Phylogeography of the African helmeted terrapin, Pelomedusa subrufa: Genetic structure, dispersal, and human introduction
Abstract and Figures
The African Helmeted Terrapin, Pelomedusa subrufa is currently recognized as a single species, and is found throughout sub-Saharan Africa, as well as on the Arabian Peninsula and in Madagascar. A preliminary genetic study of Pelomedusa based on mitochondrial and nuclear DNA is presented to determine the genetic diversity within Pelomedusa, and whether the disjunct populations are natural or anthropogenic. The monophyly of Pelomedusa is in question, as Pelusios may be nested within Pelomedusa. Within Pelomedusa there are three subgroups: Western, Eastern, and Southern. The Western clade is composed of two monophyletic groups divided by ecoregion, one through the Sahel region of Africa, and the other in the savanna region of West Africa. The Eastern clade contains a disjunct population on the Arabian Peninsula, and sequence divergence and divergence dating estimates indicate that this population was probably established through a natural dispersal event. The Southern clade includes a disjunct population in Madagascar, and this Malagasy population likely is the result of a recent human-mediated introduction, since sequence divergence compared to other individuals in the Southern clade is relatively low.
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... Pelomedusidae Pelomedusa Vargas-Ramírez et al. (2010), Fritz et al. (2014Fritz et al. ( , 2015, Petzold et al. (2014), Vamberger et al. (2018) Pelomedusidae Pelomedusa, Pelusios Fritz et al. (2011) Pelomedusidae Pelusios sinuatus Vamberger et al. (2019b) Testudinidae Chersina angulata Daniels et al. (2007), Spitzweg et al. (2020) Testudinidae Chersobius signatus Daniels et al. (2010) Testudinidae Cylindraspis Kehlmaier et al. (2019a) Testudinidae Homopus areolatus Hofmeyr et al. (2020) Testudinidae Kinixys Kindler et al. (2012) Testudinidae Psammobates tentorius Zhao et al. (2020aZhao et al. ( , 2020bZhao et al. ( , 2021a Testudinidae Stigmochelys pardalis Fritz et al. (2010), Spitzweg et al. (2019), Dajčman et al. (2021) Testudinidae Testudinidae Hofmeyr et al. (2017) Madagascar. Together with their successive sister group, the Chelidae from South America, Australia, and New Guinea, they constitute the suborder Pleurodira (sidenecked turtles; TTWG 2021), which originated on Gondwana (de la Fuente et al. 2014;Pereira et al. 2017 Wong et al. (2010), andFritz et al. (2011), the knowledge of the diversity and the phylogenetic relationships of the two pelomedusid genera Pelomedusa and Pelusios received a considerable boost. Previously, it was believed that Pelusios is a speciose genus of 18 species, whereas Pelomedusa was thought to be monotypic, with Pelomedusa subrufa as the only species (Fritz and Havaš 2007;TTWG 2009). ...
... Previously, it was believed that Pelusios is a speciose genus of 18 species, whereas Pelomedusa was thought to be monotypic, with Pelomedusa subrufa as the only species (Fritz and Havaš 2007;TTWG 2009). However, two independent studies revealed that Pelomedusa comprises deeply divergent genealogical lineages (Vargas-Ramírez et al. 2010;Wong et al. 2010). Ten of these lineages were later formally recognized as distinct species Petzold et al. 2014) and several additional lineages most likely represent additional undescribed species (Fig. 2;Petzold et al. 2014;Fritz et al. 2015;Nagy et al. 2015;Vargas-Ramírez et al. 2016;Vamberger et al. 2018). ...
... Pelomedusa subrufa sensu stricto is widespread in southern Africa, ranging from southern Angola and Namibia eastward to Mozambique. The species also occurs beyond southern Africa in East Africa and has been introduced in Madagascar (Vargas-Ramírez et al. 2010;Wong et al. 2010;TTWG 2021). In southern Africa, its range marginally extends into northeastern South Africa, and in Limpopo Province, it occurs in close proximity to the morphologically similar species P. galeata (Vamberger et al. 2018). ...
Species-level phylogeny and especially phylogeography of African chelonians is a comparatively under-studied field of research. We review the current knowledge of phylogeny and phylogeography, highlight congruence of spatial phylogeographic patterns amongst chelonians and other taxa and suggest future research directions to address gaps in knowledge. Our review shows that phylogeographic and phylogenetic investigations have led to unexpected findings. For example, for Pelomedusa, a putatively wide-ranging mono-typic terrapin genus, cryptic diversity was revealed, with more than ten species being uncovered. The formerly recognized tortoise genus Homopus sensu lato was found to be paraphyletic with respect to Chersina. To resolve this situation, Homopus was restricted to the four-toed species H. areolatus and H. femoralis and the genus Chersobius was resurrected for the five-toed species C. boulengeri, C. signatus, and C. solus. Three previously recognized taxa were shown to be invalid, viz. the putatively extinct terrapin species Pelusios seychellensis and the tortoise subspecies Chersobius signatus cafer and Stigmochelys pardalis babcocki. Together with taxonomy, the knowledge of phylogeographic structuring sets a solid foundation for conservation measures and allows the identification of Management and Conservation Units. However, the current legislation, in particular the enforcement of the Nagoya Protocol under the Convention of Biological Diversity (CBD), has largely halted research on widely distributed taxa and turned the well-intended concept of Access and Benefit Sharing into a major impediment for conservation and research. The current situation leads for many species to a continued usage of outdated and incorrect taxonomic classifications resulting in an error cascade of conservation decisions. This is counterproductive to the aims of the CBD, that is, the protection of biodiversity. Sequencing historical DNA from museum specimens using aDNA approaches could be a short-term approach to mitigate, but not solve, this impediment.
... Arillo (1967) first recorded P. subrufa from the Arabian Peninsula in Yemen, and Gasperetti et al. (1993) considered P. subrufa from Saudi Arabia and Yemen to be part of this monotypic species. However, based on a comprehensive sampling effort across the species' range and analyzing nuclear and mitochondrial DNA (mtDNA) sequences, the Arabian population was found to be genetically deeply divergent (Vargas-Ramírez et al. 2010;Wong et al. 2010;Fritz et al. 2014). A subsequent taxonomic revision using morphological traits and mtDNA sequences formally split the widespread P. subrufa into 10 separate species and described the Arabian Helmeted Turtle as a species new to science, Pelomedusa barbata , with its type locality at Zinjibar, Abyan, Yemen. ...
... The plastron in mature males is concave. Wong et al. 2010;Alqahtani 2017) at elevations from sea level to 1800 m asl. Its distribution range is largely restricted to areas with higher rainfall with available surface water, as compared to the drier interior Arabian Peninsula. ...
... The Nile crocodile population from Madagascar shares two mtDNA haplotypes that are widespread on the continent and were recorded from Tanzania, Malawi, Zimbabwe, and South Africa (Van Asch et al. 2019). A phylogeographic research of the marsh terrapin reveals a similar spatial pattern, where the mtDNA haplotypes from Madagascar clustered together with haplotypes from Botswana, Namibia, Malawi, and the Democratic Republic of Congo (Vargas-Ramírez et al. 2010;Wong et al. 2010). These phylogeographic results also indicate that Crocodylus niloticus and Pelomedusa subrufa have recently arrived to the island. ...
Madagascar houses a peculiar and largely endemic biota, having ancient Gondwanan affinities. However, the faunal composite of many invertebrate groups on the island is poorly known. For a long time, it was believed that the freshwater leech fauna of Madagascar contains a salifid species (Salifidae) only. Here, we report on a historical record of Placobdelloides multistriatus (Johansson, 1909) (Glossiphoniidae), a widespread African species, from Andrahomana, Southern Madagascar. Franz Sikora (1863-1902), an Austrian traveler and collector, who visited Andrahomana in 1899 to excavate fossils from a cave, collected the leech sample. The two specimens were obtained from an unspecified turtle species. We assume that P. multistriatus may have arrived to Madagascar relatively recently (i.e., in the Late Pleistocene or Holocene) via a long-distance dispersal event from continental Africa with its reptilian hosts such as the Nile crocodile and marsh terrapin. Based on a review of the body of available literature, two more freshwater leech species are known to occur on Madagascar: Linta be Westergren & Siddall, 2004 (Salifidae) and Alboglossiphonia sp. (Glossiphoniidae). Our findings indicate that Madagascar houses at least three freshwater leech species and that some additional taxa may have been overlooked there due to the scarcity of sampling efforts in the island's freshwater bodies.
... The assumption, that these species lists are incomplete, is also supported by species groups such as the Egyptian cobra (Naja haje) (Trape et al. 2009) and the forest cobra (Naja melanoleuca) (Wüster et al. 2018) that have recently been shown to include additional new species. There are also taxonomic uncertainties brought about by superficial "look-alike" species and or those that may have been introduced through trade activities (e.g., Pelomedusidae spp.) (Vargas-Ramírez et al. 2010;Wong et al. 2010). However, as these are the species that were presented by owners when asked and aware of our visit in advance -it likely shows a good representation and is ultimately the only existing data available. ...
Our review of the CITES trade database confirmed that the ball python is the most exported species by Togo; with 1,657,814 live individuals-comprising 60% of all live reptiles-reported by importing countries since 1978 (almost 55,000 annually since 1992). In total, 99% of the ball pythons legally exported from Togo under CITES were intended for commercial use, presumably as exotic pets. Since the turn of the century, wild-sourced snakes exported from Togo have been largely replaced with ranched snakes, to the extent that in the last 10 years 95% of these live exports were recorded using CITES source code "R" with the majority destined for the USA. We found discrepancies in the CITES trade database that suggest ball python exports were consistently underestimated by Togo and that both ranched and wild-sourced ball python annual quotas have been exceeded on multiple occasions including as recently as 2017. Furthermore, our field visits to seven of these "python farms" revealed that they are also involved in the commercial trade in at least 46 other reptile species, including eight that are already involved in formal CITES trade reviews due to concerns regarding their sustainability and legality. Ranching operations in West Africa were once thought to provide a degree of protection for the ball python; however, in light of Nature Conservation 40: 65-91 (2020) A peer-reviewed open-access journal Neil D'Cruze et al. / Nature Conservation 40: 65-91 (2020) 66 recent research, there is growing concern that ranching may not confer any significant net conservation benefits. Further scrutiny and research are required to ensure the long-term survival of wild ball python and other reptile species populations in Togo.
... There are no significant geographical or climatic barriers in the sample area and gene flow between populations of ball pythons has likely occurred over the last 10,000 years. However, unlike our study, genetic studies focussed on wild populations of other savannah inhabitant reptile species in West Africa have revealed phylogenetically distinct clades [e.g., the African helmeted turtle (Pelomedusa subrufa) (Vargas-Ramírez et al. 2010;Wong et al. 2010), the Puff adder (Bitis arietans) (Barlow et al. 2013), and the Egyptian cobra (Naja haje) (Trape et al. 2009)]. Likewise, phylogenetically distinct clades have also been previously reported for ball python prey species [e.g., Misonne's soft-furred mouse (Praomys misonnei)] (Nicolas et al. 2011). ...
The ball python ( Python regius ) is the world’s most commonly traded python species for the “exotic” pet industry. The majority of these live snakes are produced via a number of python farms in West Africa that have been in operation since the 1960s and involved with “ranching” operations since the 1990s. However, to date no thorough taxonomic review or genetic studies have been conducted within its range, despite the fact that the evaluation of a species’ genetic variability is generally considered mandatory for effective management. We used mtDNA sequence data and eight polymorphic microsatellite markers to assess the underlying population genetic structure and to test the potential of the nuclear markers to assign farm individuals to wild reference populations in southern Togo. Despite the relatively large distances between sample locations, no significant genetic population structure was found, either in mtDNA sequence data or in the microsatellite data. Instead, our data indicate considerable gene flow among the locations. The absence of a distinct population subdivision may have resulted from an anthropogenic driven admixture of populations associated with commercial wildlife trade activity in recent decades. Given the ongoing largely unregulated nature of the commercial ranching of ball pythons in West Africa, should a wild release component continue, as a first measure we recommend that the Management Authorities should develop an action plan with specific release protocols for python farms to minimise any potential negative conservation impacts resulting from admixture (genetic pollution) between farmed and wild individuals.
... Together with their sister taxon, the African hinged terrapins (Pelusios), helmeted terrapins constitute the side-necked turtle family Pelomedusidae (TTWG 2017). While it was assumed for decades that all helmeted terrapins are conspecific (Boycott and Bourquin 2008;Branch 2008;Ernst and Barbour 1989;Mertens 1961, 1977), several investigations revealed deep genetic divergences between geographically coherent populations, which resemble or exceed the divergences of distinct Pelusios species (Fritz et al. 2011(Fritz et al. , 2014Petzold et al. 2014;Vamberger et al. 2018;Vargas-Ramírez et al. 2010;Wong et al. 2010). This resulted in the formal recognition of no less than 10 distinct species TTWG 2017;Vamberger et al. 2018). ...
Records from the putative gap in the distribution range of Pelomedusa galeata in western South Africa provide evidence for the occurrence of helmeted terrapins in those areas. Further research is needed to reveal the genetic and taxonomic identity of these populations.
Defining priorities is important both in research and in conservation, especially when knowledge gaps are hindering successful management. In this review, we quantify the knowledge gaps for all non-marine West African chelonians based on 21 criteria. Additionally, we combine these knowledge gaps with each species' maximum size, range size, presence in nationally protected areas, and IUCN Red List or TFTSG provisional status to introduce a ranking of species conservation priority in the region. Our analyses revealed a divergence between which species are lacking research studies and which would benefit most from conservation actions, though Cyclanorbis elegans is the species that is both the least-known and most-in-need of conservation. Broadly, Pelomedusidae are in the greatest need of research, yet they are also collectively the least threatened. Conversely, Trionychidae and Testudinidae have received greater research attention in most cases, however, these two families represent the greatest conservation priorities amongst West African chelonians. Our analyses also enabled us to evaluate which criteria representing aspects of chelonian biology have been most overlooked by the scientific community. Priorities for future research include reproductive and long-term population studies, each of which are critical for informing conservation actions and evaluating the results of those actions.
The present study reports on a case of high richness in an assemblage of non-native freshwater turtles in a suburban wetland of Tyrrhenian Central Italy (Torre Flavia Nature Reserve), providing evidence for rst observations of species at regional, national and continental levels. Following a standardized sampling procedure, 54 specimens belonging to seven taxa (ten taxa, including subspecies) were sampled. These included Trachemys scripta (overwintering in the nest of a juvenile, corroborating its reproduction in the wild), Graptemys pseudogeographica, Pelomedusa olivacea (rst observation recorded for Europe), Pseudemys concinna, Pseudemys nelsoni, Mauremys sinensis and an unclassi ed Kinosternidae (Kinosternon subrubrum subrubrum vel Sternotherus odoratus; rst observation recorded for Europe at the family level). Due to the high frequency of the most common species (Trachemys scripta: >80% in frequency), this non-native assemblage was characterized by high Simpson dominance, low Simpson diversity and low evenness values. This appears to be the rst evidence of a local hotspot of these non-native reptiles in Europe. These relevant data and their ecological implications (e.g., alien food webs) are discussed, as well as their conservation concerns and wetland management perspective.
We use a combination of phylogenetic analysis of mtDNA sequences and multivariate morphometrics to investigate the phylogeography and systematics of the Egyptian cobra (Naja haje) species complex. Phylogenetic analysis of mitochondrial haplotypes reveals a highly distinct clade of haplotypes from the Sudano–Sahelian savanna belt of West Africa, and that the haplotypes of Naja haje arabica form the sister group of North and East African N. h. haje. Multivariate morphometrics confirm the distinctness of the Arabian populations, which are consequently recognised as a full species, Naja arabica Scortecci. The Sudano-Sahelian populations are also found to represent a morphologically distinct taxon, and thus a separate species, which we describe as Naja senegalensis sp. nov. The new species differs from all other members of the N. haje complex by a combination of colour pattern and scalation characteristics (especially higher numbers of scale rows around the neck), and the possession of a unique clade of mtDNA haplotypes. The distribution of the new species includes savanna areas of West Africa, from Senegal to western Niger and Nigeria.
LEACHE A.D., CHONG R.A., PAPENFUSS T.J., WAGNER P., BÖHME W., SCHMITZ A., RÖDEL M.-O., LEBRETON M., INEICH I., CHIRIO L., BAUER A., ENIANG E.A., BAHA EL DIN S., 2009 – Phylogeny of the genus Agama based on mitochondrial DNA sequence data. Bonner zoologische Beiträge, 56(4): 273-278.
Existing techniques for estimating natural fluctuations of sea level and global ice-volume from the recent geological past exploit fossil coral-reef terraces or oxygen-isotope records from benthic foraminifera. Fossil reefs reveal the magnitude of sea-level peaks (highstands) of the past million years, but fail to produce significant values for minima (lowstands) before the Last Glacial Maximum (LGM) about 20,000 years ago, a time at which sea level was about 120m lower than it is today. The isotope method provides a continuous sea-level record for the past 140,000 years (ref. 5) (calibrated with fossil-reef data), but the realistic uncertainty in the sea-level estimates is around +/-20m. Here we present improved lowstand estimates-extending the record back to 500,000 years before present-using an independent method based on combining evidence of extreme high-salinity conditions in the glacial Red Sea with a simple hydraulic control model of water flow through the Strait of Bab-el-Mandab, which links the Red Sea to the open ocean. We find that the world can glaciate more intensely than during the LGM by up to an additional 20-m lowering of global sea-level. Such a 20-m difference is equivalent to a change in global ice-volume of the order of today's Greenland and West Antarctic ice-sheets.
The emydid turtle Callagur borneoensis nests on Malaysian ocean beaches with the true sea turtles. Adults were seen mainly in tidal upstream areas of the Perak and Setiu Rivers. It is likely that hatchlings must swim through the sea to reach the river mouths, yet they are intolerant of long term immersion in sea water when tested in the laboratory. Fasting turtles in the initial week of exposure undergo a net weight loss of 0.9 and 1.4% body weight/day in 50% and 100% sea water (35‰ salinity) respectively. In 25% sea water a net weight gain of 0.9% body weight/day was recorded. Turtles move to or remain in fresh water when given a choice between it and sea water in a divided tank. In 100% sea water, body water influx and efflux were 0.616 and 0.546 ml/100 g·h, respectively. This is equivalent to a turnover of 16-18% of the body water daily (81% weight is water). Influx must be mainly occurring through the skin and/or shell since turtles apparently do not drink 100% sea water. This is proven by the very low Na influx, 5.6 μmoles/100g·h, which could be accounted for if a 50g turtle "drank" only 10 μl/h of the radioactive bath. Na efflux is even lower (about 1 μmole/100g·h) and does not increase after injection of salt loads. Less than 0.5% of the total body Na content (82 μmoles/g) is lost daily. Hatchling C. borneoensis are not physiologically specialized for a life in estuaries of high salinity, yet they can survive for at least two weeks in 100% sea water.
Pseudemys nelsoni and Trachemys decussata inhabit brackish water in mainland areas of extreme southern Florida and on Grand Cayman Island. They appear to be intermediate in their salinity tolerance between truly freshwater forms and the highly specialized estuarine terrapin (Malaclemys). Unfed P. nelsoni (730-1240 g) had especially low rates of mass loss (primarily net water loss) in 100% sea water (about 0.4% initial mass/day). Smaller T. decussata (200-240 g) had higher values (about 0.8% /day), yet these rates were still lower than four values obtained on typical freshwater species (1.8-7.6% /day) held in 100% sea water. Mean whole body water effluxes in 100% sea water of adult P. nelsoni and T. decussata larger than 60 g were low (0.24-0.47 ml/100 g·h). Hatchling T. decussata had much higher rates of water efflux (1.0 ml/100 g·h). Sodium effluxes in 100% sea water were low (less than 100 μmol/100 g·h) in all size classes. There was no stimulation in sodium efflux after salt loading in P. nelsoni, nor in T. decussata after dehydration in saline solutions. This implies the lack of salt glands in these species. Sodium influx in 100% sea water was very low in adult P. nelsoni and in T. decussata larger than 200 g. There was a progressive increase in sodium influx with declining size in T. decussata, so that hatchlings underwent a considerable net uptake of sodium in sea water. Hatchling T. decussata fed fish ad libitum were unable to maintain mass or grow when the salinity exceeded 41% sea water. Juveniles of about 80 g grew at salinities up to 59% sea water, representing a significant increase in tolerance above that of the hatchlings. Additionally, 80 g turtles grew significantly faster in 25% sea water than in fresh water. Large individuals (>200 g) of both species tolerated immersion in 100% sea water for prolonged periods (at least 10-24 days). Their natural habitats vary seasonally in salinity, but remain on average quite dilute due to rainfall.
THE evolution of the Red Sea depression and the extent within it of
oceanic crust have been widely discussed1-5. It is generally
accepted that the axial trough is floored by oceanic lithosphere formed
at a constructive margin over the last 3-4 Myr by spreading at a rate of
about 1.0 cm yr-1 per flank2,6. It is also clear
from stratigraphic continuity and the trend of isofacial lines that the
opening of the Red Sea started less than 45 Myr ago after a long period
of tectonic and magmatic quiesence7,8. Two areas of
contention exist. First, how much of the Red Sea on either side of the
axial trough is underlain by oceanic crust, and second, when was this
oceanic crust formed?