneous individual growth rates. Sipsey Fork and Brushy Creek are similar-sized confluent tributaries of the Black Warrior River system. Carapace length records for individual turtles were available from a 1983 study by Ernst et al. (1989); 1985 and 1986 studies by Dodd et al. (1988); a report for the Water Works and Sewer Board of the City of Birmingham, AL by Mount et al. (1991); 1994 and 1995 studies by Bailey and Guyer (1998); and from the current study conducted in 2002 and 2003. Data 2011 S.R. Melancon, R.A. Angus, and K.R. Marion 401 from each of these studies were compiled, and turtles which had been captured more than once were identified. Any cases where there was doubt of individual identification or inconsistency in gender assignment between captures were discarded. A total of 192 instances of recapture between years were found. In cases when the same individual was recaptured more than once over the period of these studies, only the carapace lengths at the first and last captures were used. The resulting 154 growth intervals (90 males, 61 females, and 3 juveniles) were used in our analyses. Turtles in all studies were captured using wire-mesh funnel traps (Iverson 1979a) baited with sardines in soybean oil or were hand collected by wading at dusk or night with a flashlight. In all studies except the current one, captured Flattened Musk Turtles were given a unique identification using scute notching; however, in the current study, an 11-mm passive integrated transponder (PIT) tag (Biomark, Inc., Boise, ID) was injected into the right anterior inguinal region parallel to the bridge of the shell to give each captured animal a unique identifi- cation number (Buhlmann and Tuberville 1998), and any notching from previous studies was recorded. Carapace length in all studies was measured by calipers to the nearest 0.1 mm. Variation in individual growth rates Growth rates in individual turtles have been shown to be highly variable (Davenport and Scott 1993, Gibbons et al. 1981, Moll and Legler 1971, Plummer 1977, Sexton 1965). Relative instantaneous growth rates were determined for each recaptured turtle using the ΔGR equation modified from Brody’s (1945) derivation using the formula ΔGR = loge(L2 / L1) / (t2 - t1) = (loge[L2] - loge[L1]) / (t2 - t1), where L1 and L2 represent the carapace lengths (in mm) at first and second captures, respectively, and t2 - t1 represents the time interval (in years to two decimal places) between consecutive measurements. The formula yields an estimate of instantaneous growth rate at mean carapace length (CL) that can be used to compare the growth rates of turtles of similar CL’s. The instantaneous growth rate for each individual was plotted against its mean size between captures. Linear regression was performed separately for each sex to investigate trends in growth rates as size increased. The difference between sexes in the slope of the growth vs. size regression was tested for significance using a t test (Zar 2010). Outliers with unusually high growth rates were checked for common features such as area and year of capture. This procedure was used by Cox et al. (1991) to evaluate variations in growth rates in Sternotherus minor. von Bertalanffy growth model Growth was modeled separately for each sex using the von Bertalanffy growth equation 402 Southeastern Naturalist Vol. 10, No. 3 L = a(1 - be-kt), where L is carapace length, a is the asymptotic carapace length, b is a parameter related to the size at hatching, k is the intrinsic growth rate, and t is age. The a and k parameters were estimated using the von Bertalanffy growth interval equation for capture-recapture data L2 = a - (a - L1)e-kd, where L1 is CL at first capture, L2 is the CL at recapture, and d is the time between captures (Aresco and Guyer 1991, Cox et al. 1991, Frazer and Ehrhart 1985). The r2 (observed vs. predicted) value was used to indicate the goodness-of-fit to the data. After the asymptotic size and intrinsic growth rate parameters were estimated, b was estimated using the formula b = 1 - (h / a), where h is the carapace length at hatch (28 mm; based on the average of two clutches measured two days after hatching). Ninety-five percent confidence intervals were constructed around the growth curves using the method of Seber and Wild (1989). To test the hypothesis that the growth parameters were different for males and females, a dummy variable (z) was coded to be 0 for females and 1 for males. The growth interval equation was fitted to the total data set (males and females) using nonlinear least squares regression, but with an extra two “difference” parameters (da and dk) that allowed the asymptote and intrinsic growth rate to take on different values in males and females: L2 = (a + da x z) - ([a + da x z] - L1) x e-(k + dk x z) x d. If the 95% confidence interval for the estimate of da or dk did not contain zero, the corresponding parameter (a or k) was considered to differ significantly between sexes at α = 0.05. Due to the primarily insectivorous diet of smaller juvenile Flattened Musk Turtles (Tinkle 1958), only a few juveniles were captured by baited traps during all of the various studies. Thus, the generated growth curves might not accurately estimate the rate of growth during the first few years of life. In order to validate the generated growth curves and the 95% confidence intervals, eight preserved smaller juveniles (ranging from 34–55 mm CL) were obtained from collections at the University of Alabama and Auburn University. The age of each individual was estimated by counting growth annuli on the carapacial scutes using the technique of Sexton (1959). These individuals of undetermined sex were then plotted on the growth curve for each sex. The results of this study were compared to those of a similar study on the closely-related Sternotherus minor (Cox et al. 1991). The S. minor study was conducted in a warm-water spring in Florida with an abundant food supply, whereas the Flattened Musk Turtle occurs in cooler-water streams with abundant shade, where activity is suspended during the winter. 2011 S.R. Melancon, R.A. Angus, and K.R. Marion 403 Results Instantaneous growth rate The amount of time between first capture and last capture for the 154 individuals used in the analysis averaged 3.8 years and ranged from 1 to 18 years. ΔGR was negatively correlated with mean size between the initial capture and recapture in both sexes (females: r = -0.60, P = 3.63 × 10-7; males r = -0.26, P = 0.014; Fig. 1). The decrease in growth rate with size was steepest in females. However, due to the large amount of variability in the data, the slopes of the regression lines did not differ significantly between the sexes (P = 0.106). Capture location and year of capture were not predictors of the outliers. von Bertalanffy growth model Figure 2 shows the von Bertalanffy growth curves for both sexes. The r2 (observed vs. predicted) for males was 0.96 and for females was 0.95, both indicating good fits. The estimated asymptotic CLs (a) of male and female Flattened Musk Turtles were 102.7 and 102.1 mm, respectively. The Wald 95% confidence interval for the difference variable, da, included zero, indicating that the difference in asymptotic size between males and females was not significant at α = 0.05; however, males and females do not reach their maximum sizes at the same rate. The intrinsic growth rate parameter (k) estimate for males was 0.04 and for females 0.07. The Wald 95% confidence interval Figure 1. Relative instantaneous growth rates of individual turtles (ΔGR) plotted against mean carapace length (CL) between initial capture and recapture. 404 Southeastern Naturalist Vol. 10, No. 3 Figure 2. von Bertalanffy growth curves for male (a) and female (b) Flattened Musk Turtles. CL is carapace length (mm). Dashed lines represent 95% confidence limits. Darkened circles represent juveniles from museum specimens of undetermined sex whose ages have been estimated from growth annuli on carapacial scutes. Open circles represent two superimposed individuals. 2011 S.R. Melancon, R.A. Angus, and K.R. Marion 405 for the difference variable, dk, did not contain zero, indicating that the difference was significant at α = 0.05. Length and age estimates from museum specimens of smaller unsexed juveniles are indicated as dots on the growth curves of both sexes (Fig. 2). These individuals fall within the 95% confidence intervals for females. Two of the eight fall outside the confidence intervals for male growth, perhaps indicating that the curve may slightly underestimate early growth rate in males or that those individuals were females. Discussion Differential growth rates between the sexes have been noted in several species of turtles (Ernst and Lovich 2009, Gibbons et al. 1981). Our results indicate that female Flattened Musk Turtles grow faster early in life than do males, but reach the same asymptotic adult size. Female Flattened Musk Turtles lay 1–3 large eggs per clutch up to two times per year (Close 1982). The eggs can be larger than 30 mm x 15 mm and can weigh more than 5 grams (Dodd et al. 1988). The accelerated growth rate of females early in life may represent an adaptive strategy to reach egg-bearing size as soon as possible, thereby minimizing the risk of juvenile female mortality. In contrast, the generated growth model indicates that male growth throughout life is more gradual. Male Flattened Musk Turtles have larger home ranges than females (Dodd et al. 1988). In order to maximize their reproductive potential, males may spend more energy searching for potential mates and less energy on growth. Consequently, females reach 95% of their asymptotic size at 38.0 years of age, while males do not reach 95% of their asymptotic size until 61.0 years of age (Fig. 2). Based on histological examination of gonads, Close (1982) conservatively estimated that male Flattened Musk Turtles reach maturity around 60 mm CL, while females become sexually mature between 70 mm and 75 mm CL. Based on the generated growth curves (Fig. 2), males should reach sexual maturity at 10–12 years of age, while females become sexually mature in 12–15 years. These estimates of time to reach maturity are somewhat greater than for most other kinosternid turtles (Ernst and Lovich 2009; Iverson 1979b, 1991), and may reflect the relatively unproductive environmental conditions of their habitat. Cox et al. (1991) applied the von Bertalanffy and Gompertz growth models to a springdwelling Florida population of the closely related Loggerhead Musk Turtle, and estimated that females reached maturity in 8 years at a mean of 80 mm CL, while males averaged 5.6 years to reach maturity at 55 mm CL. Additionally, both sexes essentially reached their asymptotic size between 25 and 30 years of age, earlier than for Flattened Musk Turtles. Loggerhead Musk Turtles also had a higher instantaneous growth rate and reached a greater asymptotic size (male = 112.8 mm CL, female = 110.4 mm CL). Such differences in growth characteristics between Flattened Musk Turtles and the population of Loggerhead Musk Turtles studied by Cox et al. (1991) likely represent physiological and evolutionary responses to differing environmental conditions. The Loggerhead Musk Turtle study was 406 Southeastern Naturalist Vol. 10, No. 3 conducted in a relatively warm-water spring, where the turtles have a long activity period and an abundant mollusk food supply. Our study was conducted in a temperate stream with abundant shade cover where activity is suspended during the winter. In addition, mollusk populations in Sipsey Fork and Brushy Creek are low to moderate in density (Rogers and Marion 2004). The Flattened Musk Turtle has suffered significant population declines, local extirpation, and habitat fragmentation over most of its geographic range, primarily due to habitat degradation caused by previous coal strip-mining activities (Dodd 1990). Fonnesbeck and Dodd (2003) also found that a disease of unknown etiology reduced population size on a stretch of the Sipsey Fork in the mid-1980s. They noted that population levels had not recovered significantly over time. 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