Long-Term Trends in Ringed Sawback (Graptemys oculifera) Growth, Survivorship, Sex Ratios, and Population Sizes in the Pearl River, Mississippi Author(s): Robert L. Jones Source: Chelonian Conservation and Biology, 16(2):215-228. Published By: Chelonian Research Foundation https://doi.org/10.2744/CCB-1268.1 URL: http://www.bioone.org/doi/full/10.2744/CCB-1268.1
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BioOne sees sustainable scholarly publishing as an inherently collaborative enterprise connecting authors, nonprofit publishers, academic institutions, research libraries, and research funders in the common goal of maximizing access to critical research. Chelonian Conservation and Biology, 2017, 16(2): 215–228 doi:10.2744/CCB-1268.1 Ó 2017 Chelonian Research Foundation Long-Term Trends in Ringed Sawback (Graptemys oculifera) Growth, Survivorship, Sex Ratios, and Population Sizes in the Pearl River, Mississippi
ROBERT L. JONES
Mississippi Department of Wildlife, Fisheries, and Parks, Museum of Natural Science, 2148 Riverside Drive, Jackson, Mississippi 39202 USA [[email protected]]
ABSTRACT. – Effective management of long-lived species requires demographic and life-history data that are best acquired from long-term studies. The ringed sawback (Graptemys oculifera), endemic to the Pearl River watershed of Mississippi and Louisiana, is a species of management concern at both the state and federal levels. Population sizes, trapping success, basking counts, sex ratios, survivorship, and growth of this species were investigated at 5 sites on the Pearl River in Mississippi over a 25-yr period. Estimates of age at maturity were 4.6 yrs for males and 9.1 yrs for females. Mean annual survivorship estimates for males, females, and juveniles were 0.88, 0.93, and 0.69, respectively. Maximum longevity estimates were 48.8 yrs for males and 76.4 yrs for females. Average longevity estimates were 8.5 yrs for males and 13.9 yrs for females. The sex ratio of captured turtles was male-biased before 2000 but unbiased after 2000. Realized population growth estimates indicated that 4 populations were stable over the 25-yr period and 1 population had declined. Population estimates and basking counts trended downward through time at most sites. Trapping success after 2000 for all sites combined declined by 77%, 45%, and 25% for juveniles, males, and females, respectively. Taken together, these data indicate that 1 population of G. oculifera has declined, 3 appear to be in the initial stages of decline, and 1 is relatively stable. Additional monitoring of these populations will be necessary to determine if these trends continue into the future.
KEY WORDS. – Reptilia; Testudines; Emydidae; Graptemys oculifera; population sizes; trapping success; basking counts; sex ratios; survivorship; longevity; realized population growth; Pearl River; Mississippi
Aspects of the population ecology and demography of as Threatened in 1986. Jones and Hartfield (1995) studied long-lived species may only be understood through population size, growth, and age at maturity of this species analysis of information from studies of sufficient duration at 5 sites on the Pearl River in Mississippi from 1988 to (Likens 1983; Strayer et al. 1986; Pelton and van Manen 1990, and Jones (2006) documented the reproductive 1996; Gibbons et al. 2000; Armstrong and Ewen 2013), as biology of G. oculifera at one of these sites, Ratliff Ferry, research conducted on a time scale that is short relative to a in 1995 1996. Trapping at the 5 study sites continued species’ life span may generate data that lead to inaccurate periodically from 1994 to 2014 to investigate G. oculifera estimates of the traits under study (Zweifel 1989; Pelton population size changes through time. These efforts also and van Manen 1996; Madsen and Shine 2001). Data from provided data on trapping success, growth, morphology, long-term studies are important not only for accurately and survivorship of G. oculifera and on trapping success for estimating demographic parameters of long-lived species Graptemys pearlensis, a poorly known species also but also for their effective management (Lindenmayer et endemic to the Pearl River watershed (Selman and Jones al. 2012; East et al. 2013). Given that many turtle species 2017). These data allowed a reassessment of growth and are in decline (Gibbons et al. 2000) and that demographic age at maturity of G. oculifera, provided estimates of data, including adult survival estimates and population survivorship and longevity, and permitted an examination growth rates, are essential in making management of population size, sex ratio, and body size variation decisions for those species (Converse et al. 2005), long- through time at each of the 5 sites. This information should term studies are particularly important for turtles, which as not only help wildlife officials make informed decisions a group may include some of the longest-lived vertebrates about the management of this species but will also provide a (Gibbons and Semlitsch 1982; Gibbons 1987). baseline for comparative studies in the future. Theringedsawback,Graptemys oculifera,isendemic to the Pearl River system of Mississippi and Louisiana, METHODS where it occurs primarily in the main channel of both the Pearl River and its largest tributary, the Bogue Chitto River. The 5 study areas were described in Jones and The species was listed by the US Fish and Wildlife Service Hartfield (1995) and Selman and Jones (2017). The most 216 CHELONIAN CONSERVATION AND BIOLOGY, Volume 16, Number 2 – 2017
Trapping sessions during 1988 1990 are described in Jones and Hartfield (1995) and for the Ratliff Ferry reproductive study by Jones (2006). Sampling for the reproductive study was directed toward females as traps were attached to larger logs and limbs normally used by that sex as basking sites. Males and juveniles were likely underrepresented in these samples, so data from the 1995 1996 reproductive study are included in overall body size, growth, and survivorship analyses, but were not used in estimates of sex ratios, capture success, or population sizes. Trapping from 1994 to 2014 occurred over a 5-d period at each study site. Captured turtles were sexed, measured, and permanently marked by drilling holes in the marginal scutes using the coding system of Cagle (1939) as was done in earlier studies (Jones and Hartfield 1995; Jones 2006; Selman and Jones 2017). If a captured turtle had been previously marked, the mark was recorded and the turtle was remeasured. Sex was determined based on the lengths of the foreclaws and the tail (Lindeman 2013). Small turtles that could not be sexed were classified as Figure 1. Locations of the study areas on the Pearl River, Mississippi. juveniles, but if sex could be determined upon recapture, they were included with the appropriate sex in subsequent analyses. Straight-line maximum carapace length (CL) was upriver site is near Carthage and the most downriver site is measured along the midline of the shell to the nearest near Columbia (Fig. 1). Sampling occurred at Carthage millimeter with either tree or dial calipers depending upon and Columbia in 1989 1990, 1994, 2002, 2009, and 2014. the size of the turtle. Midline plastron length (MPL) was Trapping at the other 3 sites took place in 1988 1990, measured to the nearest 0.1 mm with dial calipers. Turtles 1994, 2002, 2008, and 2013, so each site was sampled were temporarily marked for population estimates by over a period of 25 yrs. applying a spot of nontoxic red or orange waterproof paint Turtles were captured in open-topped, rectangular to both sides of the carapace. The paint dried in less than 2 basking traps constructed of 2.54-cm hex wire poultry min and remained visible for up to 3 mo. There was no netting (chicken wire) or poultry netting coated with evidence that paint marks were lost prior to counts of 3 plastic (crayfish wire). Traps varied in size from 100 50 turtles. 3 25 cm to 150 3 65 3 45 cm and were attached to limbs Recaptured turtles were divided into 4 classes based and logs used as basking sites by the turtles. Traps were on their sizes at capture and at recapture. Class 1 turtles monitored frequently during the day and at the approach of were first captured as juveniles (not sexable) or immatures the monitoring boat, basking turtles usually jumped from (males, , 65 mm MPL; females, , 120 mm MPL) and basking structure into the trap. A basking trap of this recaptured as immatures, Class 2 were first captured as nature requires frequent monitoring to be successful, juveniles or immatures and recaptured as adults, Class 3 because turtles that fall into the traps can escape within a were adults smaller than the hypothesized asymptotic MPL few seconds by swimming out of the open top, in contrast (males, 78.21 mm; females, 134.08; Jones and Hartfield to treadle basking traps (e.g., Ream and Ream 1966), 1995) at capture, and Class 4 were adults larger than the which are more difficult to escape and thus do not require hypothesized asymptotic MPL at capture. Only 3 males continuous monitoring. met the requirements for Class 1, and as these were within The number of basking traps deployed per day varied , 1 mm of 65 mm MPL, they were added to Class 2. from 28 to 30, so the midpoint of this range (29) was used From 1988 to 1990, 2 basking counts/site were to calculate capture effort. The number of hours trapped conducted to estimate population sizes at Carthage, Ratliff per day sometimes varied owing to the onset of inclement Ferry, and Columbia, and 4/site at Lakeland and weather, rising water levels, or mechanical difficulties with Monticello (Jones and Hartfield 1995). From 1994 to the trapping boat, so a full day of trapping was considered 2014, 5 basking counts were conducted for each sample to last for a minimum of at least 6 hrs. Days with , 6 hrs period at all sites. In all basking counts, the numbers of of trapping were eliminated from analyses of capture painted and unmarked G. oculifera were recorded. Turtles success to avoid biasing the results. Traps were moved were counted primarily from concealed points on the river periodically to minimize trap avoidance and to sample as bank using binoculars or a spotting scope or from a slow- much of the available basking structure as possible at a moving boat in the center of the channel when the river particular study site. banks were steep or otherwise inaccessible. Population JONES — Ringed Sawback Turtles in the Pearl River, Mississippi 217
Table 1. von Bertalanffy growth model and interval equations, in which CL = carapace length, MPL = midline plastron length, a = asymptotic length, k = intrinsic growth rate, e = base of the natural logarithm, b = birth parameter (a parameter related to hatchling size), hCL = CL at hatching (35.51 mm), hMPL = MPL at hatching (29.75 mm), t = age in years, CLC = CL at capture, CLR =CLat recapture, MPLC = MPL at capture, MPLR = MPL at recapture, and d = time in years between capture and recapture. Both hCL and hMPL are from Jones (2006).
Carapace length Midline plastron length
kt kt Growth model, CLt = aCL(1 bCLe ) MPLt = aMPL(1 bMPLe ) where: bCL =1 hCL /aCL bMPL =1 hMPL /aMPL kd kd Interval equations CLR = aCL (aCL CLC)e MPLR = aMPL (aMPL MPLC)e sizes for each site were estimated using both the Schnabel equation CL = 1.092(MPL) þ 5.04, based on the relation- mark–recapture model (SM) and the Lincoln-Peterson ship between MPL and CL in juveniles of this species model (LP) calculated as in Tanner (1978). SM and LP (F1,151 = 3685.14, p , 0.001). Growth curves were population estimates were made at Ratliff Ferry, Lakeland, estimated for each sex using CL and MPL separately, and Monticello in 1988, at Carthage and Columbia in first with recapture data only (FI and MI models) and then 1989, at all 5 sites in 1994 and 2002, at the first 3 sites in with recapture data combined with back-calculated growth 2008 and 2013, and at the last 2 sites in 2009 and 2014. increments (FII and MII models). One LP estimate was generated per basking count but only Survivorship (u), recapture probability (q), and 1 SM estimate was generated per study period per site, realized population growth (k)ofbothsexeswere resulting in 5 SM and 22 24 LP estimates per site. calculated using recapture data with Cormack-Jolly-Seber Kofron (1991) stated that male G. oculifera matured (CJS) models for the first 2 parameters and a Pradel model at an MPL of 60 70 mm and Jones and Hartfield (1995) (Pradel 1996) for the third (Program Mark; White and used the midpoint of that range (65 mm) as an estimate of Burnham 1999, version 8.0). Both the CJS and Pradel size at maturity. Females with an MPL 120 mm were models assume that q is equal for all animals in a considered adults based upon both a growth curve (Jones population and that marked animals have equal u from and Hartfield 1995) and reproductive data (Jones 2006). sample to sample (Pollock et al. 1990). These assumptions Sexable individuals smaller than these sizes were consid- may be violated when data is pooled across different ered immature. populations or sex/age classes within the same population In an earlier study of G. oculifera growth using MPL (Lebreton et al. 1992), so to minimize potential bias in the as the body size variable, the von Bertalanffy (VB) growth estimates of both q and u, these parameters were model provided the best fit to recapture data (Jones and calculated for males and females separately in each of Hartfield 1995). Growth curves in that study were the 5 study populations. estimated for each sex by fitting data from turtles Four models to estimate u and q were evaluated for recaptured approximately 1 yr or more after their initial each sex at each site. Both u and q were either held capture to the VB growth equation (Table 1) as defined in constant or were allowed to vary with sampling period. Frazer and Ehrhart (1985). Few juvenile turtles , 1 yr old Models for each sex-by-site combination were evaluated at initial capture were recaptured during that study and the using the quasi-Akaike’s information criterion (QAICC; absence of data from very young individuals resulted in a Hurvich and Tsai 1989), which estimates the best fit of the poor fit of the recapture data to the VB growth model. To data using the fewest parameters. I used Program Mark to remedy the problem, growth increments in MPL were calculate QAICC weights, which provided an index of the back-calculated using Sergeev’s formula (Moll and Legler likelihood of a model relative to other models in the 1971) for 10 juveniles to provide growth data from analysis and can be interpreted as model probabilities hatching to age 1, which resulted in an increase in the (Burnham and Anderson 2004). Program Mark was also coefficient of determination (R2) and thus a better fit to the used to calculate median cˆ, a variance inflation factor that VB growth model. quantifies overdispersion of the data and is analogous to a In the present study, CL and MPL were each used to goodness-of-fit test (Burnham et al. 1987). A median cˆ of generate separate growth equations for each sex. Both a 1.0 indicates a model that fits the data well while a cˆ . 3.0 and k were estimated by nonlinear regression of MPL and indicates that the model does not provide an adequate fit to CL on the VB growth interval equation, and the hatchling the data (Lebreton et al. 1992). Both the QAICC weights length parameter b (Table 1) was estimated using hatchling and median cˆ values were used to evaluate models. length data from Jones (2006). As in the earlier study, few Parameter estimates were averaged using the model recaptured G. oculifera (2 males and 2 females) were in averaging routine of Program Mark. Models that exhibited their first year of growth when initially captured. Back- parameters which were either poorly supported (low calculated MPL growth increments were again generated QAICC weights), confounded, or poorly estimated by the from 10 juveniles and those MPLs were then used to data (e.g., zero standard error), were eliminated from the calculate CLs for those individuals at age 1 using the analyses. 218 CHELONIAN CONSERVATION AND BIOLOGY, Volume 16, Number 2 – 2017
Table 2. Means of initial carapace length (CL) and midline plastron length (MPL) of recaptured Graptemys oculifera by sex, by class based on state of maturity at capture and at recapture (see text), and for turtles in each group that exhibited no growth between capture and recapture. n = sample size, YRS1 = mean number of years between capture and recapture, DCL = mean change in CL/yr, CVDCL = coefficient of variation of DCL, DMPL = mean change in MPL/yr, CVDMPL = coefficient of variation of DMPL, NODCL = number of turtles and percentage (in parentheses) in each group that showed no growth in CL between capture and recapture, and YRS2 = mean number of years between capture and recapture for the turtles showing no growth. All means are followed by 1 standard deviation (in parentheses).
n CL MPL YRS1 DCL CVDCL DMPL CVDMPL NODCL (%) YRS2 Males Class 2 19 63.8 (11.2) 53.3 (10.2) 8.4 (7.5) 3.3 (2.2) 0.65 3.1 (2.0) 0.63 0 (0.0) Class 3 95 85.6 (4.2) 72.5 (3.3) 6.0 (6.2) 0.5 (0.9) 1.69 0.6 (0.8) 1.43 39 (40.4) 4.5 (5.2) Class 4 56 95.6 (2.9) 81.7 (2.7) 5.9 (5.0) 0.2 (0.4) 1.64 0.2 (0.3) 1.43 30 (53.6) 5.7 (5.0) Mean 86.4 (10.6) 73.4 (9.4) 6.9 (5.9) 0.8 (1.4) 1.82 0.7 (1.2) 1.68 69 (40.6) 5.0 (5.1) Females Class 1 26 84.8 (23.8) 72.5 (21.4) 4.1 (2.8) 9.2 (6.2) 0.68 8.3 (5.7) 0.69 0 (0.0) Class 2 64 108.1 (21.3) 94.5 (19.4) 8.8 (5.7) 5.3 (3.1) 0.58 4.6 (2.6) 0.57 4 (6.3) 3.4 (2.3) Class 3 63 148.1 (5.0) 127.8 (3.9) 6.6 (5.0) 0.9 (1.6) 1.84 0.8 (1.4) 1.90 15 (23.8) 6.6 (6.1) Class 4 52 162.4 (5.6) 141.1 (4.9) 7.7 (5.4) 0.6 (0.8) 1.25 0.6 (0.8) 1.35 15 (28.8) 4.8 (2.4) Mean 131.2 (31.7) 113.8 (27.7) 7.2 (5.3) 3.3 (4.2) 1.30 2.9 (3.8) 1.32 34 (16.6) 5.4 (4.5)
The Pradel model was used to estimate k for each sex where MR = instantaneous mortality rate and u = annual at each site. This model also estimates u and q, and all 3 survival probability. parameters were either held constant or allowed to vary Few G. oculifera first captured as juveniles were with time, resulting in 8 models for each site-by-sex recaptured, which precluded an estimate of u for juveniles combination. Model suitability was evaluated by Akaike’s from recapture data. This parameter can be calculated, information criterion (AICC) and AICC weights. The however, if u of adult females, mean age at female estimates of k for the first interval in several models were maturity, mean annual clutch frequency, and mean clutch problematic because of exceptionally high or low k values size are known, by using the following equation (modified or standard errors, so all first-interval estimates of k from from Pike et al. 2008): all models were eliminated from further consideration 1=FM because of the potential for bias and confounding as uJ ¼ 2ð1 uAÞ=ðCFÞðCSÞ suggested by White and Burnham (1999). The estimates of k were averaged for all sites using the model averaging where uJ = juvenile annual survival rate, uA =adult routine of Program Mark and the geometric mean of these female annual survival rate, CF = average number of estimates, their standard deviations, and their 95% clutches per year, CS = average clutch size, and FM = fe- confidence intervals (CI) were calculated. male age at first reproduction. Maximum longevity (ML) for each sex at each site All statistical tests unless otherwise indicated were was estimated using the following equation (modified performed by Systatt (Systat 2009), and the figure was from Litzgus 2006): produced using DIVA-GIS (Hijmans et al. 2012) and Microsoft Paint. Sequential Bonferroni adjustments for ML ¼ lnðnÞ=lnðuÞ multiple comparisons were calculated as in Rice (1989) where u = annual survival probability, and n = estimated with an experiment-wise error rate set at a =0.10 population size. Average population size at each site over (Chandler 1995). the course of the study was calculated from the SM estimates, but these represented both sexes combined. The RESULTS sex ratios of males and females at each site, exclusive of turtles captured during the reproductive study at Ratliff Recaptures. — Almost 400 G. oculifera were Ferry, were calculated and were used with the population recaptured at least 1 yr or more after their initial capture estimates to determine the number of each sex at each site. (Table 2). Most males (147, 86.5%) and females (168, Average longevity (AL) for each sex at each site was 82.0%) were recaptured , 10 yrs after initial capture, 8 estimated using the following equation (van der Toorn males (4.7%) and 25 females (12.2%) were recaptured 1997): between 10 and 20 yrs after initial capture, and 12 males (7.1%) and 8 females (3.9%) were recaptured 20 yrs AL ¼ 1=lnðuÞ after initial capture. There were no significant correlations where u = annual survival probability. The instantaneous between date and the number of recaptures (males: mortality rate (the inverse of AL) was estimated using the r = 0.174, p = 0.116; females: r = 0.140, p = 0.149; following equation (modified from Tucker et al. 2001): sexes combined: r = 0.129, p = 0.138), implying that the overall rate of recapture for all areas combined was MR ¼ lnðuÞ relatively constant for the duration of the study. JONES — Ringed Sawback Turtles in the Pearl River, Mississippi 219
Table 3. Results of nonlinear regressions on carapace length (CL) and midline plastron length (MPL). The model designations MI and FI include data from recaptures only, MII and FII include recapture data plus back-calculated CL and MPL from 10 individuals (see text). a = asymptotic length, k = intrinsic growth rate, RMS = residual mean square, R2 = coefficient of determination, and b = birth parameter. Values in parentheses following parameter estimates are standard errors, and 95% CI are von Bertalanffy 95% support-plane confidence intervals on a and k.
Model a 95% CI k 95% CI RMS R2 b Males MI MPL 80.07 (0.49) 79.10 81.04 0.153 (0.012) 0.129 0.176 9.58 0.662 0.628 MII MPL 78.79 (0.48) 77.84 79.73 0.281 (0.025) 0.232 0.331 16.98 0.747 0.622 MI CL 93.27 (0.54) 92.19 94.34 0.163 (0.013) 0.137 0.189 12.87 0.663 0.619 MII CL 92.02 (0.53) 90.97 93.06 0.293 (0.027) 0.241 0.346 21.74 0.742 0.614 Females FI MPL 140.18 (0.92) 138.37 141.99 0.189 (0.010) 0.169 0.210 49.28 0.789 0.788 FII MPL 140.14 (0.89) 138.38 141.90 0.190 (0.010) 0.171 0.209 48.40 0.906 0.788 FI CL 162.40 (1.16) 160.12 164.68 0.176 (0.010) 0.156 0.196 71.19 0.781 0.781 FII CL 162.26 (1.12) 160.05 164.47 0.178 (0.009) 0.160 0.197 69.82 0.896 0.781
Growth. — Growth rate as measured by change in CL females but not in males (Table 3) as the CI for the or MPL was greater in the smaller size classes of both estimates of k in the latter did not overlap, implying that sexes (Table 2). Some individuals in Classes 3 and 4 they were significantly different. apparently did not grow between capture and recapture, Ages at Maturity. — Estimated age at maturity although this occurred more frequently in males. Four differed based upon which body measurement was used females in Class 2 did not grow and may have had either a (Table 4), as those based on CL generated greater values in lower than normal growth rate or matured at a smaller than both sexes. Estimates of female age at maturity averaged typical size, as none had reached the hypothesized size at slightly over 9 yrs and the CI of the estimates overlapped maturity (120 mm MPL) upon recapture. Although overall regardless of whether recapture data or recapture data growth apparently declined in larger turtles, variability in combined with back-calculated growth increments were growth appeared to increase with size. The coefficient of used (Table 4). Estimated male ages at maturity using only variation of change per year in CL and MPL was small in recapture data, however, were over 3 yrs greater than those both sexes for Classes 1 and 2 but increased in the larger from recapture data combined with back-calculated growth size classes, implying that variation in growth was increments (Table 4) and their CIs did not overlap, substantially higher for larger turtles relative to smaller indicating that they were significantly different. and presumably younger G. oculifera (Table 2). CJS Models. — The model that best fit recapture data Recapture data used with back-calculated CL or MPL for both sexes at most study sites was one in which growth increments provided a better fit to the VB growth estimates of both u and q were constant through time model for both sexes than did recapture data alone, as (Table 5). The best model for both sexes at Ratliff Ferry regressions using only recapture data (MI, FI) had lower and for females at Columbia, however, was one where u R2 values than those using recapture plus back-calculated was constant but q varied with sampling period. The mean data (MII, FII) in the analyses (Table 3). The CI for annual u for males was approximately 88% and for estimates of a for both sexes and both morphological females approximately 93%. The mean q for both sexes variables using only recapture data and those using was generally low, at approximately 8% for males and 5% for females (Table 5). recapture data combined with back-calculated growth Maximum and Average Longevity. — Estimated mean increments overlapped (Table 3), implying that the ML was almost 50 yrs for males and ranged from estimates did not differ regardless of the type of data approximately 29 to 68 yrs (Table 6). Mean AL of males used. Similar results occurred when estimating k in was much lower at almost 8.5 yrs and ranged from approximately 5 to 12 yrs. Estimated average ML for Table 4. Estimated ages (yrs) at maturity and their 95% CI for females was over 76 yrs and ranged from approximately male and female Graptemys oculifera. Model designations as in 59 to 88 yrs, while mean AL was almost 14 yrs and ranged Table 3. from approximately 10 to 16 yrs (Table 6). The longest Males Females period between capture and recapture for turtles first captured as adults was approximately 25 yrs in both sexes. Model Age 95% CI Model Age 95% CI If males mature at 4.6 yrs and females at 9.1 yrs (Table 4), MI CL 7.96 6.61 9.85 FI CL 9.42 8.11 11.12 these males at recapture were a minimum of almost 30 yrs MI MPL 7.90 6.59 9.71 FI MPL 8.99 7.78 10.51 old and the females were older than 34 yrs. These turtles MII CL 4.62 3.77 5.86 FII CL 9.33 8.09 10.91 MII MPL 4.51 3.69 5.70 FII MPL 8.94 7.81 10.36 may have been considerably older as there was no MI Means 7.93 FI Means 9.21 indication at initial capture in either sex that they had MII Means 4.56 FII Means 9.14 recently become mature. 220 CHELONIAN CONSERVATION AND BIOLOGY, Volume 16, Number 2 – 2017
Table 5. Cormack-Jolly-Seber (CJS) model estimates of the probabilities of survival (u) and recapture (q) of male and female Graptemys oculifera by study site. SE is the standard error of the preceding parameter estimate. The variance inflation factor (cˆ) and the quasi-Akaike’s information criterion (QAICC weight) were used to evaluate the suitability of the models (see text). CJS models that best fit the recapture data for each sex at each site are shown, where (.) indicates the estimated parameter was constant over time and (t) indicates the estimated parameter varied with recapture period.
cˆ Model QAICC weight u SE q SE Males Carthage 1.0101 u(.)q(.) 0.9036 0.8370 0.0558 0.0765 0.0296 Ratliff Ferry 1.3184 u(.)q(t) 0.8785 0.9012 0.0338 0.0855 0.0223 Lakeland 1.4057 u(.)q(.) 0.9549 0.8260 0.0479 0.0991 0.0298 Monticello 1.6421 u(.)q(.) 0.9669 0.9177 0.0302 0.0511 0.0135 Columbia 1.8089 u(.)q(.) 0.7116 0.9068 0.0598 0.0720 0.0284 Mean 0.8769 0.0751 Females Carthage 1.1016 u(.)q(.) 0.9372 0.9404 0.0371 0.0426 0.0207 Ratliff Ferry 1.0412 u(.)q(t) 0.9796 0.8996 0.0184 0.0500 0.0189 Lakeland 1.5559 u(.)q(.) 0.9727 0.9343 0.0356 0.0370 0.0144 Monticello 1.0980 u(.)q(.) 0.9856 0.9304 0.0361 0.0275 0.0109 Columbia 1.1217 u(.)q(t) 0.6911 0.9365 0.0772 0.0897 0.0310 Mean 0.9281 0.0455
Using an average adult female survival rate of 0.93 (adult males: CL r = 0.166, MPL r = 0.145; adult (Table 5), an average of 1.19 clutches/yr and an average females: CL r = 0.229, MPL r = 0.212; subadult females: clutch size of 3.17 (both from Jones 2006), and female age CL r = 0.348, MPL r = 0.343) and for adult males at of maturity of 9.14 yrs (Table 4), estimated annual juvenile Columbia (CL: r = 0.262, p , 0.001; MPL: r = 0.212, u was calculated for each site (Table 6). Assuming that p , 0.001) but not at any of the other sites. Adult G. these parameters are similar throughout the Pearl River, oculifera of both sexes from Ratliff Ferry and adult males mean estimated annual juvenile u was 0.686 and mean AL from Columbia captured after 2000 (the approximate was almost 2.7 yrs (Table 6), i.e., on average, a hatchling midpoint of the study) were significantly larger than those G. oculifera would survive 2.7 yrs. The mean instanta- captured earlier (Table 7). Immature females captured at neous mortality rate for females was slightly more than Ratliff Ferry before 2000 did not differ in size from those half that of males, while the rate for juveniles was about 5 captured after 2000, but this may have been due in part to times that of females and almost 3 times that of males the small sample size of immature females after 2000. (Table 6). Sex Ratios. — The sex ratio for G. oculifera from all Body Size Variation over Time. — For combined sites, excluding recaptures and those trapped during the study sites, there were significant correlations between 1995 1996 reproductive sampling, was male biased, as body size and date of capture for adult males (CL: was the sex ratio for turtles captured before 2000, but for r = 0.103, p , 0.001; MPL: r = 0.114, p , 0.001), adult turtles captured after 2000 the sex ratio was 1:1 (Table 8). females (CL: r = 0.152, p , 0.001; MPL: r = 0.178, There was no difference between sexes in the numbers p , 0.001), and immature females (CL: r = 0.134, p captured by month (Kruskal-Wallis H = 6.0, p = 0.423), ,0.001; MPL: r = 0.135, p , 0.001) but not for so there did not appear to be a seasonal correlation immature males (CL: r = 0.030, p =0.794;MPL: between captures and sex ratio. Considered individually, 4 r = 0.091, p = 0.425) or juveniles (CL: r = 0.073, of the 5 populations had unbiased sex ratios before 2000 p = 0.370; MPL r = 0.097, p = 0.235). All significant but all 5 populations had biased sex ratios after 2000 correlations were positive, indicating an increase in body (Table 8). size over time. Considered by study site, correlations were Population Sizes, Basking Counts, and Trapping significant (p , 0.001) for all 3 groups at Ratliff Ferry Success. — Both SM and LP population size estimates
Table 6. Estimated maximum longevity (ML), average longevity (AL), and instantaneous mortality rate (MR) of Graptemys oculifera by sex and study site, and estimated annual survival (u) and average longevity for juveniles (see text).
Males Females Juveniles Site ML AL MR ML AL MR u AL MR Carthage 28.83 5.62 0.178 83.38 16.27 0.061 0.6738 2.53 0.395 Ratliff Ferry 59.93 9.61 0.104 59.20 9.45 0.106 0.7133 2.96 0.339 Lakeland 30.30 5.23 0.191 88.38 14.71 0.068 0.6810 2.60 0.384 Monticello 68.34 11.64 0.086 72.06 13.86 0.072 0.6853 2.65 0.378 Columbia 56.31 10.22 0.098 78.81 15.24 0.065 0.6784 2.58 0.388 Means 48.76 8.47 0.131 76.37 13.91 0.075 0.6864 2.67 0.377 JONES — Ringed Sawback Turtles in the Pearl River, Mississippi 221
Table 7. Sample size (n), mean, and 1 standard deviation (in parentheses) of carapace length (CL) and midline plastron length (MPL) among age and sex classes at Ratliff Ferry and Columbia for Graptemys oculifera captured before and after 2000, with Mann-Whitney U-tests (U) of comparisons of CL and MPL among age and sex classes before and after 2000. Significant differences after adjustments for multiple comparisons are indicated by asterisks.
Before 2000 After 2000 Mann-Whitney tests
n CL MPL n CL MPL UCL UMPL Ratliff Ferry Adult male 462 88.6 (6.8) 75.6 (6.1) 103 91.7 (6.2) 77.8 (5.7) 17.42 (, 0.001)* 11.78 (, 0.001)* Adult female 741 158.5 (13.9) 137.9 (11.9) 133 166.1 (14.0) 143.6 (11.0) 40.41 (, 0.001)* 38.58 (, 0.001)* Immature female 276 109.8 (23.2) 95.7 (20.7) 17 116.3 (17.8) 100.2 (14.9) 0.98 (0.322) 0.21 (0.644) Columbia Adult male 215 87.5 (5.4) 74.2 (4.6) 76 90.7 (5.9) 76.4 (5.2) 16.06 (, 0.001)* 10.67 (0.001)* were negatively correlated with date at 4 of the 5 study slightly increasing over the duration of the study. sites (Table 9), implying that the numbers of G. oculifera Considered individually, all sites except Carthage, which at these sites declined through time. None of the SM appeared to have declined (Table 13), were relatively correlations were significant, most likely because of small stable over the study, with k estimates very close to 1. sample sizes (n = 5 in all cases) but 3 of the LP These changes were not necessarily concordant for the 2 correlations were. Mean population size estimates were sexes. Male populations appeared to be stable at all sites lower by as much as 31% after 2000 except at Lakeland, except Carthage, which decreased, while Monticello where estimates were over 50% higher after 2000 (Table appeared to exhibit a slight increase (Table 13). Female 9). populations at all sites were relatively stable, although The average density of basking G. oculifera observed Carthage, Ratliff Ferry, and Lakeland all had k estimates during the study varied from as few as 14 individuals/km slightly less than 1. The annual percentage of change in k to as many as 90 individuals/km (Table 10). Average at each site and for each sex was , 1%/yr (Table 13). numbers of basking G. oculifera observed during the study were correlated with date at 2 sites but not at the others DISCUSSION (Table 10). Basking counts before and after 2000 did not Growth. — The VB growth model has been used in a change or increased slightly at 2 sites, more than doubled number of studies, leading to a variety of opinions about at a third, but declined 25% 35% at 2 others (Table 10). how much and what types of recapture data are necessary Captures of all G. oculifera combined declined by to produce reliable estimates of the asymptotic value (a), over 36% after 2000 (Table 11). The largest decline the intrinsic growth factor (k), and age at maturity. (. 77%) was among juveniles, followed by males Dunham (1978) stated that mark–recapture data were not (. 45%) and females (almost 25%). The largest overall appropriate for the VB model if all size classes were not decline was at Carthage, where there were over 50% fewer well represented, including smaller and presumably captures/day after 2000, much of this owing to a 66% younger individuals. Martins and Souza (2008) indicated decline in the number of captured males. Captures at both that the absence of juvenile growth data when using the Ratliff Ferry and Columbia declined by about one-third, VB model resulted in underestimates of both a and k, but at Lakeland there was a small increase in the number which then led to incorrect estimates of age at maturity. of turtles captured after 2000 (Table 12). Kulmiye and Mavuti (2005) hypothesized that the 2 Pradel Models. — The k estimates averaged slightly parameters are inversely proportional, such that an . 1.0 for both sexes separately and combined (Table 13), underestimate of one results in an overestimate of the implying that on average, populations of both males and other. However, Frazer et al. (1990) found that although females and for all sites in the Pearl River were stable to the omission of larger individuals of Trachemys scripta
Table 8. Sex ratios by site for Graptemys oculifera captured during population estimate sampling and for each site before and after 2000. Ratios significantly different from 1:1 as determined by v2 tests are indicated by asterisks. All tests had 1 degree of freedom.
All captures Before 2000 After 2000 Male:female v2 p Male:female v2 p Male:female v2 p Carthage 159:158 (1:1) 0.01 0.955 134:109 (1.2:1) 2.57 0.109 25:49 (0.51:1) 7.78 0.005* Ratliff Ferry 591:608 (1:1) 0.24 0.624 484:458 (1.1:1) 0.72 0.397 107:150 (0.71:1) 7.20 0.007* Lakeland 229:283 (0.8:1) 5.70 0.017* 187:182 (1:1) 0.07 0.795 42:101 (0.42:1) 24.34 , 0.001* Monticello 462:237 (1.9:1) 72.42 , 0.001* 376:182 (2.1:1) 67.45 , 0.001* 86:55 (1.6:1) 6.82 0.009* Columbia 298:213 (1.4:1) 14.14 , 0.001* 222:178 (1.2:1) 4.84 0.028 76:35 (2.2:1) 15.14 , 0.001* All sites 1739:1499 (1.2:1) 17.79 , 0.001* 1403:1109 (1.3:1) 34.41 , 0.001* 336:390 (0.9:1) 4.02 0.045 222 CHELONIAN CONSERVATION AND BIOLOGY, Volume 16, Number 2 – 2017
Table 9. Schnabel (SM) and Lincoln-Peterson (LP) mark–resight population estimates for all study areas by sampling period, correlations (r) between population size estimates and dates of estimate, associated p-values of correlations, mean population estimates before and after 2000, and percent changes in those means. Significant correlations after adjustment for multiple comparisons are indicated by asterisks.
Carthage Ratliff Ferry Lakeland Monticello Columbia Year SM LP SM LP SM LP SM LP SM LP 1988/1989 408 440 1097 1194 689 623 837 710 633 648 1994 233 231 1095 1065 403 502 455 443 373 369 2002 499 543 1358 1378 730 771 566 601 547 480 2008/2009 321 364 822 776 774 767 366 370 166 160 2013/2014 233 226 803 778 1076 1098 452 444 396 402 r 0.32 0.14 0.56 0.46 0.74 0.60 0.74 0.48 0.60 0.35 p 0.60 0.54 0.32 0.03* 0.15 , 0.01* 0.15 0.02* 0.28 0.11 Mean estimates Before 2000 320 336 1096 1129 546 562 646 577 503 508 After 2000 351 378 994 977 860 879 461 472 370 347 % Change 9.7 12.5 9.3 13.5 57.5 56.4 28.6 18.2 26.4 31.7 underestimated a and overestimated k, the absence of earlier study (Jones and Hartfield 1995). This result likely smaller individuals had little effect on those 2 parameters. was due to greater individual variation in growth rate The addition of data derived from juveniles based on their among recaptured turtles over time in the present study (25 growth rings in the present study effectively added data yrs) relative to the earlier one (3 yrs) and because of from turtles in their first year of growth. As in an earlier greater variation in growth among larger as opposed to study (Jones and Hartfield 1995), the added data improved smaller size classes. the fit to the VB growth model for both males and females Survivorship and Recapture Probabilities. — The and had almost no effect on the estimate of a, but had a CJS model that best fit G. oculifera recapture data for both significant effect on the estimate of k in males. Without sexes and from all study areas was one in which survival these added data, k was underestimated, resulting in an was constant, relatively high, and generally lower in males overestimate of age at maturity for that sex. These results than females. Similar results have been found in other may indicate that the VB growth model is more sensitive turtle studies (e.g., Tucker et al. 2001; Bowen et al. 2004; to the absence of recapture data from very young Eskew et al. 2010; Dinkelacker and Hilzinger 2014). The individuals in either those species or sexes that mature estimate of q at all sites, however, was generally lower for earlier and at smaller sizes than those that mature later and G. oculifera than for other species (e.g., Tucker et al. at larger sizes. 2001; Ayaz et al. 2008; Martins and Souza 2008; Germano The estimates of k found here are similar to those of and Riedle 2015), although Paez´ et al. (2015) reported other species of Graptemys, which ranged from 0.264 to similar low q estimates for adult Podocnemis lewyana. 0.498 for males and from 0.110 to 0.182 for females Why recapture probabilities were so low in the present (Lindeman 1999). The recapture data, however, did not fit study is unclear. One possibility is that over time, G. the growth model in the present study as well as in the oculifera, particularly marked turtles, may have learned to
Table 10. Means and 1 standard deviation (in parentheses) of numbers of basking Graptemys oculifera by sampling period at the 5 study sites, mean density of basking G. oculifera per river kilometer, correlations (r) between numbers of basking turtles and count dates, associated p-values of the correlations, mean numbers of basking turtles and mean densities for the entire study and before and after 2000, and percent change in numbers of basking turtles and turtle densities before and after 2000. Significant correlations, after correction for multiple comparisons, are indicated by asterisks.
Carthage Ratliff Ferry Lakeland Monticello Columbia Year Mean Density Mean Density Mean Density Mean Density Mean Density 1988/1989 69 (0.7) 14 196 (6.4) 61 141 (40.1) 29 194 (39.9) 40 77 (17.7) 16 1994 78 (9.3) 16 298 (48.1) 93 92 (40.1) 19 124 (19) 26 88 (18.3) 18 2002 81 (8.5) 17 361 (44.6) 113 224 (40.9) 47 117 (63.1) 24 95 (49.4) 20 2008/2009 86 (24.3) 18 343 (70.9) 107 257 (86.1) 53 94 (8.8) 20 30 (9.3) 6 2013/2014 62 (15.5) 13 188 (51.1) 59 228 (49.2) 48 96 (33.5) 20 62 (17.7) 13 r 0.13 0.11 0.64 0.63 0.43 p 0.56 0.66 , 0.001* 0.001* 0.05 Entire study 76 (16.4) 16 289 (86.4) 90 190 (79.8) 40 122 (48.9) 25 69 (35.2) 14 Before 2000 75 (8.9) 16 269 (63.7) 84 114 (40.1) 24 155 (46.1) 32 85 (17.5) 18 After 2000 76 (19.3) 16 299 (95.8) 93 236 (59.3) 49 102 (39.9) 21 62 (39.4) 13 % Change 1.3 0 11.2 10.7 107.0 104.2 34.2 34.4 27.1 27.8 JONES — Ringed Sawback Turtles in the Pearl River, Mississippi 223
Table 11. Mean numbers of Graptemys oculifera trapped per day for the entire 25-yr study, by individual study area and by age/sex class as a whole, both before and after 2000, and the percent change between those time periods.
Study areas Age/sex class All areas Carthage Ratliff Ferry Lakeland Monticello Columbia Juveniles Males Females Captures/day 20.68 14.4 42.3 16.8 23.1 19.9 0.93 10.60 9.14 Before 2000 23.25 17.9 47.2 16.7 24.8 21.9 1.22 12.31 9.73 After 2000 14.80 8.8 31.6 17.3 18.3 14.6 0.28 6.72 7.80 % Change 36.34 50.9 33.2 4.0 26.1 33.1 77.01 45.41 24.74 avoid traps. This seems unlikely as there were no (Jones 1996). If G. oculifera has home range lengths significant correlations between date and the number of similar to those of G. flavimaculata, then it is unlikely that recaptured males, recaptured females, or all recaptured substantial numbers of marked individuals moved outside turtles combined. Chicken wire traps were used exclu- of the 5 study areas because all were 4.8 km in length sively in the early years of the study and crayfish wire later except that at Ratliff Ferry, which was 3.2 km long. as the latter is more durable and easier to use than the Although some Graptemys have been recorded moving former. A crayfish wire trap, however, appears to be more . 5 km (summarized in Lindeman 2013), there is no visible when deployed than a chicken wire trap, particu- evidence that a large proportion of a population of any larly in clear water, and thus may have been recognizable species periodically moves to new areas. It should be as something to avoid, particularly to marked turtles. Davis noted, however, that there are no movement studies in and Burghardt (2012) documented long-term memory Graptemys that have lasted for longer than 1 2 yrs, so capabilities involving visual discrimination tasks in average movements over a period of time that is short Pseudemys nelsoni and T. scripta and Soldati et al. relative to the lifespan of an individual may differ from (2017) found that Chelonoidis carbonarius were able to movements over a longer time period. discriminate between visual stimuli representing differen- The best CJS model for females at Columbia and for tial reward values and retained that ability for at least 18 both sexes at Ratliff Ferry had q values that varied with mo, so it is possible that marked G. oculifera may have sampling period, while in all other populations q values learned to recognize and avoid traps. were constant. For Ratliff Ferry females, this likely was a Another possibility is that some of the turtles captured result of the intensive sampling during the reproductive and marked were transients in the study areas and were not study at that site in 1995 1996 (Jones 2006). During that available for recapture in subsequent sampling periods. If study, trapping directed at females was conducted 4 d/wk that were the case, it is likely that their presence would for 10 wks/yr, resulting in almost as many females have been reflected in low survival probabilities (Sasso et captured and marked (559) as were captured during the al. 2006) in each of the populations. Marked turtles might rest of the study (608). Of the 559 captured in 1995 1996, also have periodically moved short distances away from 99 (18%) were recaptured, while only 57 (9%) of the 608 and then back to the study areas and thus were only females captured during the rest of the study were periodically available for recapture. Shealy (1976) found recaptured. The large number of females captured during what he described as significant movement of marked the reproductive study and later recaptured appears to have Graptemys ernsti away from a favorable trapping area but resulted in a CJS best fit model for females at Ratliff Ferry implied that these large-scale movements were to other with a variable q. Removing females captured in favorable areas only a few hundred meters away. Although 1995 1996 from the Ratliff Ferry analysis resulted in a there are no published data on movement in G. oculifera,a best fit CJS model with a constant q, further supporting radiotelemetry study of the closely related Graptemys this hypothesis. flavimaculata found that mean home range lengths of The variable q values for females at Columbia and males and females were 1.8 and 1.5 river km, respectively males at Ratliff Ferry appear to have resulted from very
Table 12. Mean numbers of Graptemys oculifera trapped per day by age/sex class for each study area as a whole, before 2000, and after 2000, and percent change between those times for sex/age classes in each study area. j = juvenile.
Carthage Ratliff Ferry Lakeland Monticello Columbia Male Female j Male Female j Male Female j Male Female j Male Female j Entire study 5.7 5.7 1.0 18.4 19.0 2.2 6.2 7.6 0.5 12.8 6.6 0.4 9.6 6.9 0.7 Before 2000 7.4 6.0 1.1 22.0 20.8 3.2 6.9 6.7 0.4 14.5 7.0 0.4 10.6 8.5 0.6 After 2000 2.5 4.9 0.8 10.7 15.0 0.0 4.2 10.1 0.2 8.6 5.5 0.3 7.6 3.5 0.1 % Change 66.2 18.3 27.3 51.4 27.9 100 39.1 50.8 50.0 40.7 21.4 25.0 28.3 58.8 83.3 224 CHELONIAN CONSERVATION AND BIOLOGY, Volume 16, Number 2 – 2017
Table 13. Realized population growth (k), 95% confidence limits of k, and annual percentage of change in k for each study area.
Male Female Site means k 95% CI Annual %Dk k 95%CI Annual %Dk k 95% CI Annual %Dk Carthage 0.906 0.836 0.983 0.395 0.986 0.951 1.022 0.056 0.945 0.898 0.995 0.226 Ratliff Ferry 1.001 0.873 1.171 0.004 0.993 0.858 1.149 0.028 1.001 0.906 1.106 0.004 Lakeland 1.020 0.886 1.174 0.079 0.976 0.884 1.076 0.097 0.997 0.918 1.083 0.012 Monticello 1.104 0.833 1.462 0.396 1.070 0.916 1.250 0.271 1.086 0.933 1.265 0.330 Columbia 0.992 0.864 1.138 0.032 1.017 0.854 1.209 0.067 1.004 0.906 1.113 0.016 Means 1.010 0.935 1.090 0.010 1.007 0.949 1.067 0.031 1.008 0.961 1.057 0.022 low numbers recaptured at those sites during the latter part tions), implying a relative increase in females in some of the study. No marked males at Ratliff Ferry were areas later in the study. recaptured after 1994, even though 504 males were Differences in ages of maturity between the sexes may marked there before 2002, 548 before 2008, and 577 have been partly responsible for some of the observed sex before 2013. At Columbia, no marked females were ratios, particularly at Monticello, which was male biased recaptured in 2009 and only 1 marked female was both before and after 2000. However, the changes in all recaptured in 2014, even though there were 191 and 201 populations after 2000 were likely influenced by additional marked females in that population in 2009 and 2014, factors. Although not yet experimentally confirmed, it is respectively. probable that the sex of hatchling G. oculifera is Many turtle demographic studies, including the determined by incubation temperature. In most species of present study, do not have recapture data suitable for Graptemys, cooler incubation temperatures produce males reliable estimates of juvenile survival rates and longevity and warmer temperatures produce females (Bull et al. (e.g., Tucker et al. 2001; Martins and Souza 2008). In 1982; Ewert and Nelson 1991; Ewert et al. 1994). If those studies that dealt specifically with juvenile survival warmer incubation temperatures occurred later in the (summarized in Iverson 1991; Shoemaker et al. 2013; study, more female than male hatchlings may have been Dinkelacker and Hilzinger 2014), estimates ranged from produced, thus altering observed sex ratios after 2000. 0.48 to 0.70, so the average estimate calculated here (0.69) However, there were few hatchlings captured after 2000, is within the range of estimates from those earlier studies. implying either a decrease in nesting success or in Longevity. — The estimate of ML for male G. hatchling survival, and without an influx of younger oculifera was approximately 64% of that of females and turtles, it appears unlikely that increased incubation was similar to estimates calculated in the same way for temperatures could have influenced sex ratios in these Clemmys guttata, in which the ML of males was populations, nor does it explain the relative increase in the approximately 59% of that of females (Litzgus 2006). number of males at Columbia. It is also unlikely that the The variation in ML estimates among populations in the sexes had differential emigration or immigration rates present study appears to have resulted from variation in based on what is known about movement in the closely survival estimates rather than in population sizes, as related G. flavimaculata as discussed earlier. The CJS calculations of longevity were more sensitive to variation models indicated that male G. oculifera generally had a in the former than in the latter. Estimates of AL were lower survival rate than females, which in the absence of overall much lower than ML estimates and support recruitment, could result in a female-biased sex ratio over Gibbons’ (1987) statement that although some individuals time. However, given the relatively long potential lifespan in a population may live a long time, most do not. of male G. oculifera relative to the length of the study, it is Sex Ratios. — Gibbons (1990) hypothesized that most unclear whether a simple difference in average survival variation in turtle sex ratios could be ascribed to 1 of 4 rates between the sexes would have acted quickly enough causes: 1) the initial sex ratio of hatchlings, 2) differential to have accounted for the changes in sex ratios after 2000. mortality between the sexes, 3) differential emigration or It seems more likely that these changes resulted from immigration rates of the sexes, or 4) differences in ages at either a decrease in the numbers of males or an increase in maturity. He considered the last to be a primary cause of the numbers of females in these populations after 2000. biased sex ratios in some turtles, including species like G. The numbers of both sexes captured per day declined oculifera, in which males mature at an earlier age and during the study, so it is unlikely that female-biased sex would thus be expected to outnumber females, other ratios resulted from an increase in female numbers. The factors being equal, in a population sample. Prior to 2000, largest declines among captured sexable turtles overall and both the overall sex ratio and that of 1 population in the in most populations during the study were among males, present study were male biased while the other 4 so it appears that the sex ratio changes were more likely populations were unbiased. After 2000, the overall sex owing to fewer males present after 2000. Dorcas et al. ratio became equal and individual study area ratios were (2007) found a change to a female-biased sex ratio in female biased (3 populations) or male biased (2 popula- Malaclemys terrapin that was attributed to the effects of JONES — Ringed Sawback Turtles in the Pearl River, Mississippi 225 differential bycatch by crab traps selective for the smaller impact on the population dynamics and life history of G. males and differential predation on females was suggested oculifera, as hypothesized for other species of turtles by as the cause of biased sex ratios in Gopherus agassizii Semlitsch and Gibbons (1989). (Esque et al. 2010). In the present study, the changes in sex The number of female G. oculifera captured per day ratios may have resulted from greater rates of predation on at Columbia declined by almost 60% after 2000, which the smaller male G. oculifera. was over twice the rate of decline in male captures. This If, as hypothesized, increased predation on male G. was contrary to what occurred in other populations, where oculifera was responsible for the changes in sex ratios, male decline was greater than that of females. The reason what species may have been responsible? It is unlikely that for this is unclear. It is unlikely that predation was any fish in the Pearl River would have been involved, as involved because that would require a predator that would none of the known species in the watershed are large substantially reduce the female population at Columbia but enough to present a significant threat to immature or adult not at the other study sites. The low numbers of females male G. oculifera. Males are rarely found on land and are captured at the Columbia site, as discussed for female G. not usually exposed to predation from terrestrial mammals. pearlensis (Selman and Jones 2017), may have resulted The only aquatic mammal that occurs in the Pearl River from geomorphic changes to the river channel resulting in watershed which is large enough to be a predator of G. less than suitable habitat for females, through increased oculifera is the northern river otter (Lutra canadensis). recreational usage of this part of the Pearl River, or Otters are known predators of turtles (e.g., Liers 1951; because there may have been illegal collecting directed Lanszki et al. 2006; Ligon and Reasor 2007; Platt and primarily toward females at this site. Rainwater 2011; Stacy et al. 2014); their impact on The decline in captured juveniles was greater than that populations may range from very low (e.g., Greer 1955; in either males or females, which may have resulted not Noordhuis 2002; Roberts et al. 2008) to moderate (e.g., only from increased direct predation but also from the Manning 1990; Brown et al. 1994; Roberts et al. 2008) to effects of increased nest predation. Major nest predators of substantial (Brooks et al. 1991). River otters, however, are G. oculifera are raccoons (Procyon lotor), armadillos not common in the Pearl River and neither they nor their (Dasypus novemcinctus), and fish crows (Corvus ossifra- tracks, scat, or slides were observed in any of the study gus; Jones 2006). These are all subsidized predators, i.e., areas, so it is unlikely that they caused the decline in male predators whose populations have benefited directly or G. oculifera. Bald eagles (Haliaeetus leucocephalus) also indirectly from human activities resulting in population prey on turtles (Clark 1982; Grubb 1995), including densities higher than natural levels (Gompper and Vanak Graptemys (Mabie et al. 1995) but there are fewer than 10 2008). Fish crows and armadillos expanded their ranges in breeding pairs of this species in the entire Pearl River Mississippi prior to 1995 (Jones 2006) and both of these watershed in Mississippi (N. Winstead, pers. comm., species as well as raccoons appear to have increased their August 2017), so it is unlikely that they had an impact on populations since then, so it is possible that they are now G. oculifera populations. having greater impacts on G. oculifera nesting success. A predator that did increase during the study was the Increased recreational activity at some sites, particularly American alligator (Alligator mississippiensis). When the Ratliff Ferry, may also have impacted nesting success and study began in the late 1980s, alligators were listed as juvenile recruitment. Sandbars are the primary nesting endangered in Mississippi and were infrequently encoun- habitats of G. oculifera (Jones 2006), but are also prime tered during sampling. Populations of A. mississippiensis recreational sites on the Pearl River, and increased human have increased substantially since then to the point that the use of sandbars has been associated with reduced nesting species was removed from the state endangered species list attempts by G. oculifera (Jones 2006). Recreational use of and a sport hunting season was initiated in 2005. sandbars often results in the deposition of food refuse from Lindeman (2008) hypothesized that alligators prefer more picnicking and camping. These sources of anthropogenic lentic waters than those normally occupied by Graptemys, foods may attract fish crows and raccoons, so increased but in the Pearl River both species were frequently recreational use of the Pearl River sandbars may not only observed in the same riverine habitats during the latter part result in reduced nesting attempts but also increased nest of the study. Alligators are known predators of turtles predation by attracting additional predators to nesting (Valentine et al. 1972; Delany and Abercrombie 1986) and habitat. would presumably capture and eat G. oculifera if they Population Trends.—Basedonthek estimates, the were available. This would likely impact not only males Pearl River population of G. oculifera as a whole remained but immature females and juveniles as well, but would not relatively stable over the course of the 25-yr study, as have impact adult females to the same degree, as the latter are populations at 4 of the 5 study sites. It should be noted that larger and thus would be more difficult to eat for smaller k estimates are summaries of what happened in the past alligators. Females also appear to be more wary and able to rather than forecasts of what will happen in the future. Other swim more rapidly than either males or juveniles (R.L.J., lines of evidence, including those parameters that were pers. obs.). Although there are no studies of their diets in statistically different over time and those that, although not the Pearl River, alligators may have had a significant statistically different, exhibited trends that were consistent 226 CHELONIAN CONSERVATION AND BIOLOGY, Volume 16, Number 2 – 2017 over time and across sites, may be necessary to predict the avoid certain types of traps. A radiotelemetry study of G. fate of Pearl River populations of G. oculifera. Population oculifera would assist in determining home range sizes estimates and basking counts, for example, generally and short-term movements in the species. Nesting at trended downward at all sites except Lakeland. Trapping Ratliff Ferry should be reinvestigated to determine if nest success also trended downward at all sites, including predation rates have remained the same or, as suspected, Lakeland, but the decrease there was relatively small increased because of an increase in subsidized predators compared with other sites. The downward trend in trapping correlated with increased recreational use of sandbars. success was not uniform across age and sex classes, as the Reproduction should also be monitored at one or more of largest decreases were in juveniles, followed by males, and the other populations to determine if and by how much then by females, nor were these trends concordant among nesting success differs from that at Ratliff Ferry. Food sites. Additionally, males and females at Ratliff Ferry and habits of alligators in the Pearl River should also be males at Columbia captured after 2000 were significantly investigated to determine if they actually do eat significant larger than those trapped before that date, implying that numbers of G. oculifera. those 2 populations, particularly at Ratliff Ferry, are Graptemys oculifera, although still relatively abun- composed of older individuals. dant, is slowly declining over much of its range in the Based on these trends, it appears that 4 of 5 study Pearl River. One of the difficulties in managing a species populations of G. oculifera in the Pearl River have either like G. oculifera is that a long lifespan in concert with a already declined (Carthage) or are in the early stages of slow decline may mean that population and demographic decline (Ratliff Ferry, Monticello, Columbia), while the changes are not conspicuously evident. Wildlife managers, population at Lakeland appears to be stable to increasing. particularly those accustomed to working with relatively Dorcas et al. (2007) found an overall decline in several short-lived species, may not immediately notice these populations of M. terrapin, a shift to larger body sizes and changes and assume that the species is stable. Continued older turtles, and a change to a female-biased sex ratio, all monitoring of Pearl River G. oculifera over the long term changes that are very similar to what was found in the will be important in determining whether the apparent present study. In both studies, the primary cause appears to decline continues or if populations stabilize at some point be differential loss of individuals related to body size, in the in the future. first case based on trapping mortality and in the present case because of predation, presumably by alligators, which were ACKNOWLEDGMENTS once nearly extirpated in the Pearl River but which now Partial funding was provided by the US Fish and have recovered and are assumed to be approaching Wildlife Service, Project No. E-1, under a Section 6 historical levels. There are no data, however, on population Cooperative Agreement with the Mississippi Department levels of G. oculifera prior to the decline of the alligator in of Wildlife, Fisheries, and Parks, which also permitted the Mississippi. The assumption that G. oculifera population capture and marking of this species. Field assistance sizes observed in the late 1980s were normal for the species during the early part of the study was provided by P.D. may be a hypothesis analogous to the shifting baseline Hartfield, T.C. Majure, J.B. Wiseman, Jr., and T.L. syndrome in fisheries (Pauly 1995; Pinnegar and Engelhard Vandeventer. The constructive comments of 3 anonymous 2008), where base stocks observed at the beginning of a reviewers greatly improved an earlier draft of this fisheries scientist’s career are assumed to be normal for a manuscript. species and are used to evaluate subsequent changes. In the absence of alligator predation prior to the 1980s, did G. LITERATURE CITED oculifera populations increase to higher than normal levels? ARMSTRONG, D.P. AND EWEN, J.G. 2013. Consistency, continuity Is the decline of G. oculifera observed in the present study and creativity: long-term studies of population dynamics on evidence of population levels adjusting to the increased Tiritiri Matangi Island. 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