Evolution of the Nasal Structure in the Lower Tetrapods

The gross structure of the nasal cavities and the distributionof the various types of epithelium lining them are describedbriefly; each living order of amphibians and reptiles possessesa characteristic and distinctive pattern. In most groups thereare two sensory areas, one lined by olfactory epithelium withnerve libers leading to the main olfactory bulb and the otherby vomeronasal epithelium with fibers to the accessory bulb.All amniotes except turtles have the vomeronasal epitheliumin a ventromedial outpocketing of the nose, the Jacobson's organ,and have one or more conchae projecting into the nasal cavityfrom the lateral wall. Although urodeles and turtles possessthe simplest nasal structure, it is not possible to show thatthey are primitive or to define a basic pattern for either amphibiansor reptiles; all the living orders are specialized and the nasalanatomy of extinct orders is unknown. Thus it is impossible,at present, to give a convincing picture of the course of nasalevolution in the lower tetrapods.     

The ontogeny of the olfactory system in ceratophryid frogs (Anura,Ceratophryidae)

The aquatic‐to‐terrestrial shift in the life cycle of most anurans suggests that the differences between the larval and adult morphology of the nose are required for sensory function in two media with different physical characteristics. However, a better controlled test of specialization to medium is to compare adult stages of terrestrial frogs with those that remain fully aquatic as adults. The Ceratophryidae is a monophyletic group of neotropical frogs whose diversification from a common terrestrial ancestor gave rise to both terrestrial (Ceratophrys, Chacophrys) and aquatic (Lepidobatrachus) adults. So, ceratophryids represent an excellent model to analyze the morphology and possible changes related to a secondary aquatic life. We describe the histomorphology of the nose during the ontogeny of the Ceratophryidae, paying particular attention to the condition in adult stages of the recessus olfactorius (a small area of olfactory epithelium that appears to be used for aquatic olfaction) and the eminentia olfactoria (a raised ridge on the floor of the principal cavity correlated with terrestrial olfaction). The species examined (Ceratophrys cranwelli, Chacophrys pierottii, Lepidobatrachus laevis, and L. llanensis) share a common larval olfactory organ composed by the principal cavity, the vomeronasal organ and the lateral appendix. At postmetamorphic stages, ceratophryids present a common morphology of the nose with the principal, middle, and inferior cavities with characteristics similar to other neobatrachians at the end of metamorphosis. However, in advanced adult stages, Lepidobatrachus laevis presents a recessus olfactorius with a heightened (peramorphic) development and a rudimentary (paedomorphic) eminentia olfactoria. Thus, the adult nose in Lepidobatrachus laevis arises from a common developmental ‘terrestrial’ pathway up to postmetamorphic stages, when its ontogeny leads to a distinctive morphology related to the evolutionarily derived, secondarily aquatic life of adults of this lineage.     

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.     

Driftnet fishery threats sea turtles in the Atlantic Ocean

Fisheries are recognised as a major threat to sea turtles worldwide. Oceanic driftnets are considered the main cause of the steep decline in Pacific Ocean populations of the leatherback sea turtle Dermochelys coriacea. The world’s largest leatherback population nests in West Africa and migrates across the Atlantic Ocean to feed off the South American coast. There, the turtles encounter a range of fisheries, including the Brazilian driftnet fishery targeting hammerhead sharks. From 2002 to 2008, 351 sea turtles were incidentally caught in 41 fishing trips and 371 sets. Leatherbacks accounted for 77.3% of the take (n = 252 turtles, capture rate = 0.1405 turtles/km of net), followed by loggerheads Caretta caretta (47 individuals, capture rate = 0.0262 turtles/km of net), green turtles Chelonia mydas (27 individuals, capture rate = 0.0151 turtles/km of net) and unidentified hard-shelled turtles (25 individual, capture rate = 0.0139 turtles/km of net) that fell off the net during hauling. Immediate mortality (i.e., turtles that were dead upon reaching the vessel, excluding post-release mortality) was similar among the species and accounted for 22.2 to 29.4% of turtles hauled onboard. The annual catch by this fishery ranged from 1,212 to 6,160 leatherback turtles, as estimated based on bootstrap procedures under different fishing effort scenarios in the 1990s. The present inertia in law and enforcement regarding gillnet regulations in Brazil could result in the reestablishment of the driftnet fishery, driving rates of leatherback mortality to levels similar to those observed in previous decades. This development could potentially lead to the collapse of the South Atlantic leatherback population, mirroring the decline of the species in the Pacific. In light of these potential impacts and similar threats to other pelagic mega fauna, we recommend banning this type of fishery in the region.     

The aquatic Lystrosaurus: A palaeontological myth

Evidence previously cited for the aquatic nature of the Triassic mammal‐like reptile Lystrosaurus is reviewed. It is concluded that this evidence does not constitute a convincing case.

General adaptations of aquatic tetrapods are reviewed and applied to the morphology of Lystrosaurus, in order to determine whether aquatic adaptations not previously sought in Lystrosaurus are present It is concluded that few or any such adaptations are present. Such as are, for example a widened knee and flared scapula blade, are as compatible with a digging function, as with swimming.

Nevertheless, the distinctive nature of the skull and to a lesser extent the postcranial skeleton of Lystrosaurus stands out, and several features require functional interpretation. These include: a downwardly‐directed and elongated snout, a short and high temporal region, a pear‐shaped external nasal opening bounded by a rugose ridge, slight dorsal flaring of the scapula, a powerful forelimb and wide knee joint These are dealt with elsewhere (King and Cluver, 1991).     

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.     

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     

The influence of body size on the diving behaviour and physiology of the bimodally respiring turtle, Elseya albagula

In aquatic vertebrates that acquire oxygen aerially dive duration scales positively with body mass, i.e. larger animals can dive for longer periods, however in bimodally respiring animals the relationship between dive duration and body mass is unclear. In this study we investigated the relationships between body size, aquatic respiration, and dive duration in the bimodally respiring turtle, Elseya albagula. Under normoxic conditions, dive duration was found to be independent of body mass. The dive durations of smaller turtles were equivalent to that of larger individuals despite their relatively smaller oxygen stores and higher mass specific metabolic rates. Smaller turtles were able to increase their dive duration through the use of aquatic respiration. Smaller turtles had a relatively higher cloacal bursae surface area than larger turtles, which allowed them to extract a relatively larger amount of oxygen from the water. By removing the ability to respire aquatically (hypoxic conditions), the dive duration of the smaller turtles significantly decreased restoring the normal positive relationship between body size and dive duration that is seen in other air-breathing vertebrates.     

Oropharyngeal morphology in the basal tortoise Manouria emys emys with comments on form and function of the testudinid tongue

In tetrapods, the ability to ingest food on land is based on certain morphological features of the oropharynx in general and the feeding apparatus in particular. Recent paleoecological studies imply that terrestrial feeding has evolved secondarily in turtles, so they had to meet the morphological oropharyngeal requirements independently to other amniotes. This study is designed to improve our limited knowledge about the oropharyngeal morphology of tortoises by analyzing in detail the oropharynx in Manouria emys emys. Special emphasis is placed on the form and function of the tongue. Even if Manouria is considered a basal member of the only terrestrial turtle clade and was hypothesized to have retained some features reflecting an aquatic ancestry, Manouria shows oropharyngeal characteristics found in more derived testudinids. Accordingly, the oropharyngeal cavity in Manouria is richly structured and the glands are large and complexly organized. The tongue is large and fleshy and bears numerous slender papillae lacking lingual muscles. The hyolingual skeleton is mainly cartilaginous, and the enlarged anterior elements support the tongue and provide insertion sides for the well‐developed lingual muscles, which show striking differences to other reptiles. We conclude that the oropharyngeal design in Manouria differs clearly from semiaquatic and aquatic turtles, as well as from other reptilian sauropsids. J. Morphol., 2011. © 2011 Wiley‐Liss, Inc.     

Effects of release method on the survival,somatic growth,and body condition of headstarted turtles

Headstarting involves ex situ rearing of vulnerable life stages, then releasing individuals into the wild once they are larger and less vulnerable to predation. Sometimes, headstarted animals display underdeveloped behaviors that may lead to an acclimation period of reduced survival and growth after release. Using data from a 6-year headstarting program, we tested whether the early release condition affected survival, body condition, and somatic growth rate in 2 groups of headstarted Blanding's turtles (Emydoidea blandingii) released into Rouge National Urban Park (RNUP) in Toronto, Ontario, Canada. The first group included turtles released directly into the wild (i.e., hard release). The second group included turtles released into an in situ enclosure in which individuals remained for a week without food supplementation before being fully released into the wild (i.e., delayed release). Release condition did not affect survival or growth rate. In the delayed-release group, body condition initially declined rapidly and remained low for up to 1 year after release. Given the lack of wild juveniles in RNUP, we compared body condition of headstarted turtles at various time points since release to similar-sized wild juveniles from 2 other Ontario populations, one from Algonquin Provincial Park (APP) and one near Lake Erie (LE). Body condition of headstarted turtles was similar to those of wild APP turtles regardless of release method, and higher than those of wild LE turtles. Our results indicate that delayed release did not improve post-release outcomes for headstarted turtles in an urban landscape and headstarted turtles sustain similar health metrics as wild turtles.     

The effects of temperature and inter-individual variation on the locomotor performance of juvenile turtles

The effects of temperature on aquatic and terrestrial locomotor performance, including measures of burst speed, endurance, and righting response, the inter-individual correlation between measures of locomotor performance, and the temporal repeatability of performance were assessed in juvenile western painted turtles, Chrysemys picta bellii. Locomotor performance increased as temperature increased, with Q ₁₀ values ranging from 1.33 to 1.98 for burst speed and 2.28 to 2.76 for endurance measures. Righting response performance also increased with temperature. Aquatic and terrestrial measures of locomotor performance were highly correlated; however, righting response was not correlated with any other measure of performance. Measures of terrestrial locomotor performance were highly repeatable over the entire 30-week study period, whereas aquatic locomotor performance was only repeatable through week 12. The righting response was repeatable over a 6-week study period. Both the interindividual variation and temperature effects on locomotor performance likely influences the survival of turtles, especially juveniles, by affecting the length of time turtles are exposed to potential predators and their ability to escape.     

Chromosomal relationships of the tortoises (family Testudinidae)

Banded chromosomes of five species of testudinid turtles (Geochelone pardalis, G. elongata, G. elephantopus, Gopherus berlandieri, and G. polyphemus) reveal little variation within either genus, although there are differences in amount and distribution of heterochromatin between Geochelone pardalis and G. elongata. The chromosomal position and size of the nucleolar-organizer region differs between species of the two genera.Comparisons of standard karyotypes of these species and Malacochersus tornieri with data in the literature on other tortoises show a diploid number of 52 characterizes the family. These data are consistent with those for other families which show turtles are karyotypically conservative. G-banded chromosomes of Geochelone are identical to those of Chinemys reevesi, a karyotypically primitive batagurine emydid, supporting a derivation of the tortoises from a batagurine ancestor.     

The Head and Neck Anatomy of Sea Turtles (Cryptodira: Chelonioidea) and Skull Shape in Testudines

Background

Sea turtles (Chelonoidea) are a charismatic group of marine reptiles that occupy a range of important ecological roles. However, the diversity and evolution of their feeding anatomy remain incompletely known.

Methodology/Principal Findings

Using computed tomography and classical comparative anatomy we describe the cranial anatomy in two sea turtles, the loggerhead (Caretta caretta) and Kemp’s ridley (Lepidochelys kempii), for a better understanding of sea turtle functional anatomy and morphological variation. In both taxa the temporal region of the skull is enclosed by bone and the jaw joint structure and muscle arrangement indicate that palinal jaw movement is possible. The tongue is relatively small, and the hyoid apparatus is not as conspicuous as in some freshwater aquatic turtles. We find several similarities between the muscles of C. caretta and L. kempii, but comparison with other turtles suggests only one of these characters may be derived: connection of the m. adductor mandibulae internus into the Pars intramandibularis via the Zwischensehne. The large fleshy origin of the m. adductor mandibulae externus Pars superficialis from the jugal seems to be a characteristic feature of sea turtles.

Conclusions/Significance

In C. caretta and L. kempii the ability to suction feed does not seem to be as well developed as that found in some freshwater aquatic turtles. Instead both have skulls suited to forceful biting. This is consistent with the observation that both taxa tend to feed on relatively slow moving but sometimes armoured prey. The broad fleshy origin of the m. adductor mandibulae externus Pars superficialis may be linked to thecheek region being almost fully enclosed in bone but the relationship is complex.     

Comparative limb bone scaling in turtles: Phylogenetic transitions with changes in functional demands?

Several terrestrial vertebrate clades include lineages that have evolved nearly exclusive use of aquatic habitats. In many cases, such transitions are associated with the evolution of flattened limbs that are used to swim via dorsoventral flapping. Such changes in shape may have been facilitated by changes in limb bone loading in novel aquatic environments. Studies on limb bone loading in turtles found that torsion is high relative to bending loads on land, but reduced compared to bending during aquatic rowing. Release from torsion among rowers could have facilitated the evolution of hydrodynamically advantageous flattened limbs among aquatic species. Because rowing is regarded as an intermediate locomotor stage between walking and flapping, rowing species might show limb bone flattening intermediate between the tubular shapes of walkers and the flattened shapes of flappers. We collected measurements of humeri and femora from specimens representing four functionally divergent turtle clades: sea turtles (marine flappers), softshells (specialized freshwater rowers), emydids (generalist semiaquatic rowers), and tortoises (terrestrial walkers). Patterns of limb bone scaling with size were compared across lineages using phylogenetic comparative methods. Although rowing taxa did not show the intermediate scaling patterns we predicted, our data provide other functional insights. For example, flattening of sea turtle humeri was associated with positive allometry (relative to body mass) for the limb bone diameter perpendicular to the flexion-extension plane of the elbow. Moreover, softshell limb bones exhibit positive allometry of femoral diameters relative to body mass, potentially helping them maintain their typical benthic position in water by providing additional weight to compensate for shell reduction. Tortoise limb bones showed positive allometry of diameters, as well as long humeri, relative to body mass, potentially reflecting specializations for resisting loads associated with digging. Overall, scaling patterns of many turtle lineages appear to correlate with distinctive behaviors or locomotor habits.     

<Emphasis Type="Italic">Aphanomyces sinensis</Emphasis> sp. nov., isolated from juvenile soft-shelled turtle, <Emphasis Type="Italic">Pelodiscus sinensis</Emphasis>, in Japan

A species of Aphanomyces was isolated from juvenile soft-shelled turtles, Pelodiscus sinensis, cultured in Japan. Typically, an infected turtle showed small whitish maculae on the carapace. Many hyphae were observed in the epidermis. The hyphae were isolated using glucose–yeast (GY) agar plates. The morphological characteristics were very similar to those of Aphanomyces laevis, but a clear nuclear spot was observed in the center of the oospore in the strains isolated from the soft-shelled turtles. The optimal growth temperature for the isolates was 25–30°C and the optimum pH was 6–9. Experimental infection tests with isolates produced small whitish maculae on the carapace, and soft-shelled turtles artificially infected with the zoospores showed high mortality, especially in the high-dose group. Phylogenetic analysis based on the internal transcribed spacer (ITS) region of ribosomal DNA (rDNA) indicated that the isolates from the soft-shelled turtles were unidentified species of Aphanomyces. As a result, the strain was described as a new species, Aphanomyces sinensis.     

Morphology of the endocranial cavities of Campinasuchus dinizi (Crocodyliformes: Baurusuchidae) from the Upper Cretaceous of Brazil

Two specimens of Campinasuchus dinizi (CPPLIP 1319 and CPPLIP 1360) belonging to Baurusuchidae (Crocodyliformes, Notosuchia) from the Upper Cretaceous Bauru Group of Minas Gerais state (Brazil) were scanned in a Toshiba Aquilion 64 CT machine. Based on these data, it was possible to identify and reconstruct the paranasal sinuses, the nasal cavity proper, the nasopharyngeal duct, the encephalon, the paratympanic sinuses, and the semicircular canals of the inner ear. The paranasal sinuses present similar morphology to those of other mesoeucrocodylians, especially eusuchians. The nasal cavity proper occupies the entire rostral region, with an expansion in the olfactory region. The expansion in the nasal cavity is present in other notosuchians and theropod dinosaurs (e.g., Tyrannosaurus rex Osborn, 1905), but less developed in aquatic crocodilians, which may indicate an olfactory acuity related to terrestrial habits. The encephalon is similar in shape to that of other mesoeucrocodylians. The rostral semicircular canal is smaller than the caudal one, differing from most mesoeucrocodylians. The paratympanic sinuses are more developed in C. dinizi than in eusuchians, being more similar to Tyrannosaurus rex. Campinasuchus dinizi presents few variations in the internal structures of the skull in relation to taxa with different ecological niches, probably indicating that ecological factors do not strongly influence the morphology of these structures.     

A non‐aquatic otter (Mammalia,Carnivora, Mustelidae) from the Late Miocene (Vallesian,MN 10) of La Roma 2 (Alfambra,Teruel, Spain): systematics and functional anatomy

A new genus and species of otter‐like mustelid, Teruelictis riparius, is created on the basis of a partial skeleton from the Late Miocene (Vallesian age, MN 10) locality of La Roma 2 (Teruel, Spain), including several postcranial elements, the skull, and the mandible. The combination of a typically lutrine dentition, similar to that of other fossil otters such as Paralutra jaegeri, with a very slender postcranial skeleton, including a long back and gracile long bones and metacarpals, thus lacking any aquatic adaptations, was previously unknown in the fossil record. This mosaic of features strongly suggests the possibility that the aquatic lifestyle of otters could have appeared after the initial development of the distinctive dental morphology of this specialized group of mustelids. © 2013 The Linnean Society of London     

The diet and digestive energetics of an Australian short-necked turtle, Emydura macquarii

We described the diet of Emydura macquarii, an omnivorous turtle from south-eastern Australia, compared its digestive performance on diets of fish or plants at two temperatures, and related how both diet and temperature affect its food selection in nature. Filamentous algae constituted 61% of the stomach content of E. macquarii. The turtles rarely fed on motile prey, but selected carrion from the lagoon bottom and terrestrial insects (Diptera, Hymenoptera and Coleoptera) trapped on the surface of the water. Digestive efficiency of E. macquarii was affected little by body temperature, in contrast to consumption rates and rates of passage which were strongly influenced by both temperature and diet. In combination, these responses resulted in a slower rate of digestion at 20°C than at 30°C. Digestive efficiency of E. macquarii on a herbivorous diet at 30°C (49%) was about half that of turtles on a carnivorous diet (91%), but they had longer transit times (118 h on the plant diet versus 70 h). Lower consumption rates and longer mean retention times in turtles fed plants compared those fed fish relate to slower digestive processing of the plant. Rapid processing and higher consumption rates of fish by E. macquarii resulted in higher energy gains compared to turtles consuming plants (almost 100 times more energy at 30°C). The laboratory results suggest that fish carrion and aquatic and terrestrial invertebrates are probably essential dietary items of E. macquarii in the wild, because its metabolic requirements cannot be met from aquatic macrophytes alone.     

Genetic connectivity across marginal habitats: the elephants of the Namib Desert

Locally isolated populations in marginal habitats may be genetically distinctive and of heightened conservation concern. Elephants inhabiting the Namib Desert have been reported to show distinctive behavioral and phenotypic adaptations in that severely arid environment. The genetic distinctiveness of Namibian desert elephants relative to other African savanna elephant (Loxodonta africana) populations has not been established. To investigate the genetic structure of elephants in Namibia, we determined the mitochondrial (mt) DNA control region sequences and genotyped 17 microsatellite loci in desert elephants (n = 8) from the Hoanib River catchment and the Hoarusib River catchment. We compared these to the genotypes of elephants (n = 77) from other localities in Namibia. The mtDNA haplotype sequences and frequencies among desert elephants were similar to those of elephants in Etosha National Park, the Huab River catchment, the Ugab River catchment, and central Kunene, although the geographically distant Caprivi Strip had different mtDNA haplotypes. Likewise, analysis of the microsatellite genotypes of desert‐dwelling elephants revealed that they were not genetically distinctive from Etosha elephants, and there was no evidence for isolation by distance across the Etosha region. These results, and a review of the historical record, suggest that a high learning capacity and long‐distance migrations allowed Namibian elephants to regularly shift their ranges to survive in the face of high variability in climate and in hunting pressure.