Population Structure, Status, and Conservation of Two Species from the Pearl River, Author(s): Will Selman and Robert L. Jones Source: Journal of Herpetology, 51(1):27-36. Published By: The Society for the Study of Amphibians and DOI: http://dx.doi.org/10.1670/15-082 URL: http://www.bioone.org/doi/full/10.1670/15-082

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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. Journal of Herpetology, Vol. 51, No. 1, 27–36, 2017 Copyright 2017 Society for the Study of Amphibians and Reptiles

Population Structure, Status, and Conservation of Two Graptemys Species from the Pearl River, Mississippi

1,2,3 4 WILL SELMAN AND ROBERT L. JONES

1 Department of Biological Sciences, University of Southern Mississippi, 118 College Drive, 5018, Hattiesburg, Mississippi, USA 2 Department of Biology, Millsaps College, 1701 North State Street, Jackson, Mississippi, USA 4Mississippi Department of Wildlife, Fisheries, and Parks, Museum of Natural Science, 2148 Riverside Drive, Jackson, Mississippi, USA

ABSTRACT.—Graptemys is one of the least studied genera in North America. Graptemys oculifera (Ringed Sawback) and Graptemys pearlensis (Pearl Map Turtle) are endemic to the Pearl River system of Mississippi and southeastern . We studied both species near Columbia, Mississippi, on the Pearl River via a trapping and basking surveys over two years. Additionally, five sites including Columbia were trapped for 27 years to determine long-term trends in capture success and relative abundance (RA). At the Columbia site, body size distribution was bimodal for G. oculifera and atypically unimodal for G. pearlensis; G. pearlensis body lengths were smaller than museum specimens. Population estimates for G. oculifera at the Columbia site indicate a stable population over 25 years. Long-term RA trends indicated that G. pearlensis was less common than G. oculifera in all periods and at all sites from 1988 to 2013. Trends in long-term capture success for G. oculifera and G. pearlensis were negative at all sites, with significant declines at three sites for both G. oculifera and G. pearlensis. Declines occurred both upstream and downstream of a major reservoir. Therefore, a combination of factors (including altered hydrology, human disturbance, lack of recruitment, excessive sedimentation, impaired water quality, and/or the pet trade) appear to be contributing to declines. Additional conservation and protection is warranted for G. pearlensis, and current protections for G. oculifera should be extended. Future studies should continue at our long-term sites to determine whether population declines persist or whether populations stabilize.

Understanding wildlife population sizes and demography are either G. pulchra (sensu lato; Lovich and McCoy, 1992) or G. central tenets for species conservation efforts; however, these gibbonsi (sensu lato; Ennen et al., 2010); 2) it was perceived to data are lacking for many southeastern freshwater turtle species need less conservation attention, because it was not a drainage to aid in conservation efforts. In particular, Graptemys (map endemic as either G. pulchra (sensu lato) or G. gibbonsi (sensu and sawbacks) is considered one of the least studied lato); and 3) it was overshadowed by the federally threatened turtle genera in North America (Lovich and Ennen, 2013); yet status of G. oculifera. The latter directed more funding resources many species within the are of conservation concern toward G. oculifera research to understand basic life-history and (Buhlmann and Gibbons, 1997; van Dijk et al., 2014) and lack ecological characteristics, with data for G. pearlensis only basic life-history information (Lindeman, 2013). Further, most of collected secondarily. the species solely inhabit riverine environments and associated The first objective in this study was to document in-depth water bodies (e.g., oxbows and bayous), with nine of the 14 population structure and densities of both G. oculifera and G. species endemic to single river drainages of the Gulf of Mexico pearlensis at one site on the lower Pearl River of southern (Lindeman, 2013). Many of the endemic Gulf Coast Graptemys Mississippi. The second objective was to examine trends in are considered the least understood within the group (Lovich trapping success (i.e., catch per unit effort, CPUE) and relative and Ennen, 2013). abundance (RA) at five sites throughout the Pearl River system Two such species, Graptemys oculifera (Ringed Sawback; Baur, in Mississippi for 27 yr. The third goal was to compare the data 1890) and Graptemys pearlensis (Pearl Map Turtle; Ennen et al., collected in this study to historical data for both species within 2010), occur sympatrically in the Pearl River system of central the drainage. Mississippi and southeastern Louisiana. Considerable knowl- edge is available for G. oculifera including population densities (Jones and Hartfield, 1995; Dickerson and Reine, 1996; Linde- MATERIALS AND METHODS man, 1998; Shively, 1999), population structure (Jones and Hartfield, 1995), reproductive ecology (Jones, 2006), and Study Sites.—For the detailed demographic study, we conduct- population genetics (Gaillard et al., 2015). Most of this ed fieldwork on 8.3 river kilometers (rkm) of the Pearl River near information was made possible because the species was listed the town of Columbia (Marion County, MS; Fig. 1). The as federally threatened in 1986 (USFWS, 1986) and with the Columbia site is characteristic of a medium-sized (~75–175 m undertaking of proposed studies outlined in the G. oculifera wide), Gulf Coastal Plain river, with alternating pointbar and recovery plan (Stewart, 1988). Most of the available data for G. cutbank sections, abundant submergent and emergent dead- pearlensis, however, is coincidental to visual population density wood snags, and a sand and gravel substrate. The flow of the 3 surveys focused on G. oculifera (Dickerson and Reine, 1996; Pearl River (discharge: 24–1700 m /sec) is primarily regulated by Lindeman, 1998; Shively, 1999), with all data reported prior to the Ross Barnett Reservoir spillway, ~240 rkm upstream from the its recognition as a separate Graptemys taxon (Ennen et al., 2010). site. The site is surrounded by riparian bottomland forest (i.e., Presumably, the lack of data available for G. pearlensis is because Water Oak [Quercus nigra], Baldcypress [Taxodium distichum], 1) it previously had a much wider range when considered as Sycamore [Platanus occidentalis], Spruce Pine [Pinus glabra]), as well as a small amount of pasture land and a small number of 3Corresponding author. E-mail: [email protected] fishing camps. The eastern bank at the southern end of the site is DOI: 10.1670/15-082 bordered by a local park, which is a county-maintained and - 28 W. SELMAN AND R. L. JONES

FIG. 1. The geographic location of the Pearl River in the southeastern United States (top inset) and map of sample sites in central Mississippi (bottom). Cross-hatching represents areas where Graptemys oculifera and Graptemys pearlensis co-occur, whereas stippling represents upstream areas only occupied by G. pearlensis (based on maps by Lindeman, 2013) and new records of Lindeman (2014a, b). operated park with a boat launch, ball fields, and pavilions. (Lakeland, Monticello, Columbia). These study sites are Boating levels on the river are relatively low even though the described in more detail by Jones and Hartfield (1995). boat ramp provides river access. Short-Term Study.—During 2005–2006, Graptemys species were For the long-term study (1988 and 2014), we trapped over trapped at the Columbia site for 2–4 days per month from April to October. We trapped turtles by attaching open topped basking multiple sampling periods, not including the 2005/2006 traps (made of 3/4-inch PVC coated crawfish wire; Fish Net trapping at Columbia described below. This includes at the Company, Jonesville, LA) to emergent deadwood and left them Columbia site (N = 6 sampling periods) and four other sites— slightly submerged (Selman et al., 2012). Traps varied in size Carthage (6), Ratliff Ferry (7), Lakeland (7), and Monticello (7)— (from 56 · 46 · 31 cm to 122 · 61 · 25 cm) and were attached to determine long-term trends in species CPUE and RA (Fig. 1). with nails and cotton twine to known Graptemys basking logs or Two sites are located upstream of the Ross Barnett Reservoir branches used by both sexes and different size classes. Trap sites (Carthage, Ratliff Ferry), and three sites are located downstream were later approached rapidly via motorized boat, which startled PEARL RIVER GRAPTEMYS STATUS AND CONSERVATION 29 basking turtles into the traps. A maximum of 17 traps were used 1996), because it did not require uniquely marked turtles, and during a trap-day, and each trap was checked approximately additional marked individuals could be added to the popula- every hour; traps were occasionally adjusted because of tion between survey intervals. fluctuating water levels or moved if turtles avoided the trap site. For the long-term study, we used a linear regression to Turtles also were captured opportunistically by hand or by dip analyze the RA of G. pearlensis for all sites over the 27-yr time net. period; G. oculifera RA trend would be the inverse relationship. After capture, male G. oculifera turtles were determined by We also used linear correlations to analyze daily capture success smaller body sizes and longer foreclaws, taller carapacial spines, over the 27-yr period for both species at all sites. We used JMP and longer tails (Jones and Selman, 2009). Graptemys pearlensis 9.0 for all statistical analyses (SAS Institute, Inc., Cary, NC, males were smaller, did not have a greatly enlarged head, and http://www.jmp.com) except for the linear correlations for had longer tails compared to females (Lovich et al., 2009). daily capture success where we used SYSTAT (Systat Software, Midline plastron length (PL) was measured to the nearest Inc., Chicago, IL; http://www.Systat.com). millimeter with tree calipers, and body mass (in grams) was measured with a hanging scale (Ohaus, Parsippany, NJ). We RESULTS palpated females to determine their reproductive status and permanently marked turtles with holes drilled into marginal Short-Term Study.—Turtles were captured on 33 trapping days scutes (Cagle, 1939). During October in 2005 and 2006, we at the Columbia site across 13 months (April through October) in marked G. oculifera on the carapace (second and third vertebral 2005 and 2006. This excludes September 2005 immediately t scutes) with a waterproof, tree-marking spray paint (Aervoe following Hurricane Katrina. During this period, 198 G. oculifera Lead-Free Fluorescent Glo Spray Paint, Gardnerville, NV) for (107 M, 91 F) and 39 G. pearlensis (28 M, 10 F, 1 juvenile) were subsequent mark–resight surveys. captured. We also conducted basking density surveys at the Columbia Graptemys oculifera exhibited a typical bimodal size class site for G. oculifera in October 2005 and for both Graptemys distribution (Fig. 2), with females attaining significantly greater species in October 2006. The site was surveyed by walking size than that of males (t197 =-34.88, P < 0.0001) and strong sandbars from the downstream end to the upstream end using a female-biased sexual-size dimorphism (SDI = 0.67; Table 1). The 60 mm, 15–45X spotting scope with tripod to locate basking sex ratio of G. oculifera did not deviate from equality (v2 = 1.13, turtles. Population densities were calculated by counting the df = 1, P = 0.29). The mean size for gravid G. oculifera females number of turtles observed and dividing it by the total length of was 12.9 cm PL (N = 10; range: 11.6–14.0 cm PL), with all gravid river surveyed (2.75 rkm); the midriver distance was measured females captured between early May (10 May 2006) and mid- using the GoogleEarth path measuring tool (v. 6.1; Google, Inc., July (14 July 2005). Mountain View, CA). In 2006, RA was calculated for only Graptemys pearlensis exhibited an atypical unimodal size class Graptemys species, but other basking species are reported. distribution, primarily associated with a small number of female During all surveys, paint-marked G. oculifera were resighted, captures (N = 10) across a wide range of size classes (PL range: and all surveys were completed within two weeks of the initial 11.2–18.2; Fig. 2). Female G. pearlensis attained significantly paint mark application to assure that no paint marks were lost greater size than males (t36 =-5.63, P = 0.0003; Table 1) and (Selman and Qualls, 2008; Kornilev et al., 2012). also exhibited strong female-biased sexual size dimorphism Long-Term Study.—Along with the detailed data collected at the (SDI = 0.88). The sex ratio of G. pearlensis was significantly Columbia site during 2005 and 2006, Graptemys were trapped at skewed toward males (v2 = 8.8, df = 1, P = 0.0029). No gravid five sites between 1988 and 2014 to document long-term CPUE G. pearlensis females were captured, with only 3 moderately and RA trends using similar trapping methods described above. sized, nongravid females (13.7, 17.0, 18.2 cm PL) captured Each day, we used 28 to 30 traps throughout the entire study and between May and July for both years. used a mean of 29 traps/day for calculations. We tallied the For October basking surveys, mean basking densities of G. number of captured G. oculifera and G. pearlensis, along with oculifera in 2006 were nearly double those observed in 2005 morphological data for G. oculifera as described elsewhere (Jones (2005 mean: 36.5 per rkm, 2006 mean: 62.1 per rkm; Table 2). and Hartfield, 1995; Jones, 2006). These data permitted us to Even though basking densities showed high variability across calculate yearly and daily CPUE and RA for each species at each the two survey years, population estimates via mark–resight site. The former method permits comparisons of densities over methods were nearly identical (Table 2). Graptemys oculifera RA time, whereas the latter method has been used in other studies as in 2006 was high (mean: 0.79, range: 0.79–0.80), and they were an indicator of species rank abundance relative to other the dominant basking turtle species at the site. sympatric species (Lindeman, 1998, 1999, 2013). Population estimates for G. pearlensis via mark–resight could Statistical Analyses.—For the short-term study at the Columbia not be completed because we were unable to capture and paint- site, we used t-tests for both species to compare male and female mark enough individuals in a short period of time to meet the plastron lengths. To determine the degree of sexual size assumption of a closed population; however, G. pearlensis mean dimorphism for each species, we calculated the sexual dimor- basking density in 2006 was 16.1 per rkm (range: 14.9–18.1 per phism index (SDI; Lovich and Gibbons, 1992): rkm), and G. pearlensis RA (mean: 0.21, range: 0.20–0.22) was  Mature female PL much lower than that of G. oculifera. Other turtle species SDI= -1: Male PL observed in 2006 surveys include concinna (; mean density = 10.3 per rkm), scripta (Slider We use a Chi-square contingency table to determine whether Turtle; 0.6 per rkm), carinatus (Razorback Musk populations deviated from a 1 : 1 sex ratio. Population size Turtle; 0.6 per rkm), and sp. (softshell turtle species; 0.2 estimation via mark–resighting of paint-marked G. oculifera was per rkm). completed in 2005 and 2006. Similar to methods used by Selman Long-Term Study.—Between 1988 and 2013, RA was much and Qualls (2008, 2009), we used program NOREMARK (White, greater for G. oculifera than for G. pearlensis at all five sites and 30 W. SELMAN AND R. L. JONES

for both species only at the Columbia site (Table 3). For these two sites, RA was highly skewed toward G. oculifera (Monticello: 0.78–1.0; Columbia: 0.67–0.73) relative to G. pearlensis (Monticello: 0.22–0.0; Columbia: 0.27–0.33). With all sites considered through- out the study, the RA trend for G. pearlensis was negative but not significant (F1,36 = 0.52, P = 0.47). Comparisons of the two long-term data sets indicate that RA and CPUE did not always align (Fig. 3A, 3B). Both data sets indicated declining trends for G. pearlensis at Ratliff Ferry, Lakeland, and Columbia, but RA and CPUE data did not align at Carthage (CPUE–ns decline; RA–increase) or Monticello (CPUE–ns decline; RA–stable). Both RA and CPUE data indicated declines for G. oculifera at Carthage but did not align at Ratliff Ferry (CPUE–sig decline; RA–increase), Lakeland (CPUE–ns decline; RA–increase), Monticello (CPUE–ns decline; RA–stable), or Columbia (CPUE–sig decline; RA–increase).

DISCUSSION

Short-Term Study.—When comparing our G. oculifera data to Jones and Hartfield (1990, 1995) at the same Columbia site using the same basking trap methods, mean body lengths for both males and all females are slightly greater, but the SDI for this study (0.67) is similar to that of 1990 (0.70; Jones and Hartfield 1995). We captured no unsexable juveniles in 198 captures (0%) in 2005/2006, compared to 15 juveniles in 362 captures in 1989/ 1990 (4%; Jones and Hartfield 1995). This appears to be an aging population attributable to limited recent recruitment as evi- denced by larger adult body sizes and a lack of juveniles compared to 25 yr prior. Very few G. pearlensis were captured to accurately document population structure at the Columbia site, and no gravid females were sampled, although no other prior data are available to compare either of these metrics. Male G. pearlensis mean (7.4 cm PL) and maximum body lengths (9.2 cm PL) were small compared to larger males observed in other localities (pers. obs.) and in museum collections (Ennen et al., 2010; P. Lindeman, pers. comm.). Even more noticeable was the low numbers of female captures (N = 10 over 2 yrs) with no

FIG. 2. Number of captures for different size classes of Graptemys definitive size class distribution. Similar to males, female G. oculifera (top) and Graptemys pearlensis (bottom) from the Columbia site pearlensis mean (14.1 cm PL) and maximum body lengths (18.2 (Marion County, MS). Unknown sex juveniles are in black, males in light cm PL) were small compared to females from other locations gray, and females in dark gray. The black arrows indicate the size classes throughout the Pearl River system (pers. obs.) and museum of gravid females in G. oculifera found at the site and the smallest gravid female G. pearlensis found by Cagle (1952). specimens (P. V. Lindeman, pers. comm.; Table 1). For the latter, Ennen et al. (2010) noted the maximum size for a G. pearlensis female was 29.5 cm CL, which equates to ~25 cm PL (based on a across all years (Table 3, Fig. 3). The northernmost site near mean 0.85 PL:CL ratio for the 10 females in this study); this Carthage had declining CPUE trends for both Graptemys species, would be approximately 40% greater than the largest individual but the G. oculifera trend of decline was significant (Table 3). encountered at the Columbia site (18.2 cm PL). Particularly Carthage, however, had the most equitable ratios between the lacking at the Columbia site were the reproductive size classes two species, but G. oculifera RA (0.69–0.83) was always greater (N = 3; 16.9 cm, 17.5 cm, 18.2 cm) as defined by Cagle (1952; than that of G. pearlensis RA (0.17–0.31). The next site >17 cm max PL, ~16 cm midline PL), which are also downstream, Ratliff Ferry, had significant declining CPUE trends represented in museum specimen collections (P. V. Lindeman, for both Graptemys species (Table 3). Ratliff Ferry also had the pers. comm.). The three basking surveys in 2006 similarly most skewed species ratios with G. oculifera (0.95–1.0) vastly indicated a male-skewed population with only 15 females outnumbering G. pearlensis (0.00–0.05) in all years sampled. For observed compared to 123 males. the middle site, Lakeland, both species had declining CPUE Using identical mark–resight survey methodology at the trends, but the G. pearlensis trend of decline was significant (Table same site, Jones and Hartfield (1995) found that G. oculifera 3). At Lakeland, G. oculifera RA (0.67–0.97) was always greater population estimates (131 per rkm) were similar to this study than G. pearlensis (0.03–0.33), with G. pearlensis nearly absent from (146–151 per rkm). There are not similar mark–resight data for the site by the end of the study period (from 0.33 to 0.03). For the G. pearlensis, but our densities for both G. pearlensis (16.1 per next two sites downstream, Monticello and Columbia, declining rkm) and G. oculifera (62.1 per rkm) were threefold higher than trends in CPUE were all negative, but it was a significant decline those described by Lindeman (1998, 1999) for the region around PEARL RIVER GRAPTEMYS STATUS AND CONSERVATION 31

TABLE 1. Comparisons of male and female plastron lengths (cm) and body mass (g) for Graptemys oculifera and Graptemys pearlensis from the Columbia site (Marion County, MS). Body-size comparisons for G. pearlensis are for museum specimens throughout the species’ range.

G. oculifera G. pearlensis

This study Jones and Hartfield (1990, 1995) This study P. V. Lindeman, pers. comm.

Male Female Male Female Male Female Male Female PL N 107 92 138 115 28 10 70 21 Mean 7.8 12.6 7.4 10.6 9.3 14.1 8.1 16.0 Min 5.6 8.0 6.1 6.1 8.1 11.2 5.8 7.1 Max 9.1 15.4 9.2 14.5 10.2 18.2 9.8 21.5 SE 0.06 0.13 – – 0.10 0.85 0.11 1.09 Mass N 107 92 28 10 Mean 96.7 437.4 178.6 740.5 Min 50 110 105 290 Max 140 775 235 1500 SE 1.72 13.22 6.79 147.1 the Columbia site (5.1 G. pearlensis per rkm, 20.4 G. oculifera per pearlensis. Shively (1999) encountered fewer G. pearlensis (N = rkm). Even though absolute densities differed, RA values from 370, 22% of basking turtles) than G. oculifera (N = 513, 30%) on Lindeman’s study (1 G. pearlensis: 4.0 G. oculifera) are similar to Bogue Chitto River in Louisiana, a tributary of the Pearl River. our observations (1 G. pearlensis: 3.9 G. oculifera). The discrep- Therefore, all investigators over the last 20 yr have found G. ancy between these studies’ density values is likely because pearlensis to be a smaller component of the Pearl River basking surveys occurred during different seasons (fall for this study, turtle community. For future studies, mark–resight population summer for Lindeman’s studies) and the river distance sampled estimates would be preferable, because of the considerable (boat surveys, walking, and counting sandbars for this study, variation observed in basking densities across time of day, fixed point counts for Lindeman’s studies). Thus, higher month, and environmental conditions (Jones and Hartfield, basking densities in this study were expected, because of 1995; Selman and Qualls, 2011). decreased fall air and water temperatures that promoted higher Long-Term Study.—Our long-term trapping RA data indicated basking frequencies compared to the summer (Selman and that G. oculifera was more abundant than G. pearlensis at all sites Qualls, 2011). Using basking density surveys, Dickerson and and during all sampling periods. However, because using RA Reine (1996) also found G. oculifera to be more abundant than G. comparisons over long periods has limitations (i.e., assumptions pearlensis at all nine sites on the Pearl River, with G. oculifera about similar population growth rates and direct competition), densities ranging from 10 to 22 times higher than densities of G. inferring actual population density changes using this data set is

TABLE 2. Population density and relative abundance (RA) of Graptemys species from the short-term study site at Columbia site (Marion County, MS) and historical studies (organized by year). Basking density and mark–resight values are expressed as number of turtles per river kilometer. Method of sampling is next to the study name; methods include basking density surveys (BD) without marked individuals and mark–resight surveys (MR) for Graptemys oculifera with paint-marked individuals. For the latter, confidence levels are included in parenthesis below the population estimate.

Graptemys oculifera Graptemys pearlensis

Survey month Number Basking Mark–resight Number Basking Study Site and year observed density RA population estimate observed density RA Jones and Hartfield (1990) MR Columbia July 1995 131 (84–211) Lindeman Pearl River May and June 23.6 0.91 2.4 0.09 (1998) BD S. Pearl River 1994, 1995 20.4 0.80 5.1 0.20 Dickerson Ratliff Ferry July 1996 924 83.2 0.92 75 6.8 0.08 and Reine Lakeland ‘‘ 389 52.6 0.96 18 2.4 0.04 (1996) BD Pools Bluff ‘‘ 11 1.4 0.92 1 0.1 0.08 Pools Bluff Sill ‘‘ 10 3.0 0.91 1 0.3 0.09 Bogue Chitto Sill ‘‘ 58 15.7 0.94 4 1.1 0.06 Lock no. 1 ‘‘ 101 13.7 0.94 7 1.0 0.06 I-59 ‘‘ 43 2.9 1.00 0 0 0 I-10 ‘‘ 3 1.6 1.00 0 0 0 Hwy 90 ‘‘ 0 0 0 0 0 0 Shively (1999) BD Bogue Chitto May–July 1999 513 4–17 0.58 370 2–15 0.42 This Study Columbia October 2005 96 34.9 BD, MR ‘‘ 106 38.5 ‘‘ 99 36.0 2005 Mean 100 36.5 146 (94–259) October 2006 181 65.8 0.78 50 18.1 0.22 ‘‘ 166 60.4 0.80 42 15.3 0.20 ‘‘ 165 60.0 0.80 41 14.9 0.20 2006 Mean 171 62.1 0.80 151 (107–230) 44 16.1 0.20 32 W. SELMAN AND R. L. JONES

S difficult. Therefore, we also used CPUE data as a comparison to determine 1) long-term trends and 2) whether differences occur between the two methods. Even though RA comparisons showed 0.363 Gp Gp - that G. oculifera appeared to be doing ‘‘relatively well’’ compared to G. pearlensis, our CPUE data indicated that both species were S in decline at all sites over the 27-yr period, with six of the 10 species by site comparisons indicating a significant decline. For

0.389 the latter, three of these were for G. oculifera (Carthage, Ratliff Go Go - Ferry, Columbia), and three were for G. pearlensis (Ratliff Ferry, Lakeland, Columbia). Interestingly, the CPUE data indicated that ) by sample site within the Pearl 87 27 0.31 10 0.12

116 49 0.42 19 0.16 declines of both species have occurred both upstream and Gp ( downstream of the Ross Barnett Reservoir (RBR). There are many STD potential explanations for the observed demographic irregular- ities we observed for the G. pearlensis population and for declines

0.204 of both species downstream of the RBR. These include 1) Gp Gp - impaired water quality attributable to industrial and/or munic- ipal effluents, 2) associated impacts of reservoir flow regulation, r.) of daily capture success over time. S

Graptemys pearlensis 3) collection by the pet trade, or 4) a combination of these. First, industrial, agricultural, and municipal effluents may 0.295 ) and have historically impaired water quality in the lower Pearl Go Go - Go

( River. Effluents have degraded water quality and negatively impacted freshwater mussels and gastropods (Neves et al., 1997), likely primary food items for large male and female G. pearlensis (Lovich et al., 2009; pers. obs.) but not major foods

STD items for G. oculifera (Kofron, 1991). In the late 1970s, McCoy and Vogt (1979) noted severe sewage pollution in the Pearl

Graptemys oculifera River downstream of Jackson, with no Graptemys observed 0.366 Gp Gp - between the towns of Jackson and Terry (~43 rkm). Presumably,

S) of water quality in the Pearl River has improved since 1975 with S Gp wastewater and sewer infrastructure improvements in the vicinity of Jackson (Mississippi Department of Environmental Sor

0.034 Quality, 1998). McCoy and Vogt (1979) also noted heavy Go Go Go - discharges from paper mills in Monticello, with the water being ‘‘brown and foamy’’ in this area. They concluded that the cumulative effects of these sources may cause chemical accumulation in Graptemys, leading to death or impaired reproduction while also indirectly impacting invertebrate prey STD densities; however, the irregularities in the population demo- graphics may be attributable and a relic of these municipal or

0.346 c¸

Gp Gp industrial impacts. Shelby and Mendon a (2001) reported a - severe pulp mill discharge that led to direct mortality of turtles S (unspecified species) in the Leaf and Pascagoula Rivers (Mississippi), with a similar spill causing mortality in G.

0.361 oculifera from the lower Pearl River (Finn, 2011). ), and annual species capture success ( - Go Go Second, the RBR, (constructed in 1963) may have had a Gp

or negative impact on downstream Graptemys populations due to

Go habitat alterations. The RBR maintains a relatively stable water level throughout the year (within ~0.6 m; USGS Water

STD Resources, Station 02485600) such that, during lower flow periods (e.g., typically during the summer months), very little water is released to downstream reaches of the Pearl River 0.185 (Station 02485601). In this and other ways, reservoirs alter - riverine hydrology (for review, see Bunn and Arthington, 2002) and are a leading contributor to species endangerment in the United States, particularly in the southeastern United States Carthage Ratliff Ferry Lakeland Monticello Columbia (Czech et al., 2000). More specifically, freshwater mollusks, a 0.566 0.003* 0.37 0.04* 0.05* 0.84 0.03* 0.09 0.24 0.04* 0.05* Go Go S Gp Gp - primary food item of G. pearlensis (Lindeman, 2013), may be impacted below reservoirs attributable to changes in flow regimes (Neves et al., 1997). The Mobile River system of TD , Mississippi, and is one of the most 3. Number of trap days (TD), captures ( impounded river systems in the United States, with high ABLE

T imperilment of freshwater mollusks (Neves et al., 1997; Year -value 3.36 0.921 2.15 2.05 0.20 2.29 1.78 1.20 1.293 2.025 t P River system of Mississippi. Sites are ordered from upstream (left) to downstream (right). The asterisks (*) indicate significant correlations (cor 20132014TotalMean 116Corr. 812 22 385 0.19 7 100 0.06 0.47 928 0.13 1419 116 89 37 0.77 1.45 0 0.0 1,073 607 0.04 116 31 0.27 117 1 0.01 0.56 1,044 116 814 58 0.10 0.50 13 155 0.11 899 0.71 581 0.14 263 0.58 0.25 1988198919901994 3192002 116 1582008 87 0.502009 69 87 0.59 70 33 32 87 0.80 0.10 21 0.37 116 0.18 34 15 203 0.39 0.17 271 9 2.34 0.10 293 15 87 1.44 0.17 8 87 126 15 0.07 232 1.45 113 0.07 1.30 449 116 4Williams 203 1.94 0.05 3 79 78 0.03 0.68 5 87 87 0.38 0.02 et 37 87 46 21al., 78 0.32 377 0.53 0.10 50 0.89 2008). 246 116 0.58 0.65 2 174 4 64 0.02 152Throughout 0.46 41 8 0.55 0.87 0.11 0.09 87 18 87 39 377 0.16 87 75 0.22 78 355 348 0.86 174the 0.90 67 0.94 282 114 0.77Mobile 21 0.81 5 57 0.66 0.24 133 0.06 0.15 5 57 0.38 87 0.06River 0.33 87 68 87 40drainage, 0.78 41 0.46 29 0.47 0.33 2 15 0.02 0.17 PEARL RIVER GRAPTEMYS STATUS AND CONSERVATION 33

FIG. 3. Catch per unit effort (CPUE; panel A) and relative abundance (RA; panel B) of Graptemys oculifera (dashed lines) and Graptemys pearlensis (solid lines) from five sites sampled over 27 yr in Mississippi. Each site is represented by a different color with site colors the same for both panels.

G. pulchra (), a similar mollusk specialist, is Third, G. pearlensis (particularly females) may have been observed at much lower RAs (0.15) when compared to the more captured for the pet trade in the lower Pearl River, whereas generalist G. nigrinoda (Black-Knobbed Sawback, 0.85; Godwin, collectors may have been deterred from capturing G. oculifera, 2003). Furthermore, when water is released from the RBR, it is because of their state (Mississippi Department of Wildlife, often done rapidly; once water levels approach the target Fisheries, and Parks, 2000) and federal (USFWS 1986) listing reservoir level, the flow is quickly stopped. This type of dam status. Because G. pearlensis is one of the few Graptemys species operation contributes to waterlogged banks downstream that not protected by state or federal listing, many turtles of all age collapse under their own weight when water recedes too classes are offered for sale at pet expositions (C. Lechowitz, rapidly. Substantial channel filling follows, and we have pers. comm.) and online classified pages (pers. obs.); however, observed this at downstream sites over the 27-yr study. very little information exists on the trade of G. pearlensis.A 34 W. SELMAN AND R. L. JONES source known to the authors stated in 2007 that almost all of In other Gulf of Mexico river drainages with two Graptemys the G. pearlensis currently on the market were collected from species, broad-headed species are outnumbered by the sympat- the Pearl River by a single collector. Therefore, our numbers ric narrow-headed species, except for headwater reaches of river and lack of females in the Columbia population may reflect the systems (the Mobile Basin, Godwin, 2003; Pascagoula River impacts of over-collecting, especially if females were more system, Selman and Qualls, 2009; Selman and Lindeman, 2015; highly sought by collectors. This site may have been impacted Sabine and Calcasieu River systems, Louque, 2014). Because by the presence of a nearby public boat ramp. Similarly, broad-headed species are generally scarcer than sympatric Conway-Gomez (2007) found that river turtle populations narrow-headed species, environmental and demographic sto- closer to human settlements in the Amazon were more likely to chastic events (Lande, 1993) will have greater impacts on them be exploited than those farther from settlement. compared to the more abundant narrow-headed species. Along with the previously described scenarios downstream Ultimately, chances of population extinction are higher in of the RBR, declines also were observed upstream of the RBR. species with smaller populations like G. pearlensis and broad- Declines of both species during the study period at Ratliff Ferry headed Graptemys species. may be attributable to increased human recreational boating on Conservation Implications.—Based on identical sampling meth- the river and extended human presence on nesting sandbars odology as Jones and Hartfield (1995), G. oculifera appear to have (i.e., semipermanent camps during the summer months). For the maintained a stable population over 25 yr at the Columbia site, former, Selman et al. (2013) found that G. flavimaculata, a similar but currently it appears to be an aging population. The species in the Pascagoula River, was impacted by boating population structure of G. pearlensis depicts a struggling recreation through behavioral changes (e.g., limited basking) population with few reproductively mature females. Numerous and physiological changes (e.g., increased long-term stress). factors may be responsible for these irregularities in the Additionally, it seems likely that more direct mortalities may be population, and these factors could have been historical (e.g., occurring in this population attributable to faster and larger municipal effluents and water quality) or continue to the present boats using the river than in the 1980s and 1990s (RLJ, pers. (e.g., impacts of reservoir on hydrology). Our long-term RA data obs.). For the impacts of human presence on sandbars, Moore indicate that G. oculifera has outnumbered G. pearlensis at all sites and Seigel (2006) found limited opportunities for nesting in G. over the last 27 yr, whereas our long-term CPUE data indicate flavimaculata attributable to long-term human disturbance on that populations of both species have declined at all sites, and nesting beaches. significantly at some sites. Data sets for RA and CPUE align only Upstream at Carthage, declines of G. oculifera may be 40% of the time; hence, we suggest caution when using only RA attributable to excessive sedimentation. Tuscolameta Creek data for species comparisons attributable to the difficulty in empties into the Pearl River in the lower section of the site inferring actual population densities. and was channelized in the late 1950s to facilitate drainage Based on our data and comparisons to historical data, G. along ~40 km of the creek. The creek has been classified as an pearlensis population declines may have occurred prior to our impaired stream attributable to organic enrichment and oxygen study, and declines at some sites have continued to the present; depletion, nutrient load, and sedimentation (Mississippi De- likewise, G. pearlensis also may represent a naturally less partment of Environmental Quality, 2014). Channelization has abundant member of the Pearl River turtle fauna. Regardless increased sediment input into the Pearl River since the of the exact scenario, all evidence indicates that additional beginning of the study and subsequently decreased the state/federal protections, comprehensive surveys, and studies availability of deeper water habitats preferred by Graptemys are warranted for G. pearlensis. First, rangewide surveys for G. (RLJ, pers. obs.). pearlensis should focus on documenting their current distribu- Historical Comparisons.—Comparisons of our data to historical tion and abundance, with particular attention to smaller rivers data from the Pearl River are difficult to make because of and creeks within the system that may harbor populations. New differing sampling methodologies. Historical efforts used night localities and drainages may be found similar to G. gibbonsi in hand/dipnet capture methods between the 1950s and 1970s the Pascagoula River system (Selman and Qualls, 2009) and (Cagle, 1953; Tinkle, 1958; Cliburn, 1971), and these studies found other Graptemys species (Lindeman, 2013). Second, extensive G. pearlensis were about twice as abundant as G. oculifera.This field efforts should be initiated for G. pearlensis that simulta- method, however, may not be representative of the population, neously document 1) population size via mark–resight efforts, with the specimen record indicating hand/dipnet sampling was 2) population structure, 3) diet, and 4) aspects of reproduction. biased toward juveniles (WS, pers. obs.). Hence, these sampling Third, G. oculifera long-term declines at all sites (three being efforts may have other biases and misrepresent the true historical significant) indicate that continued protection and monitoring densities of the two Graptemys species. Later collections using for this species remains warranted. Fourth, because turtles have fyke nets indicated a more equitable capture record between the long generation times and population trends may not be two Pearl River Graptemys species (105 G. oculifera:80G. noticeable without longer-term data (>30 yr), additional pearlensis; Vogt, 1980). This sample is an intermediate point in trapping efforts using similar methods at our study sites should time between earlier hand capturing samples and our later determine if both G. oculifera and G. pearlensis populations basking trap samples. Our data from 1988 to 2014 at all sites and continue declining or eventually stabilize. These studies would all time periods indicated that G. oculifera RA was always higher make great strides in closing the existing life history and than G. pearlensis, and our CPUE data indicate G. pearlensis ecology gaps for both species, while also providing valuable declines over the last 27 yr at three of the five study sites. information for future conservation of Graptemys and river Therefore, G. pearlensis may have declined between the 1950s and management efforts. mid-1980s, and declines may continue at some sites to the present. Acknowledgments.—We thank the Mississippi Department of Graptemys pearlensis also may have been a naturally rare Wildlife, Fisheries, and Parks (MDWFP) for providing project member of the Pearl River community compared to G. oculifera. funding. This project could not have been completed without PEARL RIVER GRAPTEMYS STATUS AND CONSERVATION 35 the technical assistance of T. Mann (Mississippi Museum of Iverson, R. 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