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Sampling locales for alligator snapping turtles. Shaded area approximate native range, dots trapping sites. Collections 3E, 3F, and 3G are combined as the Red River/ Louisiana population in some analyses
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A previous mtDNA study indicated that female-mediated gene flow was extremely rare among alligator snapping turtle populations in different drainages of the Gulf of Mexico. In this study, we used variation at seven microsatellite DNA loci to assess the possibility of male-mediated gene flow, we augmented the mtDNA survey with additional sampling of...
Citations
... Studies comparing eDNA analyses with conventional sampling have increased over time (Akre et al., 2019;Evans et al., 2017;Fuji et al., 2019;McElroy et al., 2020;Moss et al., 2022;Shaw et al., 2016), but cost comparisons between these methods remain uncommon (Akre et al., 2019;Bálint et al., 2018;Qu & Stewart, 2019;Smart et al., 2016). And yet, eDNA assessments are frequently touted as more sensitive and/or less expensive than conventional sampling approaches, particularly for RTE species (Qu & Stewart, 2019 However, the long lifespan of this species, which can be 59-70 years in captivity (Gibbons, 1987), and its limited dispersal ability (Echelle et al., 2010;Roman et al., 1999), suggests that Stream 19 is likely to still be occupied by M. temminckii when eDNA samples were collected. A potential false negative (i.e., the species is present but not detected) could be the result of many different factors. ...
Environmental DNA (eDNA) analysis is an effective and non‐invasive technique for surveying and monitoring rare, threatened, or endangered (RTE) species. Compared to conventional capture‐based sampling, eDNA analysis may offer a more cost‐effective approach for surveying RTE species, yet few studies have compared their cost‐efficiency—a critical consideration for conservation planning. We compared the costs, effort, and relative performance of aquatic eDNA sampling and conventional trapping for detecting the Alligator Snapping Turtle, Macrochelys temminckii Troost, 1835, in southwest Louisiana, United States. Environmental DNA was sampled quarterly over 1 year (2018–2019) at 19 streams, including three streams where M. temminckii presence had been previously confirmed via conventional trapping efforts (2012–2013). Water samples from each stream were analyzed using quantitative polymerase chain reaction (qPCR) to assess M. temminckii eDNA presence/absence. Time and costs (i.e., labor, travel, wages, and supplies) per detection via eDNA analysis and trapping were calculated and compared. Environmental DNA analysis documented the presence of M. temminckii DNA at two of the three streams where individuals had previously been trapped and yielded detections (qPCR amplifications) at 16 additional streams not previously sampled, expanding M. temminckii 's documented distribution at our study sites by 84%. Environmental DNA analysis returned a detection rate (per site) 5.55 times higher than conventional trapping and was 18.7% less expensive. Our results provide evidence that strategically deployed eDNA surveys may be an effective and cost‐efficient approach for detecting freshwater RTE species. With eDNA analysis, additional resources can be invested toward expanding survey coverage and increasing sampling frequency, allowing managers to more effectively target subsequent intensive monitoring efforts.
... We sourced turtles for reintroduction from Tishomingo National Fish Hatchery (TNFH; Tishomingo, OK, USA; n = 126), which operates a breeding program, and the Peoria Zoo (PZ; Peoria, IL, USA; n = 57), which is a partner in the recovery primarily by housing and quarantining turtles from various sources (e.g., confiscations, other zoos, private donations). We only considered turtles of the Mississippi River haplotype (Roman et al. 1999, Echelle et al. 2010) for release to ensure genetic compatibility with historical populations at the release site (Kessler et al. 2017). The broodstock maintained at TNFH are all of the appropriate haplotype, whereas we determined the haplotype for individual PZ animals before release. ...
Maladaptive movement behavior is a leading cause of failure for reptile reintroductions, thus characterizing movement for translocated populations is important to project success. From 2014–2016 we radio‐tracked 183 immature reintroduced alligator snapping turtles ( Macrochelys temminckii ) using very high frequency telemetry in a stream in southern Illinois, USA. We assessed environmental, temporal, morphometric, and microhabitat factors influencing movement, including post‐release dispersal from reintroduction sites, movement probability, and step length. We used directional statistics to investigate the effects of precipitation and age on directional movement in the stream. Numerous factors influenced active movement, including ambient temperatures, time since release, use of log jams, turtle size, and age. Precipitation had an age‐biased effect on movement. Directional analyses suggested that movement was largely passive as turtles were swept downstream with increased discharge. Overall, the behavior of reintroduced alligator snapping turtles was similar to that reported in wild populations. Passive downstream transport has implications for reintroduced and natural populations as a force for unintentional emigration in channelized streams under current conditions and future high flow regimes.
... The third species described by Thomas et al. (2014) was included in the synonymy of M. temminckii in the checklist. That third potential taxon of Macrochelys has been known to be genetically distinct for some time (Roman et al. 1999) and has been referred to as its own evolutionarily significant unit, ESU (Echelle et al. 2010, Roman et al. 1999. Most recently, it was regarded as a distinct "analysis unit" within M. temminckii in the species status assessment (USFWS 2021a), i.e., the Apalachicola Unit, which is how we refer to it here. ...
Herein we briefly provide a background context for and summary overview of the articles comprising this special issue of the Southeastern Naturalist on Macrochelys spp. (alligator snapping turtles). We also make a case for standardization in collecting and reporting morphometric data on these species, clarify the current taxonomic status within the genus, provide updated information on the distribution of Macrochelys in the US, and include a current bibliography and categorical analysis over time of the rapidly growing collection of literature focused on these iconic turtles.
... Roman et al. (1999) used mitochondrial DNA to show that M. temminckii exhibited strong phylogeographic and population-level structuring, delineating 3 major clades: an eastern assemblage from the Suwannee River, a central assemblage from the Choctawhatchee River in the east to Econfina Creek in the west, and a western assemblage from the Pensacola Bay in the east to the Trinity River in the west. Adding microsatellite loci to the mitochondrial, Echelle et al. (2010) also found support for the 3 evolutionary lineages (Roman et al. 1999), although the exact placement of divergent individuals from Pensacola Bay differed between mitochondrial and nuclear microsatellite data. Echelle et al. (2010) also found high among-population divergence, measured by F ST , and suggested conservationists recognize 6 evolutionarily significant units (ESUs; Moritz 1994). ...
... Adding microsatellite loci to the mitochondrial, Echelle et al. (2010) also found support for the 3 evolutionary lineages (Roman et al. 1999), although the exact placement of divergent individuals from Pensacola Bay differed between mitochondrial and nuclear microsatellite data. Echelle et al. (2010) also found high among-population divergence, measured by F ST , and suggested conservationists recognize 6 evolutionarily significant units (ESUs; Moritz 1994). Based on the divergent genetic clades, and analysis of carapace and head morphology, Thomas et al. (2014) described 2 new species corresponding to the groups originally described by Roman et al (1999): Macrochelys suwanniensis Thomas, Granatosky, Bourque, Krysko, Moler, Gamble, Suarez, Leone, Enge, and Roman (Suwannee Alligator Snapping Turtle) from the Suwannee and Santa Fe Rivers in Florida and Georgia, Macrochelys apalachicolae Thomas et al. (Apalachicola Alligator Snapping Turtle) from the Ochlockonee River to the Choctawhatchee River, and restricted the original species, M. temminckii, to drainages from the Pensacola Bay and westwards. ...
... J.J. Apodaca, A.R. Krohn, L. Collins, J.C. Godwin, L. Pearson, and A.D. Walde 2023 Vol. 22, Special Issue 12 Additionally, Folt and Guyer (2015) noted the discrepancy between mitochondrial and nuclear data (Echelle et al. 2010) in defining the western assemblage, calling into question the reciprocal monophyly of M. apalachicolae. Thus, because of mitonuclear discordance and morphological similarity between M. temminckii and M. apalachicolae, M. temminckii and M. suwanniensis were recognized as distinct taxa, but M. apalachicolae was synonymized as part of M. temminckii (Turtle Taxonomy Working Group 2017). ...
Historically believed to harbor unrecognized diversity, the taxonomy of the declining genus Macrochelys (alligator snapping turtles) is debated. The original species, M. temminckii, was recently split into M. temminckii, M. apalachicolae, and M. suwanniensis. However, the status of M. apalachicolae is contested. In this study, we generated thousands of genome-wide loci to quantify population structure and genetic differentiation across the range of Macrochelys spp. Our data indicate that M. apalachicolae is genetically distinct, with little gene flow between M. apalachicolae and other species, thus adding evidence that M. apalachicolae may be a distinct species. We also find genetic variation partitioned among river drainages, with very high intra- and interspecific genetic divergence among river drainages. We suggest that translocations and re-introductions only move turtles in this genus within their natal river drainages to preserve existing patterns of genetic diversity.
... data). All M. temminckii from the rivers of Arkansas and Oklahoma, as well as other rivers within the Mississippi River Drainage, are characterized by the mitochondrial haplotype A (Echelle et al. 2010, Roman et al. 1999. ...
We investigated nesting behavior and terrestrial activity in a captive population of Macrochelys temminckii (Alligator Snapping Turtle) housed outdoors in semi-natural environmental conditions in Oklahoma. The nesting season lasted from 12 May to 15 June 2012, and turtles were most active between the hours 2300-0300. Nesting duration averaged 182.5 min. Over 50% of nest construction time was spent excavating the cavity, whereas covering the eggs accounted for ~28% of the total duration. Individual females averaged 25 non-nesting emergences before successfully depositing eggs. Terrestrial activity was positively correlated with increasing average nighttime temperature. We found thermal profiles generated by temperature data loggers affixed to females useful for studying terrestrial activity during nesting.
... That populations are structured by rivers sharing a bay may be an artifact of those rivers being connected as a single drainage when sea levels were lower in the Pliocene and Pleistocene, as has been suggested before for AST and other Gulf Coast freshwater turtles (Lamb et al. 1994;Roman et al. 1999). Regardless of the cause for divergence, across the range of AST (Echelle et al. 2010;Apodaca et al. 2023), we find strong patterns of population subdivision (as defined by Hartl and Clark 1997), likely indicating that migration between populations is very low. We attest this divergence to rare overland dispersal (Reed et al. 2002). ...
Texas comptroller natural resource management report
... Additional alligator snapping turtles should be necropsied for polystome infections across this turtle's geographic distribution and especially within Gulf of Mexico river drainages (Southeastern United States): distinct host populations or cryptic species may exist that harbor innominate polystomes. At present, the alligator snapping turtle is accepted as a single species that exhibits infrequent or limited dispersal between rivers in the Southeastern United States, with at least 6 evolutionarily significant units (ESUs) diagnosed with mtDNA and microsatellite DNA evidence (Echelle et al., 2010). The most distinctive ESU is alleged to be represented by alligator snapping turtles in the Suwannee River, Florida, and some authors regard these alligator snapping turtles as comprising a distinct species, Macrochelys suwanniensis Thomas, Grantaosky, Bourque, Krysko, Moler, Gamble, Suarez, Leone, Enge, and Roman, 2014 (see Roman et al., 1999;Echelle et al., 2010;Murray et al., 2014;Thomas et al., 2014;Folt and Guyer, 2015). ...
... At present, the alligator snapping turtle is accepted as a single species that exhibits infrequent or limited dispersal between rivers in the Southeastern United States, with at least 6 evolutionarily significant units (ESUs) diagnosed with mtDNA and microsatellite DNA evidence (Echelle et al., 2010). The most distinctive ESU is alleged to be represented by alligator snapping turtles in the Suwannee River, Florida, and some authors regard these alligator snapping turtles as comprising a distinct species, Macrochelys suwanniensis Thomas, Grantaosky, Bourque, Krysko, Moler, Gamble, Suarez, Leone, Enge, and Roman, 2014 (see Roman et al., 1999;Echelle et al., 2010;Murray et al., 2014;Thomas et al., 2014;Folt and Guyer, 2015). It is possible that this putatively distinct alligator snapping turtle in the Suwannee River hosts a species of Neopolystoma that is not conspecific with our specimens. ...
Herein, we describe several newly-collected specimens of Neopolystoma cf. orbiculare from the urinary bladder of 2 alligator snapping turtles, Macrochelys temminckii (Troost in Harland, 1835) (Cryptodira: Chelydridae Gray, 1831) from Comet Lake (30°35'46.94″N, 88°36'3.12″W), Pascagoula River, Mississippi. Our specimens differed from all previous descriptions of N. orbiculare and its junior subjective synonyms by the combination of having intestinal ceca adorned with triangular pockets and that terminate dorsal to the haptor, distinctive hooklets each having a handle and guard of approximately equal length and having a much longer and curved blade, 16 genital coronet spines that each possess 1-2 flanges per spine, pre-testicular vaginal pores, and vaginal ducts that are anterior to the junction of the oviduct and genito-intestinal canal. Some of our specimens were enantiomorphic (4 and 3 had a dextral and sinistral ovary, respectively). Nucleotide sequences (large subunit ribosomal DNA [28S], small subunit ribosomal DNA [18S], and cytochrome oxidase subunit 1 mitochondrial gene [COI]) for our specimens were most similar to GenBank sequences ascribed to N. orbiculare. Single-gene and concatenated phylogenetic analyses confirmed that NeopolystomaPrice, 1939 is polyphyletic and that our isolates share a recent common ancestor with those ascribed to N. orbiculare. This is the first record of a polystomatid from Mississippi, from the Pascagoula River, and from the alligator snapping turtle (and only the second species of Neopolystoma reported from any snapping turtle).
... We present, the first results related to the population genetics of wild population of T. venusta venusta in Mexico compared to founder individuals of a captive group (Mexican UMA). With the exception of some studies that present low genetic diversity (value of H e < 0.4; Echelle et al., 2010;Vargas-Ram ırez et al., 2012), freshwater turtles generally exhibit high values of genetic diversity (generally H e > 0.6-0.7; Vargas-Ram ırez et al., 2012, Table 4 for examples; Davy et al., 2014) when using methodology based on microsatellites. ...
The Meso-American slider turtle (Trachemys venusta) is a freshwater turtle that is widely distributed from Mexico to Colombia. Due to the overexploitation of populations of this species in Mexico, it has been placed within the "subject to special protection" category formulated by the Official Mexican Standard NOM-059-ECOL-2010. In the state of Tabasco, Mexico, Management Units for the Conservation of Wildlife (UMA) were created to reduce the impact of overexploitation of freshwater turtles bred in captivity. However, no genetic management plan was considered. The present study was carried out in an UMA in the state of Tabasco. We obtained the level of genetic diversity of the founder individuals of the UMA in order to develop a management plan which will optimize reproduction in the UMA. Genetic diversity was compared between captive (n = 86) and wild (n = 45) individuals using 14 microsatellite molecular markers. The genetic diversity parameter determined in this study was slightly higher for captive than for wild population (H e = 0.606 and H e = 0.594 respectively), reflecting the mix of genetic sources in captive group (founding individuals from different localities) and demonstrating that the captive population contains a diverse subset of alleles from representative populations. The analysis of genetic structure revealed a relationship between captive and wild populations, indicating the influence of the two principal river basins in this region on the populations structure of freshwater turtles. Finally, according to the results obtained from the relationship analysis, we recommend the use of 19 females and 13 males to constitute the appropriate breeding group, generating a potential of 247 dyads with no relationship. However, in order to improve breeding program and the genetic diversity of captive population, we suggest to introduce wild-caught individuals. These results are the first regarding genetic management in a Mexican UMA and demonstrate the importance of molecular approaches in the management and conservation of captive species.
... We designed sets of forward-reverse primers and hydrolysis probes based on 11 mitochondrial (mt)DNA control region haplotypes identified by Echelle et al. (2010) using the online PrimerQuest (Integrated DNA Technologies, http://idtdna.com/prime rquest) tool. This ensured genus-level specificity for each haplotype of Macrochelys (Echelle et al., 2010) and was obtained from the authors by request. ...
... We designed sets of forward-reverse primers and hydrolysis probes based on 11 mitochondrial (mt)DNA control region haplotypes identified by Echelle et al. (2010) using the online PrimerQuest (Integrated DNA Technologies, http://idtdna.com/prime rquest) tool. This ensured genus-level specificity for each haplotype of Macrochelys (Echelle et al., 2010) and was obtained from the authors by request. ...
... primer-blast/ ). For in silico primer-probe testing, we created a sequence library of all Echelle et al. (2010) mtDNA haplotypes and 18 nontarget turtle species (Table S1). To ensure specificity of our primer-probe in vitro, we used nontarget tissues consisting of regional samples of all 11 potentially sympatric species (Table S2). ...
Background: Imperfect detection of hard‐to‐sample organisms has motivated the development of novel monitoring techniques. Environmental DNA (eDNA) can pro‐ vide a sensitive, relatively low‐cost sampling method in aquatic systems, but biotic and abiotic factors can affect its reliability.
Aims: We used a reintroduced population of radio‐tracked alligator snapping turtles (Macrochelys temminckii) to test the efficacy and ecology of eDNA in a lotic system. Materials & Methods: We collected samples at turtle locations as well as random up‐ and downstream sites. Using a novel eDNA assay, we modeled occupancy and detection of eDNA using turtle biomass and remotely sensed UV exposure and also tested the relationship between these parameters and eDNA concentration. Results: We found eDNA occupancy was best explained by upstream biomass and detection probability decreased with greater upstream UV exposure. The concentra‐ tion of eDNA in a sample was not significantly affected by biomass measures, but decreased with higher upstream UV exposure, and the effect was significant. Discussion: Our results show that UV exposure can affect aquatic eDNA sampling in situ with free‐ranging animals. The use of radiotelemetry allowed for higher control when modeling eDNA persistence and transport in a natural setting relative to labo‐ ratory, enclosure, or mesocosm studies.
Conclusion: We propose using wildlife tracking techniques to provide added realism to studies of eDNA dynamics
... Burbrink and Guiher [89] estimated that there was such low gene flow between cottonmouths (Agkistrodon piscivorus) in peninsular Florida and the mainland that speciation must have occurred between those two regions, a hypothesis immediately contested by data from Strickland et al. [93] who detected a broad geographic range of admixture using AFLP markers. Similarly, Thomas et al. [13] described alligator snapping turtles (Macrochelys temminckii) from the Apalachicola River and adjacent rivers to be a distinct species, despite microsatellite data from Echelle et al. [94] that are inconsistent with this conclusion [95]. While analyses of one or a few genetic loci can be informative by revealing apparent monophyly, they should not be viewed as sufficient to diagnose and delimit species, particularly when available life history data provide plausible mechanisms for contemporary gene flow and mito-nuclear discordance. ...
... Agkistrodon piscivorus are known to move among wetlands [96], providing ample opportunity for contemporary gene flow along peninsular Florida despite historical periods of isolation via marine inundation [46,92]. Similarly, observations of barnacles growing on shells of M. temminckii [97] indicate that this species can occupy brackish habitats, a life-history feature providing an avenue of dispersal between major drainages [94]. Thus, life history data exist for both species that demand examination of contemporary admixture and gene flow using multi-locus datasets, similar to our process with D. couperi. ...
Accurate species delimitation and description are necessary to guide effective conservation of imperiled species, and this synergy is maximized when multiple data sources are used to delimit species. We illustrate this point by examining Drymarchon couperi (Eastern Indigo Snake), a large, federally-protected species in North America that was recently divided into two species based on gene sequence data from three loci and heuristic morphological assessment. Here, we re-evaluate the two-species hypothesis for D. couperi by evaluating both population genetic and gene sequence data. Our analyses of 14 microsatellite markers revealed 6–8 genetic population clusters with significant admixture, particularly across the contact zone between the two hypothesized species. Phylogenetic analyses of gene sequence data with maximum-likelihood methods suggested discordance between mitochondrial and nuclear markers and provided phylogenetic support for one species rather than two. For these reasons, we place Drymarchon kolpobasileus into synonymy with D. couperi. We suggest inconsistent patterns between mitochondrial and nuclear DNA are driven by high dispersal of males relative to females. We advocate for species delimitation exercises that evaluate admixture and gene flow in addition to phylogenetic analyses, particularly when the latter reveal monophyletic lineages. This is particularly important for taxa, such as squamates, that exhibit strong sex-biased dispersal. Problems associated with over-delimitation of species richness can become particularly acute for threatened and endangered species, because of high costs to conservation when taxonomy demands protection of more individual species than are supported by accumulating data.
