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Genetic and Morphological Variation Between Populations of the Pascagoula Map Turtle (Graptemys gibbonsi) in the Pearl and Pascagoula Rivers with Description of a New Species
Abstract and Figures
Cryptic or undescribed species pose a major problem in conservation biology. Managing multiple unresolved taxa collectively as a single entity could precipitate the loss of unrecognized genetic variation and unique populations and, possibly, lead to extinction of undiscovered or unrecognized taxa. In contrast to other species in its clade, the Pascagoula map turtle (Graptemys gibbonsi), as currently recognized, is not confined to a single major river system (or a cluster formed by a major river and adjacent minor drainages) but occurs in two major river systems, the Pearl and Pascagoula Rivers. We analyzed G. gibbonsi samples from both rivers for the first time in a morphological and molecular assessment of the taxonomic status of this poorly studied species. We compared the extent of genetic differentiation (mitochondrial DNA; mtDNA) between G. gibbonsi populations with members within the pulchra clade and between Graptemys oculifera and Graptemys flavimaculata. We found significant carapace pattern variation and morphological differentiation between the Pearl and Pascagoula river samples of G. gibbonsi. Our mtDNA sequences showed greater genetic differentiation between G. gibbonsi samples from the Pearl and Pascagoula rivers than between two recognized and reciprocally sympatric species, G. oculifera (Pearl River) and G. flavimaculata (Pascagoula River), but revealed only a modest degree of differentiation when compared to other members of the pulchra clade. Based on the degree of differentiation in 1) morphology, 2) color patterns, and 3) mtDNA, in addition to their 4) allopatric distributions, we describe a new species from the Pearl River, restricting the species G. gibbonsi to the Pascagoula River.
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... Lovich and McCoy (1992) examined specimens from four river drainages and divided the species into three species, G. pulchra, G. ernsti, and G. gibbonsi, with the last of these inhabiting the Pascagoula and Pearl rivers of southern Mississippi and southeastern Louisiana. Later, Ennen et al. (2010) showed that the turtles in the Pascagoula and Pearl rivers were also separate species, describing those from the Pearl River drainage as a new species (G. pearlensis). ...
... barbouri, G. ernsti, and G. pulchra) is evidence of niche conservatism (Peterson et al. 1999;Peterson 2011). Graptemys pearlensis and G. gibbonsi are similar enough in appearance that they were considered conspecific until just a decade ago (Mount 1975;Lovich and McCoy 1992;Ennen et al. 2010), and phylogenetic analyses suggest they are each other's closest relatives (Praschag et al. 2017;Thomson et al. 2018). Hence, it is not surprising that they should have similar diets in adjacent, ecologically similar river systems. ...
Patterns of interspecific differences in the diets of nonavian reptiles may be complicated by intraspecific dietary diversity that is related to variation in body size and trophic morphology. Graptemys pearlensis and Graptemys gibbonsi are sister map turtle species endemic to adjacent Gulf Coastal river drainages and both are candidates for federal listing. Little has been reported about the diet of either species. We examined fecal samples collected from turtles captured throughout their respective ranges in the Pearl and Pascagoula river drainages. Females of both species primarily consumed invasive Asian clams (Corbicula spp.), with adult females being nearly exclusively molluscivorous while juvenile females also consumed softer-bodied prey items. Adult males and unsexed juveniles primarily consumed insects; males in particular specialized on trichopteran larvae and also ate more mollusks than did unsexed juveniles. In comparisons to each species' sympatric congeneric sawback species, the two focal species' avoidance of sponges caused large interspecific differences. Due to their greater consumption of insect prey than mollusks, unsexed juvenile G. pearlensis and unsexed juvenile and adult male G. gibbonsi were slightly more similar in diet to their respective sympatric congeneric sawbacks than to conspecific large juvenile females and adult females. Scoring of similarity in diet was greatly influenced by strongly predominant prey items found within each class of each species. Future studies of interspecific dietary differences in sympatric species should include consideration of intraspecific variation in diet as it relates to body size and sexual dimorphism.
... They designated 1 of the specimens from 1876 as lectotype and restricted the name G. pulchra to specimens from the Mobile Bay drainages, describing the Escambia Bay drainage specimens as Graptemys ernsti and the Pearl and Pascagoula river drainage specimens as G. gibbonsi; they also recognized some differences between specimens from the latter 2 rivers. Ennen et al. (2010) described the Pearl River drainage specimens as G. pearlensis, restricting G. gibbonsi to the Pascagoula River drainage specimens. Thomson et al. (2017) reported support for the monophyly of each of the 4 allopatrically distributed species formerly united as G. pulchra sensu lato. ...
... We believe it is clear that populations of G. gibbonsi are more robust overall than populations of G. pearlensis. A previous comparison of sawback:megacephalic species ratios in -1995(Lindeman 1998 did not consider the difference between the drainages because the 2 megacephalic species were at that time considered a single species under the name G. gibbonsi (Ennen et al. 2010). In replicated point counts conducted primarily on main stem sites (31 of 41 total sites, or 76%), the 2 sawbacks were 5.1 as abundant as the 2 megacephalics. ...
... Although this genetic structure and morphological differentiation may be the result of genetic drift, little gene flow between Mississippi and Alabama populations may occur due to the large distance between the mouth of the Pascagoula River Delta and the Alabama populations. Land and saltwater can hinder gene flow for freshwater species that are distributed in riverine systems across the Gulf of Mexico (Soltis et al., 2006), including the Pascagoula River (e.g., Dugo et al., 2004;Ennen et al., 2010). level of tolerance to brackish water (Agha et al., 2018). ...
Pseudemys alabamensis is one of the most endangered freshwater turtle species in the United States due to its restricted geographic distribution in coastal Alabama and Mississippi. Populations of P. alabamensis are geographically isolated from one another by land and saltwater, which could act as barriers to gene flow. It is currently unknown how differentiated these populations are from one another and whether they have experienced reductions in population size. Previous work found morphological differences between Alabama and Mississippi populations, suggesting that they may be evolutionarily distinct. Other Pseudemys turtles such as P. concinna and P. floridana occur naturally within the same geographic area as P. alabamensis and are known to hybridize with each other. These more abundant species could threaten the unique genetic identity of P. alabamensis through introgression. In order to evaluate the endangered status of P. alabamensis and the level of hybridization with other species, we used mitochondrial and nuclear microsatellite markers to assess genetic variation within and among populations of P. alabamensis throughout its range and estimate admixture with co‐occurring Pseudemys species. In P. alabamensis, we found no variation in mitochondrial DNA and an excess of homozygosity in microsatellite data. Our results show genetic differentiation between Alabama and Mississippi populations of P. alabamensis, and low estimated breeding sizes and signs of inbreeding for two populations (Fowl River, Alabama and Biloxi, Mississippi). We also found evidence of admixture between P. alabamensis and P. concinna/P. floridana. Based on our results, P. alabamensis is highly endangered throughout its range and threatened by both low population sizes and hybridization. In order to improve the species’ chances of survival, focus should be placed on habitat preservation, maintenance of genetic diversity within both the Mississippi and Alabama populations, and routine population‐monitoring activities such as nest surveillance and estimates of recruitment. Pseudemys alabamensis is one of the most endangered freshwater turtle species in the United States. Populations of P. alabamensis are geographically isolated from one another by land and saltwater, which could act as barriers to gene flow, resulting in the evolution of unique populations. Other Pseudemys turtles such as P. concinna and P. floridana occur naturally within the same geographic area as P. alabamensis and are known to hybridize with each other. These more abundant species could threaten the unique genetic identity of P. alabamensis through introgression. We used mitochondrial and nuclear microsatellite markers to assess genetic variation within and among populations of P. alabamensis throughout its range and estimate admixture with co‐occurring Pseudemys species. We found that P. alabamensis is highly endangered throughout its range and threatened by both low population sizes and hybridization. Conservation measures must be developed to prevent further reduction and extinction of this endangered species.
... However, often the autors advocating for splits (e.g. Vog, 1993 for G. ouachitensis from G. pseudogeographica [see also discussion byFreedberg and Myer, 2012]; Lindeman 2013, for G. sabinensis from G. ouachitensis;Ennen et al. 2010 for another split in other Graptemys turtles) do not use the biological species concept. ...
The paper presents a review of literature data, supplemented with original observations, on the presence, establishment, distribution and invasive status of alien fish, amphibian and reptile species in Romania. Consistent criteria were followed in defining alien species records, establishment and invasive status. From the 48 alien fish species, 1 fish hybrid, 1 amphibian and 18 reptile species recorded, only 16 fishes and 3 reptiles can be regarded as established. Of these we consider the criteria for invasive status as being probably fulfilled by one fish species ( Perccottus glenii ), and less likely by six more fish species. The presence and the alien status of the one amphibian are debatable. No reptile species can be considered invasive at present.
... Nine species were described in the 20th century, including G. ernsti and G. gibbonsi in 1992 (Lovich and McCoy 1992). Another, G. pearlensis, was described in 2010 (Ennen et al. 2010) and G. sabinensis was formally elevated to a full species in 2013 (Lindeman 2013), following the suggestions of earlier researchers. Clearly, our knowledge of the diversity of this genus is still evolving and new species or distinct evolutionary lineages may yet be discovered and recognized. ...
... Two endemic riverine turtle species occur sympatrically in the Pearl River system of central Mississippi: Graptemys oculifera (ringed sawback; Baur 1890) and Graptemys pearlensis (Pearl map turtle; Ennen et al. 2010). Even though information has been collected for both species throughout the river system (e.g., Jones and Hartfield 1995;Lindeman 1998Lindeman , 1999Shively 1999;Selman and Jones 2017;Lindeman et al. 2020), there is relatively little population data for either species throughout the segment of the Pearl River that flows through downtown Jackson, including the section slated for the One Lake Project. ...
The impacts of human modifications of rivers and associated riverine fauna are well documented, especially following the construction of impoundments. In the Pearl River system of Mississippi and Louisiana, 2 endemic Graptemys species are found (G. oculifera; G. pearlensis), but little is known of their densities in urban segments near Jackson, Mississippi, even though both are species of conservation concern. I used spotting scopes and binoculars to complete replicated basking surveys for both Graptemys species during the summers of 2017 and 2018 in 5 equidistant segments of the Pearl River and nearby oxbow lakes. Basking densities for both species were generally higher in river segments upstream and downstream of Jackson compared to middle segments. Graptemys oculifera were found in greater densities than G. pearlensis in all segments (14–69-times higher). Graptemys oculifera was found in 4 of the 6 oxbow lakes surveyed, but mean densities decreased 10-fold compared with river segments; G. pearlensis was absent from all oxbow lakes. Densities for a generalist turtle species, Trachemys scripta, increased 35 times in oxbow vs. river habitats. The middle 3 survey segments (∼ 15.9 river kilometers) are inclusive of a proposed river impoundment project—the One Lake Project—for flood control and economic development. Estimates of direct and indirect impacts of this project are sizeable for G. oculifera (direct impact: 1684; indirect: 2129) while estimates for G. pearlensis are lower (direct: 88; indirect: 219). The One Lake Project would surely alter existing riverine processes and will favor generalist turtles such as T. scripta that prefer nonflowing lake settings at the expense of riverine Graptemys species. The One Lake Project would be a major setback to both Graptemys species in and around the project area and would negatively impact the recovery potential of both species.
... Our molecular analyses align with the hypothetical historical connection between the Mobile and PPP, as our phylogenetic and coalescent-based species delimitation analyses strongly supported Potamilus spp. in these biogeographic provinces as distinct clines. These results align with other mussel species showing genetic distinctiveness across these drainages [53,69,83,84], as well as other aquatic species [85][86][87][88][89][90]. ...
North American freshwaters are among the world's most threatened ecosystems, and freshwater mussels are among the most imperiled inhabiting these systems. A critical aspect of conservation biology is delineating patterns of genetic diversity, which can be difficult when a taxon has been extirpated from a significant portion of its historical range. In such cases, evaluating conservation and recovery options may benefit by using surrogate species as proxies when assessing overall patterns of genetic diversity. Here, we integrate the premise of surrogate species into a comparative phylogeographic framework to hypothesize genetic relationships between extant and extirpated populations of Potamilus inflatus by characterizing genetic structure in co-distributed congeners with similar life histories and dispersal capabilities. Our mitochondrial and nuclear sequence data exhibited variable patterns of genetic divergence between Potamilus spp. native to the Mobile and Pascagoula + Pearl + Pontchartrain (PPP) provinces. However, hierarchical Approximate Bayesian Computation indicated that the diversification between Mobile and PPP clades was synchronous and represents a genetic signature of a common history of vicariance. Recent fluctuations in sea-level appear to have caused Potamilus spp. in the PPP to form a single genetic cluster, providing justification for using individuals from the Amite River as a source of brood stock to re-establish extirpated populations of P. inflatus. Future studies utilizing eDNA and genome-wide molecular data are essential to better understand the distribution of P. inflatus and establish robust recovery plans. Given the imperilment status of freshwater mussels globally, our study represents a useful methodology for predicting relationships among extant and extirpated populations of imperiled species.
... The tortoise and freshwater turtle fauna of the United States is the most diverse globally, with 58 taxa and 52 species, comprising approximately 20% of global species diversity (Buhlmann et al., 2009;Ennen et al., 2010;Lovich and Ennen, 2013;Turtle Taxonomy Working Group, 2014). Compared with most vertebrate groups, a disproportionate number of turtle species are facing population declines, local and regional extirpations, and even extinctions (Gibbons et al., 2000;Turtle Conservation Coalition, 2011). ...
Comal Springs in New Braunfels, Texas, is the largest freshwater spring west of the Mississippi. The spring is within the Edwards Plateau Savanna Ecoregion of the Southeastern United States Turtle Priority Area. Comal Springs is an environmentally sensitive spring run situated in an urbanized area visited by >1,000,000 people each year and thus may be impacted by recreational use. We assessed baseline population levels for the turtle assemblage residing in Comal Springs. We captured 4,238 turtles from February 2012 to February 2015 across 12 separate sampling sessions. Captures and individually marked turtles (in parentheses) included 2,322 (1,715) Sternotherus odoratus, 1,558 (793) Pseudemys texana, 329 (141) Trachemys scripta, and 29 (19) Chelydra serpentina serpentina. We report population densities of 1,690/ha (S. odoratus), 230/ha (P. texana), 43/ha (T. scripta), and 5/ha (C. s. serpentina). We estimated biomass for each species and sex, resulting in a total biomass estimate of 5,309.6 kg or 632.1 kg/ha. Sex ratios for P. texana and T. scripta were 1:1, whereas the sex ratio for S. odoratus was 2.26:1, male biased. Our results suggest that a robust turtle assemblage inhabits Comal Springs, similar in richness to the more well-studied freshwater spring habitats in Florida. Future studies or management actions can use our data as a benchmark as the results of few turtle surveys in Texas have been published.
... Los caracteres registrados para los individuos de Kinosternon abaxillare corresponden con las descripciones cualitativas proporcionadas para la especie por Álvarez del Toro (1973,1982), Berry e Iverson (2001), Iverson (2008Iverson ( , 2010 (Iverson, 1991;Lubcke y Wilson, 2007;Rivera, 2008;Ennen et al., 2010;Stay, 2011;Legler y Vogt, 2013). Un claro ejemplo de lo anterior es K. leucostomum, ya que, dependiendo de la región, de la calidad del hábitat y/o del alimento esta especie puede presentar una gran variedad de coloraciones y tamaños en los escudos de su caparazón, tal como lo ha reportado Legler y Vogt (2013). ...
México es el país con mayor diversidad de kinostérnidos a nivel mundial, sin embargo, pocos estudios se han realizado en la región sureste del país. La mayoría de las especies del género Kinosternon son tortugas medianas o pequeñas, omnívoras que presentan lóbulos plastrales movibles que les sirve para poder protegerse dentro de su caparazón. Kinosternon abaxillare es una especie que sólo se distribuye de manera natural en la Depresión Central de Chiapas y al norte de Guatemala. A pesar de que este taxón se describió hace más de 90 años, actualmente se desconoce mucho de su biología, ecología, distribución y estado de conservación. Acorde a lo anterior, en este estudio se abordaron aspectos de la ecología poblacional y se realizó un análisis morfológico de K. abaxillare en la localidad de Villa Hidalgo, municipio de Villaflores, Chiapas, México. El estudio se realizó en el periodo de marzo de 2018 a febrero de 2019, teniendo un total de 12 salidas de campo. Los organismos se capturaron con trampas tipo fyke net y cajas plegables. Cada individuo fue medido y pesado solamente la primera vez que fue capturado, además, se les realizaron muescas para su posterior reconocimiento, esto con el fin de aplicar un modelo de captura-marca-recaptura y determinar algunos aspectos de su ecología poblacional. Se registraron un total de 168 individuos, de los cuales se recapturaron 64, además, en esta región, esta especie tuvo mayor actividad en la época de lluvia. La población (≥ 231 ind) y densidad (> 700 ind/ha) estimada en esta región infiere que existe un gran número de individuos, sin embargo, debido a la mayor presencia de adultos en la estructura poblacional (≥ 120 mm de largo de caparazón), se puede decir que la población no es estable. La proporción de sexos estimada difirió de 1:1 y tuvo un sesgo hacia las hembras. Todas las clases de tamaño y sexo presentaron un caparazón tricarinado, además, algunos individuos en esta población (<10%) presentaron parcialmente escudos axilares. Los registros cualitativos de K. abaxillare presentan similitudes con lo reportado para K. scorpioides. Cuantitativamente, los ejemplares de K. abaxillare en esta región representaron una similitud en lo registrado para K. chimalhuaca, K. integrum y K. scorpioides. Además, de todas las especies de kinostérnidos con las que K. abaxillare comparte una cercanía filogenética, los machos adultos presentaron los porcentajes más bajos en la relación corporal (porcentual) de la longitud del escudo plastral tres y cinco con la longitud de los lóbulos plastrales anterior y posterior respectivamente. Todas las clases de tamaño presentaron el mismo arreglo plastral (4>6>1>2>5>3). Las hembras de esta especie son más grandes y pesadas que los machos, sin embargo, estos últimos se pueden diferenciar por que presentan una mayor concavidad en el plastrón, una cabeza más ancha con motas oscuras, un pico pronunciado en la ranfoteca y una cola más larga con una gran uña en la punta.
Turtles are one of the most threatened group of animals in existence today. The
Southeastern United States is one of two global biodiversity hotspots for turtle species,
including the state of Mississippi, where over 30 species can be found. However, very
few studies have occurred within the state.
The overarching goal of this project was to perform a species inclusive freshwater
survey and document the distribution and abundances of the diverse species present here.
A substantial amount of data was collected through these surveys, including
morphometric measurements, genetic samples, and habitat data recorded at each trap
location. These data were then used to determine if riverine habitat and surrounding land
cover has any effect on turtle communities. Similarly, a state-wide population genetic
study on the Spiny Softshell turtle (Apalone spinifera) was initiated.
The surveys performed for this study captured a total of 1,230 turtles, from 16
species. Analyses showed that land-use had no significant impact on turtle communities
or species, but that habitat can be a predictor of species occurrence in some
circumstances. Finally, our genetic analysis of A. spinifera from the Pascagoula and Pearl
River drainages showed two distinct populations between the two drainages, but did not
detect any intra-drainage populations structure.
Three new species of Percina are described from upland drainages of the Mobile Basin. Two of the three species are narrowly distributed: P. kusha, the Bridled Darter, is currently known only from the Conasauga River drainage in Georgia and Tennessee and Etowah River drainage in Georgia, both tributaries of the Coosa River, and P. sipsi, the Bankhead Darter, which is restricted to tributaries of Sipsey Fork of the Black Warrior River in northwestern Alabama. The third species, P. smithvanizi, the Muscadine Darter, occurs above the Fall Line in the Tallapoosa River drainage in eastern Alabama and western Georgia. In a molecular analysis using mitochondrial cytochrome b sequence data, P. kusha and P. smithvanizi were recovered as sister species, while Percina sipsi was recovered in a clade consisting of P. aurolineata (P. sciera + P. sipsi). Two of the three species, P. kusha and P. sipsi, are considered to be imperiled species and are in need of conservation actions to prevent their extinction. Description of these three darters increases the number of described species of Percina to 44. Sixteen are known to occur in the Mobile Basin, including nine that are endemic.
Variation in relative width of the head and alveolar surfaces of the jaws in map turtles (Graptemys) is associated with the degree of molluscivory in adult females. Adult males are substantially smaller in body size and are primarily insectivorous, and they take few mollusks regardless of their relative head width or alveolar width. We assessed functional relationships within and between the sexes using comparative analyses (independent contrasts and squared-change parsimony) of the residuals of regressions of head width on plastron length and alveolar width on head width. Residuals of head width and alveolar width were significantly correlated within females but not within males in all comparative analyses. Residuals of each regression were significantly correlated between males and females for a subset of analyses. Our results suggest that evolutionary changes in relative head width have been correlated with changes in relative alveolar width in females of Graptemys due to a functional relationship that is related to the tendency to feed on mollusks. Males have exhibited changes in the two characters similar to changes in females over evolutionary time, probably as a result of genetic covariation, but due to males' primarily insectivorous nature, changes in the two characters have not shown significant correlation with one another.
We describe a new species of chorus frog of the North American treefrog genus Pseudacris from the south-central United States. This new species is morphologically similar to the parapatric species P. feriarum and has thus previously been considered synonymous with this species. The new species is geographically distinct from P. feriarum and from its sister species, P. nigrita. We diagnose the new species based on advertisement call, morphological, and genetic characters.
The recently-developed statistical method known as the "bootstrap" can be used to place confidence intervals on phylogenies. It involves resampling points from one's own data, with replacement, to create a series of bootstrap samples of the same size as the original data. Each of these is analyzed, and the variation among the resulting estimates taken to indicate the size of the error involved in making estimates from the original data. In the case of phylogenies, it is argued that the proper method of resampling is to keep all of the original species while sampling characters with replacement, under the assumption that the characters have been independently drawn by the systematist and have evolved independently. Majority-rule consensus trees can be used to construct a phylogeny showing all of the inferred monophyletic groups that occurred in a majority of the bootstrap samples. If a group shows up 95% of the time or more, the evidence for it is taken to be statistically significant. Existing computer programs can be used to analyze different bootstrap samples by using weights on the characters, the weight of a character being how many times it was drawn in bootstrap sampling. When all characters are perfectly compatible, as envisioned by Hennig, bootstrap sampling becomes unnecessary; the bootstrap method would show significant evidence for a group if it is defined by three or more characters.
Replicate adaptive radiations are dichotomous morphological patterns related to resource use and repeated in a series of isolated habitats. Biologists have long noted a dichotomy in relative head width and alveolar width among species of map turtles (Graptemys), particularly with regard to adult females, which are much larger than adult males in all 12 species. I measured plastron length (PL), head width (HW), and alveolar width (AW) of nearly 2300 specimens representing the 12 recognized species, and used allometric regressions to investigate this genus as an example of both sexual dimorphism in trophic morphology and replicate adaptive radiation. Sexual dimorphism was noted in HW after correction for PL, with females having wider heads than males of similar body sizes, but AW as corrected for HW was not dimorphic, thus absolute differences in AW are the simple result of differences in HW. Sexual differences in HW probably relate to the dimorphic niches of Graptemys, as females of three species have been reported to occupy deeper water further from shore than conspecific males. Based on predicted HW at maximum PL in adult females, species were categorized as mega-, meso-, or microcephalic. Differences in relative head width are related to differences in degree of molluscivory, with little molluscivory in microcephalic females, moderate to high molluscivory in mesocephalic females, and high molluscivory in mega-cephalic females. Distributions of Graptemys species in sympatry and allopatry reveal patterns consistent with structuring of distributions via competitive interactions. Superimposing data on relative HW on a phylogeny of the genus suggests there may have been one or two episodes of character displacement, with subsequent character assortment, in Graptemys evolution. This conclusion is similar to the current model for the evolution of body size during the radation of Anolis lizards in the northern Lesser Antilles.