Anatomy of the fully formed chondrocranium of Podocnemis unifilis (Pleurodira: Podocnemididae)

This study describes the anatomy of the chondrocranium of Podocnemis unifilis (Pleurodira, Podocnemididae), based on recently hatched specimens, and cleared and double‐stained specimens. The orbitotemporal region is dramatically different from those observed for other species of turtles in that the: (1) planum supraseptale is greatly reduced and present only as tiny projections on the posterodorsal margin of the interorbital septum, (2) pila metoptica is free from all neighbouring structures and bifurcates distally, (3) pila antotica is greatly reduced, (4) foramina for optic nerve, ophthalmic artery and oculomotor nerves are open dorsally by virtue of this species lacking the taenia marginalis and taenia medialis, and (5) tectum synoticum is present and invested dorsally by the supraoccipital, despite the fact that this bone forms by replacement of the supraoccipital. The unique morphology of the pila metoptica is explained either as de novo formation of processes on the terminus of this cartilage or by retention of portions of the taenia medialis (anteriorly) and pila antotica or pila accessoria (posteriorly). Variation in the orbitotemporal region presented here is discussed for two other pleurodiran turtles (Phrynops hilarii and Emydura subglobosa) and briefly compared with the anatomy observed in Cryptodira.     

Patterns of chondrification and ossification in the skull of Graptemys pseudogeographica,the false map turtle (Emydidae)

Patterns of ossification and chondrification are well‐described for several species of turtles, but details of the chondrocranial anatomy are known for only a handful of species. Cleared and double‐stained embryos of Graptemys pseudogeographica were used to examine the fully formed chondrocranium and the formation, chondrification, and ossification of the cranium. The chondrocranium of G. pseudogeographica possesses an unusually large, irregularly shaped foramen epiphaniale that is joined with the fenestra olfactoria. As in other emydids, and many turtles generally, the taenia marginalis is present only as a small projection and the taenia medialis is lacking in mature stages of embryonic development. Ossification data for G. pseudogeographica are consistent with those of other Testudines in that the dentary and maxilla (dermal elements of the upper and lower jaws) ossify early, whereas the articular (an endochondral bone of the lower jaw) ossifies relatively late. Additionally, comparative ossification shows that the vomer is quite variable in its relative timing of ossification across Testudines.     

The ontogeny of the shell in side‐necked turtles,with emphasis on the homologies of costal and neural bones

Although we are starting to understand the molecular basis of shell development based on the study of cryptodires, basic comparative ontogenetic data for the other major clade of living turtle, the pleurodires, are largely missing. Herein, the developmental and phylogenetic relation between the bony shell and endoskeleton of Pleurodira are examined by studying histological serial sections of nine specimens of three different species, including an ontogenetic series of Emydura subglobosa. Emphasis is given to the portion of the carapace in which ribs and vertebral spinous processes become part of the carapace. Central questions are how neurals and costals are formed in pleurodiran turtles, whether costals and neurals are of endoskeletal or exoskeletal origin, and what ontogenetic factors relate to neural reduction of some Pleurodira. The neurals and costals do not develop as independent ossification centers, but they are initial outgrowths of the periosteal collar of endoskeletal ribs and neural arches. Slightly later in development, the ossification of both shell elements continues without a distinct periosteum but by metaplastically ossifying precondensed soft‐tissue integumentary structures. Through ontogeny, ribs of the turtles studied are closely associated with the hypaxial intercostalis musculature while epaxial interspinalis musculature connects the neural arches. We here propose an alternative structural hypothesis for the neural reduction and, ultimately, the complete loss of the neural series. The complete reduction of neurals in Emydura spp. may be linked to heterochrony, accompanied by a restricted influence of epaxial musculature and epidermal–dermal interaction in shell bone formation. J. Morphol., 2008. © 2008 Wiley‐Liss, Inc.     

The ontogeny of the chondrocranium in Clarias gariepinus: trends in siluroids

The ontogeny of the chondrocranium of 31 different stages of the African catfish Clarias gariepinus (Siluroidei: Clariidae) was studied, both from cleared and stained, and sectioned material. The fish ranged from 4.1 (1 day post-hatching) to 127.0 mm SL (100 days post-hatching). The chondrocranium of C. gariepinus seemed to correspond to the general adaptive trends in siluroids, especially in relation to the reduction of eye size and the dorso-ventral flattening of the skull. The platybasic neurocranium involved several modifications related to the trabecular bars, the hypophyseal fenestra, the ethmoid region and even the olfactory nerves. Certain reductions were present, which have been observed in all siluroids (e.g. absence of the pila lateralis, the commissura lateralis, the myodomes) or are part of a variable trend within siluroids (e.g. reduction of the taenia marginalis anterior and the tectum synoticum). Compared with some other siluroid species, the neurocranium of C. gariepinus is well developed, for example in the otic region. The same was observed in the splanchnocranium where some general siluroid trends persist (e.g. isolation of palatine from pterygoquadrate, presence of 'hyo-symplectic-pterygoquadrate' plate). Some trends, as observed in other siluroids, were present also (e.g. interhyal continuous with suspensorium and ceratohyal, Meckel's cartilage initially continuous with the suspensorium). The branchial basket is well developed as all expected elements are present (basibranchials I-IV, hypobranchials I-IV, ceratobranchials I-V, epibranchials I-IV). Based on the observed ontogeny of C. gariepinus and data from the literature, a hypothesis was formulated which indicated the presence of a general reductional trend within siluroids. In C. gariepinus , all four (I-IV) infrapharyngobranchials develop, although the anterior two are much reduced and fused with each other.     

Pareiasaur phylogeny and the origin of turtles

The evolutionary relationship of all the valid species (and thus genera) of pareiasaurs are assessed through a phylogcnctic analysis of these taxa together with turtles, Owenetta, Barasaurus, Sclerosaurus, procolophonids, lanthanosuchids, nyctiphruretids, and nycterolctcrids. 128 os-teological characters were used, and almost all relevant taxa were examined. The results confirm that among these taxa, pareiasaurs and turtles form a robust clade, to the exclusion of all other taxa including procolophonids. However, pareiasaurs might not be the mono-phyletic sister group of turtles, as previously suggested. Rather, there is some evidence that pareiasaurs are paraphyletic with respect to (i.e. ‘ancestral to’) turtles. Among pareiasaurs, the early, large, heavily ossified forms such as Brady.saurus are most distantly related to turtles. These forms are characterized by rather smooth skulls, and dermal armour restricted to the dorsal midline. More closely related to turtles are forms such as Scutosaurus, Pareiasuchus, and Elginia. These taxa form a distinct clade of pareiasaurs, characterized by a very ‘mammallike’ pelvis, elaborate cranial ornamentation and a loose covering of osteoderms over the entire dorsum. The late, dwarf pareiasaurs Nanoparia, Anthodon, and Pumiliopareia are the nearest relatives of turtles. These forms exhibit otherwise uniquely turtle features such as a rigid covering of dermal armour over the entire dorsal region, expanded flattened ribs, cylindrical scapula blade, great reduction of humeral torsion (to 25^o), greatly developed trochanter major, offset femoral head, and reduced cnemial crest of the tibia. Thus, many features thought to be restricted to turtles (and thus to have evolved simultaneously with the turtle shell) actually arose earlier, at various points along the pareiasaurian stem lineage. The identification of the nature and sequence of anatomical changes leading to the origin of turtles, and the possibility that turtles are derived from dwarf pareiasaurs, should have important implications for speculations on the evolutionary biology of turtle origins.     

Seasonal and diel dive performance and behavioral ecology of the bimodally respiring freshwater turtle <Emphasis Type="Italic">Myuchelys bellii</Emphasis> of eastern Australia

Freshwater turtles have an extraordinary physiological ability to endure dive times that can range from days to months using aquatic respiration. In cryptodires (e.g., white-lipped mud turtle Kinosternon leucostomum) aquatic respiration is via buccal or cutaneous routes whereas in pleurodires (e.g., Fitzroy River turtle Rheodytes leukops), it is achieved primarily via specialized cloacal bursae. This study records the voluntary diving performance of the western sawshelled turtle Myuchelys bellii in Bald Rock Creek from the temperate zone of the Murray–Darling Basin of Australia. Myuchelys bellii has a moderately specialized cloacal bursae morphology compared to other pleurodiran turtles and displays impressive dive durations spanning more than 15 days during the winter months. This is attributed to its ability to maintain aerobic dives via its cloacal bursae and low water temperatures in winter. Myuchelys bellii seasonal and diel diving performance, including its crepuscular habit, is comparable to R. leukops and Elseya albagula. This study also recorded the first aquatic hibernation at depth (>3 m) for any freshwater turtle; and only the second pleurodire to demonstrate aquatic hibernation as an overwintering strategy. Observed thermoregulation behavior in M. bellii is believed to provide multiple life history benefits.     

Climate change affects the early-life history of a freshwater turtle in a severely drying region

Freshwater turtles are one of the most threatened vertebrate groups. Climate change is a major threat to these species, with impacts affecting all life-history stages. There is currently a limited understanding of how changes in climate may alter the environmental triggers for hatching and emergence from the nests of freshwater turtle hatchlings. This precludes making predictions about how climate change may impact freshwater turtle recruitment success. The southwestern snake-necked turtle (Chelodina oblonga) is endemic to south-western Australia, a global biodiversity hotspot that has undergone severe climatic drying. Recruitment failure is thought to be occurring in many populations of the species. However, there is little understanding as to how environmental change may be influencing recruitment. This study aimed to: (1) determine the incubation duration and hatching and hatchling emergence success of C. oblonga, (2) determine if the species exhibits hatching or emergence synchrony and/or delayed emergence and (3) quantify the effects of temperature and rainfall on hatchling emergence. Using this information, the study assesses how climatic drying and warming may be impacting C. oblonga's early life-history. Between 2018 and 2020 nest sites were monitored around a large urban wetland with weekly assessments of egg and hatchling status. Incubation duration and hatching and hatchling emergence success were calculated, and generalized linear models were built to determine how temperature and/or rainfall predicted emergence. Hatchlings either emerged shortly after hatching or overwintered in the nest, and both hatching and emergence were asynchronous. Both emergence periods were positively associated with temperature and rainfall. This study reveals that incubation duration, hatching success, hatchling emergence and survival are all likely to be impacted by recent and projected climate change, and especially drying. Warming and drying are predicted for many temperate regions globally, and it is therefore important that their impacts on the early life history of freshwater turtles be better understood.     

Predicted distributions and abundances of the sea turtle ‘lost years’ in the western North Atlantic Ocean

Oceanic dispersal characterizes the early juvenile life-stages of numerous marine species of conservation concern. This early stage may be a ‘critical period’ for many species, playing an overriding role in population dynamics. Often, relatively little information is available on their distribution during this period, limiting the effectiveness of efforts to understand environmental and anthropogenic impacts on these species. Here we present a simple model to predict annual variation in the distribution and abundance of oceanic-stage juvenile sea turtles based on species’ reproductive output, movement and mortality. We simulated dispersal of 25 cohorts (1993–2017) of oceanic-stage juveniles by tracking the movements of virtual hatchling sea turtles released in a hindcast ocean circulation model. We then used estimates of annual hatchling production from Kemp's ridley Lepidochelys kempii (n = 3), green Chelonia mydas (n = 8) and loggerhead Caretta caretta (n = 5) nesting areas in the northwestern Atlantic (inclusive of the Gulf of Mexico, Caribbean Sea and eastern seaboard of the U.S.) and their stage-specific mortality rates to weight dispersal predictions. The model's predictions indicate spatial heterogeneity in turtle distribution across their marine range, identify locations of increasing turtle abundance (notably along the U.S. coast), and provide valuable context for temporal variation in the stranding of young sea turtles across the Gulf of Mexico. Further effort to collect demographic, distribution and behavioral data that refine, complement and extend the utility of this modeling approach for sea turtles and other dispersive marine taxa is warranted. Finally, generating these spatially-explicit predictions of turtle abundance required extensive international collaboration among scientists; our findings indicate that continued conservation of these sea turtle populations and the management of the numerous anthropogenic activities that operate in the northwestern Atlantic Ocean will require similar international coordination.     

Effects of wetland connectivity on overwintering and movement behaviours of Australian freshwater turtles

Freshwater turtles are important consumers in Australian freshwater ecosystems. They serve as scavengers, nutrient regulators, and as food sources and Totems for Traditional Owners throughout Australia. Despite their importance, most Australian freshwater turtle species are declining. The impact of winter wetland drying on turtle populations remains unknown, and winter exposure of hibernating turtles may be an important additional source of mortality. We aimed to examine turtle responses to seasonal and episodic wetland drying in wetlands using acoustic telemetry and active trapping. Wetlands were chosen that spanned a range of hydrological connectivity to the adjacent Edward/Kolety-Wakool River. We found that tagged Emydura macquarii typically exit wetlands disconnected from the adjacent permanent river prior to winter, and overwinter in the river. Female E. macquarii rapidly re-entered ‘home’ wetlands (wetlands in which they were initially tagged) the following spring, whereas males tended to leave the study area, returning occasionally. Although we were not able to evaluate a winter drying event, one of the wetlands experienced partial summer drying. All three local turtle species (E. macquarii, Chelodina expansa, C. longicollis) exited the wetland long before winter drying would have become a potential threat. Our results suggest that turtles in this system may be protected from winter wetland drying because they move to the adjacent permanent river prior to winter. Spending the winter in the river channel reduces the risks of being trapped in a drying wetland as temperatures drop in winter.     

The physiology of diving in a north-temperate and three tropical turtle species

We examined changes in blood gases, plasma ions, and acid-base status during prolonged submergence (6 h) of four aquatic turtle species in aerated water at 20 °C. Our objective was to determine whether the temperate species, Chrysemys picta bellii, exhibits greater tolerance to submergence apnea than the tropical species, Pelomedusa subrufa, Elseya novaeguineae, and Emydura subglobosa. Blood was sampled from indwelling arterial catheters for measurements of blood PO₂, PCO₂, pH, and hematocrit and for plasma concentrations of lactate, glucose, Na⁺, K⁺, Cl⁻, total Ca, and total Mg. The pattern of change was similar in all species: a combined respiratory and metabolic acidosis associated with a marked decrease of blood PO₂. The severity of the acidosis developed in the temperate species, however, was significantly less than that of the tropical turtles. Lactate rose significantly and HCO₃ ⁻ fell proportionately in all turtles; changes in other plasma ion concentrations were small but were generally in the directions consistent with compensatory exchanges with other body compartments; i.e., cations (K⁺, Ca, and Mg increased) and anions (Cl⁻ decreased). The results indicate that hypoxia tolerance is a conserved trait in turtles, even in those that do not experience enforced winter submergence, and that the temperate species may be superior in this capacity because of reduced metabolic rate. Accepted: 3 March 1999     

Measuring energy expenditure in sub-adult and hatchling sea turtles via accelerometry

Measuring the metabolic of sea turtles is fundamental to understanding their ecology yet the presently available methods are limited. Accelerometry is a relatively new technique for estimating metabolic rate that has shown promise with a number of species but its utility with air-breathing divers is not yet established. The present study undertakes laboratory experiments to investigate whether rate of oxygen uptake ( o ₂) at the surface in active sub-adult green turtles Chelonia mydas and hatchling loggerhead turtles Caretta caretta correlates with overall dynamic body acceleration (ODBA), a derivative of acceleration used as a proxy for metabolic rate. Six green turtles (25–44 kg) and two loggerhead turtles (20 g) were instrumented with tri-axial acceleration logging devices and placed singly into a respirometry chamber. The green turtles were able to submerge freely within a 1.5 m deep tank and the loggerhead turtles were tethered in water 16 cm deep so that they swam at the surface. A significant prediction equation for mean o ₂ over an hour in a green turtle from measures of ODBA and mean flipper length (R² = 0.56) returned a mean estimate error across turtles of 8.0%. The range of temperatures used in the green turtle experiments (22–30°C) had only a small effect on o ₂. A o ₂-ODBA equation for the loggerhead hatchling data was also significant (R² = 0.67). Together these data indicate the potential of the accelerometry technique for estimating energy expenditure in sea turtles, which may have important applications in sea turtle diving ecology, and also in conservation such as assessing turtle survival times when trapped underwater in fishing nets.     

Triassic turtle tracks and the origin of turtles

Turtle (Testudines) tracks, Chelonipus torquatus, reported from the early Middle Triassic (Anisian) of Germany, and Chelonipus isp. from the late Early Triassic (Spathian) of Wyoming and Utah, are the oldest fossil evidence of turtles, but have been omitted in recent discussions of turtle origins. These tracks provide significant clues as to how early the turtle Bauplan originated. Turtle trackways are quite distinctive: the manus and pes form tracks nearly parallel to the midline and indicate an unusually wide gait in which the trackway width is nearly equal to the stride length. These tracks do not fit what would be expected to be made by Triassic Pappochelys or Odontochelys, a supposed prototurtle and an early turtle, respectively. In contrast, these tracks are consistent with what would be expected from the Triassic turtles Proganochelys and Palaeochersis. The features inferred to be present in Triassic turtle tracks support the notion that Odontochelys is a derived aquatic branch of the turtle stem lineage rather than the ancestral state of all turtles. Chelonipus also resembles the Permian track Pachypes dolomiticus, generally assigned to a pareiasaur trackmaker. These revelations highlight the need to consider all available evidence regarding turtle origins, rather than just the body fossils.     

Not all management is equal: a comparison of methods to increase wood turtle population viability

Management generally targets the most tractable life stage to rescue declining populations; however, that stage may not have the largest influence on recovery. Freshwater turtles are declining globally and early stages are frequently targeted for management, although the effectiveness of these actions on population growth are relatively unknown because of incomplete demographic data. We estimated the hatchling yearly survival rate for a freshwater turtle in the field using in situ enclosures to collect missing demographic information. We used these data to develop demographic models to calculate growth rate for a hypothetical, declining population of wood turtles (Glyptemys insculpta) in Wisconsin, USA, 2014–2019. We modeled growth for populations across a range of scenarios from no management to combinations of nest protection and head-starting at varying levels of effort. Nest protection alone did not increase population growth rate, while head-starting alone increased population growth by 0.07, with the largest increase in growth rate, 0.11, resulting from combinations of both approaches. No combination of nest protection and head-starting, without an increase in adult survival rate from the observed 0.88 to ≥0.95, led to population stabilization or increase. Populations of freshwater turtles, like the wood turtle, will likely only recover with a multi-faceted approach that targets multiple life stages simultaneously.     

Some like it cold: the glossiphoniid parasites of the Sicilian endemic pond turtle Emys trinacris (Testudines,Emydidae), an example of ‘parasite inertia’?

The freshwater turtles of the genus Emys and some leech species of the family Glossiphoniidae are the only Palaearctic representatives of primarily Nearctic taxa, which jointly colonized Eurasia and the Maghreb during the Miocene. The strict trophic relationships occurring between the glossiphoniid parasite leech Placobdella costata and its host, the emydid Emys orbicularis, make them a prime example of host–parasite cophylogenetic evolution. In the light of the discovery of the Sicilian cryptic endemic species Emys trinacris, which is the sister species to the widespread Palaearctic E. orbicularis, the possible cophylogenetic divergence of the turtle hosts and their leech parasites was investigated. In spite of the deep divergence scored between the two pond turtle species and of their allopatric distribution, their leech parasites proved to be conspecific and indistinguishable based on the implemented molecular marker. This unexpected decoupling might likely be ascribed to the different dispersal abilities of the two taxa and/or to the recent, human‐mediated introduction of the leech parasites in Sicily. If this last scenario is confirmed, the long‐term effects of the introduced leech parasite on the endemic Sicilian pond turtle Emys trinacris should be carefully monitored. In the frame of this study, representatives of the widely spread predatory leech Helobdella stagnalis were observed on E. trinacris. Molecular analyses of their stomach content allowed to rule out the possibility of the existence of a trophic relationships between these two taxa, in contrast to what was previously suspected, and suggest that H. stagnalis specimens were rather attached to the turtles for non‐nutritional reasons.     

Exclusive predation of sea turtle hatchlings by juvenile blacktip reef sharks Carcharhinus melanopterus at a turtle nesting site in Malaysia

This study reports the discovery of the exclusive predation of sea turtle hatchlings by several juvenile blacktip reef sharks (Carcharhinus melanopterus) in Chagar Hutang bay on Redang Island, Malaysia, in the South China Sea. Three dead specimens of C. melanopterus were retrieved from ghost nets, and the entire digestive tracts of these sharks solely contained the partially digested bodies of sea turtle hatchlings, with no evidence of the remains of any other prey. Thus, juvenile C. melanopterus may opportunistically feed primarily on turtle hatchlings during times when hatchling abundance is high.     

Past, current and future thermal profiles of green turtle nesting grounds: Implications from climate change

Sex determination and hatching success in sea turtles is temperature dependent and as a result global warming poses a threat to sea turtles. Warmer sand temperatures may skew sea turtle population′s sex ratios towards predominantly females and decrease hatching success. Therefore, understanding the rates at which sand temperatures are likely to increase as climate change progresses is warranted. We recorded sand temperature and used historical sea surface and air temperature to model past and to predict future sand temperature under various scenarios of global warming at key sea turtle nesting grounds (n = 7) used by the northern Great Barrier Reef (nGBR) green turtle, Chelonia mydas, population. Reconstructed temperatures from 1990 to the present suggest that sand temperatures at the nesting sites studied have not changed significantly during the last 18 years. Current thermal profile at the nesting grounds suggests a bias towards female hatchling production into this population. Inter-beach thermal variance was observed at some nesting grounds with open areas in the sand dune at northern facing beaches having the warmest incubating environments. Our model projections suggest that a near complete feminization of hatchling output into this population will occur by 2070 under an extreme scenario of climate change (A1T emission scenario). Importantly, we found that some nesting grounds will still produce male hatchlings, under the most extreme scenario of climate change, this finding differs from predictions for other locations. Information from this study provides a better understanding of possible future changes in hatching success and sex ratios at each site and identifies important male producing regions. This allowed us to suggest strategies that can be used at a local scale to offset some of the impacts of warmer incubating temperatures to sea turtles.