Three's Company: Observations of a Nonnative Map Turtle (Graptemys pseudogeographica) Occurring Syntopically with Two Endemic Graptemys in the Pearl River, Mississippi
Abstract
Humans commonly move turtles and tortoises across geopolitical and geographic boundaries through food markets and the pet trade. One group commonly encountered in the pet trade is the genus Graptemys (map turtles and sawbacks). In the late 1980s, Graptemys pseudogeographica (false map turtle) was documented outside of its native range in the Pearl River near Jackson, Mississippi. Through replicated visual surveys in 2017 and 2018, we found that G. pseudogeographica persists in this location, but their densities were low (0.22/river km; 0.5% of all observations) compared with the 2 native Graptemys species. We evaluated the historical avenues for introduction via natural or human-mediated routes. Based on topographic profiles and historical hydrologic records, we strongly refute a prior hypothesis that G. pseudogeographica naturally colonized the Pearl from a neighboring drainage during the Easter Flood of 1979. Rather, we suggest that introduction via the release of unwanted pets is a more parsimonious conclusion. Because the lineage is shallowly diverged on an evolutionary scale, it seems possible that hybridization could occur between introduced G. pseudogeographica and Graptemys oculifera. Consequently, genetic introgression of the nonnative G. pseudogeographica genome is a possible threat to G. oculifera, a federally threatened species. This is a conservation concern to be further evaluated.
Nonindigenous species (NIS) can move into novel habitats by natural means (colonization) and through numerous human-mediated channels (introductions). For the former, large dispersal events are known for avian species that move great distances across oceans (e.g., cattle egrets, Bubulcus ibis; Crosby 1972; Arendt 1988) likely aided by meteorological events (Massa et al. 2014), while rafting has been implicated for the spread of reptilian species to remote islands (e.g., Chelonoidis tortoises; Caccone et al. 1999). However, introductions of NIS have rapidly increased through human-mediated transport in numerous pathways including but not limited to aquatic ballast associated with transoceanic shipping (Bax et al. 2003; Costello et al. 2007), the horticulture trade (Reichard and White 2001), and the pet trade (Kraus 2009; Smith et al. 2009). Introductions can have a myriad of consequences including direct predation, herbivory, poisoning (as with Rhinella marina), disease transmission, competition with native species, and in some cases, the ability to hybridize with a native species (for review, see Kraus 2015).
As a group, turtles and tortoises (Order Testudines) are popular in the global pet trade (Gong et al. 2009; Luiselli et al. 2016). They are charismatic animals that often adapt to captive settings, particularly as hatchlings and juveniles. However, many turtles have long lifespans (50+ yrs), and often quickly outgrow their enclosures. Owners usually do not have the means or will to keep these animals throughout their entire lives. Thus, many turtles are released annually into nonindigenous habitats rather than being rehomed or humanely euthanized (Spinks et al. 2003; Cadi and Joly 2004). Consequently, the pet trade is the most important pathway for reptile and amphibian introductions on a global scale (Kraus 2009). Up to the late 1990s, the slider turtle (Trachemys scripta) dominated the turtle pet trade (Telecky 2001), but recently other smaller-sized turtles, including species from the genus Graptemys, have become more prevalent in the pet trade (Mali et al. 2014; Luiselli et al. 2016).
There are 14 known Graptemys species (map turtles and sawbacks), and many are endemic to Gulf Coastal river systems (Lindeman 2013). This endemism has been structured by historical sea-level changes over the last 12–15 million yrs, and these dramatic changes led to dispersal and vicariant events that isolated populations in different river systems (Thomson et al. 2018). Because Graptemys species are riverine specialists and do not migrate long distances over land (Lindeman 2013), most species have been allopatric to and genetically isolated from similar species in neighboring river systems. Consequently, many neighboring Graptemys species occupy similar ecological niches, and genetically they are shallowly diverged (Thomson et al. 2018). Therefore, many readily hybridize with other members of the genus (Godwin et al. 2014; Mitchell et al. 2016). Thus, when one Graptemys species moves into a nonindigenous drainage—either through colonization or introduction—it could lead to hybridization with a native species.
Jones et al. (1991) documented Graptemys pseudogeographica, a species primarily of the Mississippi River drainage (Lindeman 2013), in the Pearl River system of central Mississippi around Jackson (Mississippi Museum of Natural Science Herpetological Collection [MMNS] specimen No. 2718). Jones et al. (1991) suggested that given the proximity to Jackson, the presence of G. pseudogeographica in the Pearl River was due to the release of captive individuals. However, McCoy and Vogt (1992) later suggested an alternative hypothesis for the presence of G. pseudogeographica around Jackson. They posited that the species naturally dispersed to the Pearl River due to the record Easter Flood of 1979. McCoy and Vogt (1992) believed the Pearl River may have connected Bayou Pierre of the Mississippi River system (native drainage of G. pseudogeographica) to the Pearl River.
The goal of this study was to determine if G. pseudogeographica persists in the Pearl River around Jackson. If so, we sought to understand their distribution and determine how their densities compare with the 2 native Graptemys species of the Pearl River. A secondary goal was to use digital elevation models (DEMs) to determine if the flooding hypothesis proposed by McCoy and Vogt (1992) is consistent with the Pearl River flooding reported in 1979.
METHODS
Pearl River Study Sites. — The Pearl River is a medium-sized river (in Jackson: ∼ 70–100 m wide; mean discharge, ∼ 113 m3/sec), and it drains much of central Mississippi and southeastern Louisiana (drainage basin ∼ 22,348 km2) into the Gulf of Mexico. The city of Jackson, Mississippi, is located near the geographic center of the drainage in central Mississippi. In this area, we selected 5 equidistant and consecutive river segments (5.3 river km [rkm] each; total, 26.5 rkm) of the Pearl River for turtle surveys (Hinds and Rankin counties; Fig. 1). Two of these segments (S1, S2) occur in the location where Jones et al. (1991) previously collected G. psuedogeographica, and these segments are also in the vicinity of Lefleur's Bluff State Park and Lakeland Drive (a major highway). The next 2 segments were in a highly channelized, urban section of the Pearl River (S3, S4), and the last survey segment (S5) was in a more remote section of the Pearl River south of Jackson. For additional information about these sites, see Selman (2020).
Citation: Chelonian Conservation and Biology: Celebrating 25 Years as the World's Turtle and Tortoise Journal 19, 2; 10.2744/CCB-1435.1
Methods for Field Observations. — All river survey reaches were floated by boat during the months of June and July in 2017 and 2018, and observations from this study were made during the same basking surveys reported by Selman (2020). We completed 6 replicate surveys for S1 and 5 replicate surveys for S2–S5 (total of ∼ 137.8 rkm surveyed); flooding during June 2017 prevented us from completing a sixth round of surveys for S2–S5. Using survey methods similar to those described by Selman and Qualls (2009), when sandbars were present, the boat was anchored on the upstream end of the sandbar. We then identified and counted basking turtles via spotting scope while walking down the sandbar. However, we acknowledge that individuals could have been recounted on subsequent surveys and therefore, we consider them “records” rather than individuals. We identified the sex and life-history class (adult/juvenile) of G. pseudogeographica and native Graptemys species when possible based on descriptions by Lindeman (2013). In the absence of sandbars, visual surveys were completed by floating downstream (< 5 km/hr) in an outboard motorboat. When floating, 2 observers used binoculars and counted turtles on opposite banks of the river; a third person served as data recorder. When confirmation of species identity was difficult from a distance, we used a Nikon CoolPix p900 digital camera with ×83 optical zoom to take photographs of individuals; these photographs were later examined in the laboratory. All surveys were completed between ∼ 0900 and 1530 hrs when environmental conditions were conducive to basking. We avoided surveying on days when large amounts of rain or thunderstorms occurred in order to minimize the variance of conditions during our observations and for safety reasons, respectively. Mean basking densities were calculated by dividing the total number of observed turtles in each river segment by the total distance surveyed for each river segment (i.e., S1, 31.8 rkm; S2, 26.5 rkm). Because G. pseudogeographica basking density data were nonnormally distributed, we used a nonparametric Kruskal-Wallis test to determine if densities (i.e., numbers observed per kilometer) were equal across the 5 segments surveyed. If differences were observed, we used a Wilcoxon nonparametric multiple comparisons post hoc analysis to determine differences among segments.
Elevation Profiles. — To investigate the possibility of G. pseudogeographica dispersing naturally into the Pearl River as proposed by McCoy and Vogt (1992), we used ArcMap 10.7.1 software and a 10-m DEM for Mississippi to generate topographic profiles. The DEM was obtained from the Mississippi Automated Resource Information Center (https://www.maris.state.ms.us/). We completed 3 topographic profiles including 2 potential avenues for G. pseudogeographica entering the Pearl naturally via 1) the Big Black/Bear Creek/Ross Barnett Reservoir (RBR) and 2) the Bayou Pierre/Copiah Creek hypothesis proposed by McCoy and Vogt (1992; Fig. 2). The third was an elevation profile of the divide between the Pearl River and the Big Black/Bayou Pierre river drainages from northern Madison County to southern Copiah County (Fig. 2).
Citation: Chelonian Conservation and Biology: Celebrating 25 Years as the World's Turtle and Tortoise Journal 19, 2; 10.2744/CCB-1435.1
RESULTS
Basking Observations and Densities. — During our 137.8 rkm of replicated visual surveys, we observed a total of 5643 basking turtle records. We were able to positively identify 31 of these records as G. pseudogeographica (0.5%; 0.22/rkm for all segments). For comparison with the native species, 4843 records were assigned to Graptemys oculifera (85.8%; 35.0/rkm) and 188 to Graptemys pearlensis (3.3%; 1.4/rkm; Selman 2020). We made observations of G. pseudogeographica in S2–S5 (Table 1), but did not observe them in S1 (Fig. 1). However, 19 observations were concentrated in ∼ 4.2 rkm in the lower portion of S2 and upper portion of S3, a section that is adjacent to Lefleur's Bluff State Park. The sex ratio of observed G. pseudogeographica was nearly equal (12 males, 16 females), and we did not observe any juvenile G. pseudogeographica. Mean basking densities of G. pseudogeographica were different across segments (χ2= 15.3, df = 4, p = 0.004). Wilcoxon nonparametric multiple comparisons post hoc analyses indicated that S2 and S5 had higher mean densities than S1 and S3 but similar densities to S4, while S4 had the same mean densities as S1 and S3 (Table 1).
Interactions with Other Native Turtles. — Graptemys pseudogeographica was observed basking alone (Fig. 3A), but they were also observed readily basking with other native turtle species (Fig. 3B–E). We observed G. pseudogeographica basking on 4 different instances with G. oculifera. We observed a large female G. pseudogeographica in S2 basking with a male G. oculifera (9 June 2017; Fig. 3B), while we observed a female G. pseudogeographica in S5 basking with a female G. oculifera (12 June 2018; Fig. 3C). We observed a male and female G. pseudogeographica in S2 basking with a female G. oculifera (27 June 2018), and we observed a female G. pseudogeographica basking with a juvenile, male, and female G. oculifera (3 July 2018). Graptemys pseudogeographica was also observed basking with other native species. We observed a large female in S2 basking with a Pseudemys concinna (river cooter; 9 July 2017; Fig. 3D), and we observed a female G. pseudogeographica basking with an Apalone spinifera (spiny softshell turtle) along with 3 G. oculifera (3 July 2018). In one observation on 31 July 2017, we observed all 3 Graptemys species—G. pseudogeographica, G. oculifera, and G. pearlensis—basking in the same tree crown in S5 (Fig. 3E).
Citation: Chelonian Conservation and Biology: Celebrating 25 Years as the World's Turtle and Tortoise Journal 19, 2; 10.2744/CCB-1435.1
Citation: Chelonian Conservation and Biology: Celebrating 25 Years as the World's Turtle and Tortoise Journal 19, 2; 10.2744/CCB-1435.1
Topographic Profiles. — All 3 topographic profiles indicate that the topographic divides between the Pearl River and neighboring drainages of the Big Black River and Bayou Pierre present significant barriers for drainage connectivity (Fig. 4). The US Geological Survey river gage height at Jackson is 71.2 m above mean sea level (mamsl; 233.7 feet), thus the 1979 flood would put the maximum water height at 84.4 mamsl (276.9 feet) at the US Highway 80 gauge. Because this river gauge was not installed at this location until 2014, we do not have the true value of the flooding downstream near McCoy and Vogt's (1992) hypothesized location. However, the confluence of Copiah Creek with the Pearl River is ∼ 12 mamsl lower (59 mamsl) than the gauge at US Highway 80 in Jackson. Thus, if we assume and add the same height of floodwater at Jackson (∼ 13 m), to the elevation at Copiah Creek/ Pearl River confluence (59 mamsl), the water in this area was at an elevation of ∼ 72 mamsl. This elevation is not close to approaching the divide elevation at the hypothesized location (144 mamsl), and this would preclude the connection of the 2 watersheds even during this record flood event.
DISCUSSION
Basking Observations, Densities, and Distribution. — Overall, G. pseudogeographica accounted for a small percentage of the Pearl River turtle community in the Jackson area. We observed G. pseudogeographica in 4 of 5 river segments surveyed indicating a substantial presence and distribution throughout most of the Pearl River in Jackson. But we lacked the observation of juveniles to say that they are established based on the criteria of Blackburn et al. (2011). Even though we are lacking this component to definitively say they are established, it seems likely that the species has become established for several reasons. First, the species has persisted in the same segment of river over a 30-yr period since the initial discovery by Jones et al. (1991), and our observations of large individuals suggests that the species has survived in the Pearl River for some time. Second, even though not in the Pearl River, Selman (2020) observed a juvenile G. pseudogeographica in an oxbow lake within Lefleur's Bluff State Park immediately adjacent to the S2 river segment discussed herein; it is unknown if this juvenile was a pet release or a wild-born individual. Third, because the Pearl River is adjacent to the native range of G. pseudogeographica in the Big Black River and Bayou Pierre, it seems likely that there are no apparent environmental barriers (i.e., similar climate, riverine habitat) to the species becoming established in the Pearl River. Based on the criteria for establishment as proposed by Blackburn et al. (2011), this is suggestive that they are established in the Jackson area of the Pearl River. However, additional reproductive data for G. pseudogeographica would be valuable to determine if they are indeed established in this location.
For comparison, mean G. oculifera basking density in these same segments was 159 times greater than G. pseudogeographica density (mean, 35.0/rkm; range, 11.7–52.5/rkm), while G. pearlensis mean density was 6 times greater than G. pseudogeographica (mean, 1.4/rkm; range, 0.4–3.2/rkm; Selman 2020). As of now, the presence of G. pseudogeographica does not appear to have impacted densities of G. oculifera and G. pearlensis because both native species are similar to or greater than observed densities in areas without G. pseudogeographica present. However, G. pseudogeographica may be interacting ecologically with native turtle species, and these interactions may not be manifested at the population level yet. For example, at a minimum, G. pseudogeographica may be occupying and competing for basking substrates preferred by native turtles. Second, the reported diet of G. pseudogeographica (Lindeman 2013) overlaps the diet of G. pearlensis and also that of Sternotherus carinatus (razorback musk turtle), both of which are known to consume mollusks and aquatic insects (Lindeman 2008, P.V. Lindeman, unpubl. data). Third, from a reproductive perspective, it seems possible that they may be hybridizing with G. oculifera due to the shallow genetic divergence between the 2 species (∼ 750,000 yrs; Thomson et al. 2018), and it is known that Graptemys species readily hybridize (Godwin et al. 2014; Mitchell et al. 2016). The hybridization of G. pseudogeographica with G. pearlensis seems less likely because the relationship is more distant than for G. oculifera (∼ 1.2 million yrs; Thomson et al. 2018). Many of the interactions listed above seem possible, but as of now are not well supported. They would need to be confirmed in future studies.
Explanation of Introduction. — Even though several researchers have studied river turtles of the Pearl River over the last 40 yrs (e.g., McCoy and Vogt 1979; Dickerson and Reine 1996; Lindeman 1998; Shively 1999; Selman and Jones 2017), G. pseudogeographica was not reported prior to or after Jones et al. (1991) from any additional sites. However, only after the report by Jones et al. (1991) did McCoy and Vogt (1992) state that they also captured a subadult female G. pseudogeographica in 1979 (i.e., following the Easter Flood of 1979) near Georgetown, Mississippi; this location is ∼ 75 rkm below our survey locations in Jackson. Later surveys by Lindeman (1998) and Lindeman et al. (2020) did not observe any G. pseudogeographica in the Pearl River drainage at 20 and 125 localities, respectively. Lastly, in over 27 yrs of study at 5 sites, Selman and Jones (2017) did not observe any G. pseudogeographica at any sites except the Lakeland site; the Lakeland site is inclusive of S2 described in the present study. Thus, the species appears to be localized around Jackson and potentially downstream to Georgetown, while no other verified observations have occurred in other parts of the drainage over the last 40 yrs.
The historical distribution of G. pseudogeographica includes the Mississippi River and its tributaries, as well as several river drainages west of the Mississippi River (e.g., Calcasieu, Sabine, Trinity, Brazos rivers). The nearest known native locales for G. pseudogeographica to this incipient Pearl River population is ∼ 44 km overland to the Big Black River near Edwards, Mississippi. However, upstream of Jackson, the Big Black River drainage approaches closer to the Pearl River via Bear Creek, a tributary of the Big Black River (Figs. 3 and 4). Graptemys pseudogeographica individuals have been observed in Doak's Creek, a tributary of the Big Black River in Madison County (W.S., pers. obs.). However, this path into the Pearl River does not seem possible because there are no records of the RBR (elevation ∼ 90 mamsl) flooding to an elevation of 97.5 mamsl, the elevation that could connect the lowest point of the divide between the Pearl and Big Black river drainages. A flood of this magnitude would have caused overtopping and eventual catastrophic failure of the earthen dam and spillway of the RBR, and this did not occur in the Easter Flood of 1979, the flood of record for the Pearl River. Also, because Graptemys do not migrate overland, this scenario does not appear to be a route of colonization.
As McCoy and Vogt (1992) suggested, a closer distance does exist between a Mississippi River tributary, Bayou Pierre, and a tributary of the Pearl River, Copiah Creek. Also, a G. pseudogeographica specimen (MMNS 4020) was collected in 1968 from Bayou Pierre, ∼ 10.75 km straight line distance from Copiah Creek. Because of this proximity, McCoy and Vogt (1992) hypothesized that G. pseudogeographica may have dispersed into the Pearl during the massive Easter Flood of 1979. However, based on our topographic profiles and elevation comparison of flooding in the region, we are able to strongly refute this hypothesis. For this dispersal to occur (i.e., to connect the nearest tributary of Bayou Pierre to the Pearl River), a flood would have had to overcome the 144-m elevation of the divide (∼ 46.5 m above the Big Black scenario posed above). To overcome this elevation, a flood would have exceeded > 85 m above the river gauge at the Copiah Creek/Pearl River confluence. There are no records of a Pearl River flood of this magnitude, and there is no record of flooding occurring in the town of Hazelhurst (i.e., the town between Copiah Creek and Bayou Pierre) or on Interstate 55, which also divides the 2 drainages.
Alternatively, the popularity of G. pseudogeographica in the pet trade (Kraus 2009; Mali et al. 2014; Luiselli et al. 2016), combined with the human population density in northeast Jackson (i.e., highest concentration of our sightings) suggest that the individuals observed are likely released captives as originally proposed by Jones et al. (1991). Similarly, several authors have found G. pseudogeographica outside of their native range in the United States. In Virginia, Savitsky and Mitchell (2001) attributed their observation of G. pseudogeographica specimens to the pet trade, while Krysko et al. (2011) also attributed Florida records of the species to the pet trade. Spinks et al. (2003) also documented G. pseudogeographica on the campus of University of California, Davis, and these records were similarly attributable to the pet trade. More specific to our study area, a colleague of W.S. commented that a professional colleague of his grew up in northeast Jackson and owned pet turtles as a kid, including G. pseudogeographica. These pet turtles were later released into the Pearl in the 1970s, and it is likely that other people in the area did the same thing around the same period. Therefore, the release of unwanted pets appears to be the provenance of G. pseudogeographica around Jackson, likely back to the 1970s. Thus, an explanation of the G. pseudogeographica captured by McCoy and Vogt (1992) downstream near Georgetown could have been an individual from the Jackson area that was “flushed” downstream during the Easter Flood of 1979 rather than an individual naturally colonizing the Pearl River from a neighboring watershed.
Conclusions and Conservation Recommendations. — We observed G. pseudogeographica individuals in the Pearl River that appeared to belong to both of the nominate subspecies: G. p. pseudogeographica and G. p. kohnii. Therefore, it seems that the pet-released individuals may be from multiple origins throughout the Mississippi River drainage and are likely not from a single pet release. Alternatively, the variation observed in phenotypic traits could perhaps be associated with the convergence of G. pseudogeographica and G. oculifera phenotypes associated with hybridization (particularly the postorbital crescent in G. p. kohnii or small blotch in G. oculifera); the latter species is a federally threatened species that is endemic to the Pearl River system (Jones and Selman 2009). It seems possible that hybridization may be occurring between G. pseudogeographica and G. oculifera. If so, genetic introgression of G. pseudogeographica genes into the G. oculifera genome is possible, potentially compromising the genetic entity of this federally threatened species. For this reason, further sampling and genetic studies are needed at the study site and neighboring sites upstream and downstream to determine if hybridization occurs and if so, the frequency and the extent of genetic introgression that might be occurring between G. pseudogeographica and G. oculifera. Any G. pseudogeographica encountered in the Pearl River should be removed, humanely euthanized, and deposited in a scientific collection.
Aerial view of the Pearl River in Jackson, Mississippi, and locations of the 5 segments surveyed, separated by color. S1 (green line) is farthest upstream, while S5 (blue line) is farthest downstream. The 31 locations of Graptemys pseudogeographica are marked with circles, and the circle color denotes sex (pink = female, blue = male, white = unknown sex). White lines represent major highways and interstate highways in the study area. (Color version is available online.)
Map of central Mississippi and the 3 elevation profiles discussed in text and depicted in Fig. 4. Profile A to A′ represents the Big Black River to Bear Creek to the Ross Barnett Reservoir. Profile B to B′ represents McCoy and Vogt's (1992) hypothesis from Bayou Pierre to Copiah Creek to the Pearl River. Profile C to C′ (dotted line) represents the drainage divide between the Pearl River and the Big Black River to the north and Bayou Pierre to the south.
Basking Graptemys pseudogeographica: (A, B) G. p. kohnii; (C) G. p. pseudogeographica. (B, C, D, E) Graptemys pseudogeographica basking on the same emergent deadwood as native turtle species as described in text. The white asterisk marks the G. pseudogeographica in the photos.
Topographic profiles corresponding to the 3 scenarios depicted in the Fig. 2 map. Vertical exaggeration on all profiles is ×250.
Contributor Notes
Handling Editor: Peter V. Lindeman
