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.     

On Sea Turtle‐associated Craspedostauros (Bacillariophyta), with Description of Three Novel Species

The current study focuses on four species from the primarily marine diatom genus Craspedostauros that were observed growing attached to numerous sea turtles and sea turtle‐associated barnacles from Croatia and South Africa. Three of the examined taxa, C. danayanus sp. nov., C. legouvelloanus sp. nov., and C. macewanii sp. nov., are described based on morphological and, whenever possible, molecular characteristics. The new taxa exhibit characters not previously observed in other members of the genus, such as the presence of more than two rows of cribrate areolae on the girdle bands, shallow perforated septa, and a complete reduction of the stauros. The fourth species, C. alatus, itself recently described from museum sea turtle specimens, is reported for the first time from loggerhead sea turtles rescued in Europe. A 3‐gene phylogenetic analysis including DNA sequence data for three sea turtle‐associated Craspedostauros species and other marine and epizoic diatom taxa indicated that Craspedostauros is monophyletic and sister to Achnanthes. This study, being based on a large number of samples and animal specimens analyzed and using different preservation and processing methods, provides new insights into the ecology and biogeography of the genus and sheds light on the level of intimacy and permanency in the host–epibiont interaction within the epizoic Craspedostauros species.     

Species diversity of the genus Osmundea (Ceramiales,Rhodophyta) in the Macaronesian region

Species diversity within the genus Osmundea in the Macaronesian region was explored by conducting a comprehensive sampling in the Azores, the Canary, and the Madeira archipelagos. Toward identification, all specimens were first observed alive to verify the absence of corps en cerise, a diagnostic character for the genus and morphometric data were measured (thallus length and width, first‐order branches length and width, branchlets length and width, cortical cell length and width in surface view, cortical cell length and width in transverse section). Specimens were sequenced for COI‐5P (39 specimens) and three species delimitation methods (Generalized Mixed Yule Coalescent, Automatic Barcode Gap Discovery method, and Poisson Tree Processes) were used to assess the threshold between infra‐ and interspecific relationships. Subsequently, one or several sequences of plastid‐encoded large subunit of RuBisCO (21 specimens) per delimited species were generated to assess the phylogenetic relationships among Macaronesian Osmundea. Moreover, for each delineated species, vegetative and reproductive anatomy was thoroughly documented and, when possible, specimens were either assigned to existing taxa or described as novel species. This integrative approach has provided data for (i) the presence of O. oederi, O. pinnatifida, and O. truncata in Macaronesia; (ii) the proposal of two novel species, O. prudhommevanreinei sp. nov. and O. silvae sp. nov.; and (iii) evidence of an additional species referred as “Osmundea sp.1,” which is a sister taxon of O. hybrida.     

Ecological regime shift drives declining growth rates of sea turtles throughout the West Atlantic

Somatic growth is an integrated, individual‐based response to environmental conditions, especially in ectotherms. Growth dynamics of large, mobile animals are particularly useful as bio‐indicators of environmental change at regional scales. We assembled growth rate data from throughout the West Atlantic for green turtles, Chelonia mydas, which are long‐lived, highly migratory, primarily herbivorous mega‐consumers that may migrate over hundreds to thousands of kilometers. Our dataset, the largest ever compiled for sea turtles, has 9690 growth increments from 30 sites from Bermuda to Uruguay from 1973 to 2015. Using generalized additive mixed models, we evaluated covariates that could affect growth rates; body size, diet, and year have significant effects on growth. Growth increases in early years until 1999, then declines by 26% to 2015. The temporal (year) effect is of particular interest because two carnivorous species of sea turtles—hawksbills, Eretmochelys imbricata, and loggerheads, Caretta caretta—exhibited similar significant declines in growth rates starting in 1997 in the West Atlantic, based on previous studies. These synchronous declines in productivity among three sea turtle species across a trophic spectrum provide strong evidence that an ecological regime shift (ERS) in the Atlantic is driving growth dynamics. The ERS resulted from a synergy of the 1997/1998 El Niño Southern Oscillation (ENSO)—the strongest on record—combined with an unprecedented warming rate over the last two to three decades. Further support is provided by the strong correlations between annualized mean growth rates of green turtles and both sea surface temperatures (SST) in the West Atlantic for years of declining growth rates (r = −.94) and the Multivariate ENSO Index (MEI) for all years (r = .74). Granger‐causality analysis also supports the latter finding. We discuss multiple stressors that could reinforce and prolong the effect of the ERS. This study demonstrates the importance of region‐wide collaborations.     

The leaf turtle population of Phnom Kulen National Park (northwestern Cambodia) has genetic and morphological signatures of hybridization

Cambodia is known to harbour three distinct species of Southeast Asian leaf turtles (Cyclemys spp.), which are heavily traded and common in seizures of wildlife. Confiscated leaf turtles are often released to natural habitats. Thus, an exact knowledge of the distribution of the individual species is of great importance to avoid the introduction of non‐native turtles, posing the risk of competition and hybridization. In this study, we examine a recently discovered leaf turtle population from Phnom Kulen National Park using external morphology, 17 unlinked microsatellite loci and the mitochondrial cytochrome b gene. Leaf turtles from the Phnom Kulen National Park morphologically resemble C. oldhamii, but harbour mitochondrial haplotypes of C. atripons. With respect to microsatellite loci, the turtles are distinct from C. atripons. Unfortunately no material of C. oldhamii was available from Cambodia. We propose that the Phnom Kulen population represents either a natural hybrid swarm of C. atripons and C. oldhamii or a distinct undescribed species with introgressed mitochondria of C. atripons. This underlines that genetic differentiation of wild leaf turtle populations in Cambodia is complex and suggests that this differentiation pattern becomes increasingly threatened by translocations of confiscated individuals. For drawing a definite conclusion about the taxonomic status of the Phnom Kulen population, denser sampling of other Cambodian leaf turtle populations would be required, in particular of C. oldhamii.     

High concentration of long‐snouted beaked whales (genus Messapicetus) from the Miocene of Peru

Abstract: Eight skulls of beaked whales (Cetacea, Odontoceti, Ziphiidae), in six cases associated with elements of the mandible, were collected from a limited area (about 1.5 km²) and roughly from the same stratigraphic horizon at Cerro Colorado, 35 km south‐south‐west of the city of Ica (Peru), where the late Middle Miocene basal strata of the Pisco Formation crop out. They represent the highest concentration reported of fossil Ziphiidae. These finely preserved Cerro Colorado fossils are described and assigned to a new species Messapicetus gregarius, together with another specimen collected from sediments of the same age at Cerro la Bruja (33 km south‐east to Cerro Colorado). Messapicetus gregarius shares with M. longirostris Bianucci, Landini and Varola, 1992 (Tortonian of Italy), an extremely elongated rostrum, but is clearly different from the Italian species in the more distinct maxillary tubercle and prominential notch, the more robust premaxillary crest, and the abrupt ventrolateral descent of the medial margin of the maxilla from the vertex. A parsimony analysis reveals that Messapicetus belongs to a basal clade, which includes other ziphiids with a dorsally closed mesorostral groove and prenarial basin. The high concentration of specimens belonging to the same species (some of them tentatively identified as adult males and females), combined with the presence of a calf, supports the hypothesis of site fidelity; these cetaceans might have lived in a limited region for a long period for both breeding and feeding. Besides the eight specimens of M. gregarius, strata at Cerro Colorado include many other cetacean remains (with several specimens of the pontoporiid Brachydelphis including a foetus), pinnipeds, turtles, fishes, and birds.     

Foraging area fidelity for Kemp's ridleys in the Gulf of Mexico

For many marine species, locations of key foraging areas are not well defined. We used satellite telemetry and switching state‐space modeling (SSM) to identify distinct foraging areas used by Kemp's ridley turtles (Lepidochelys kempii) tagged after nesting during 1998–2011 at Padre Island National Seashore, Texas, USA (PAIS; N = 22), and Rancho Nuevo, Tamaulipas, Mexico (RN; N = 9). Overall, turtles traveled a mean distance of 793.1 km (±347.8 SD) to foraging sites, where 24 of 31 turtles showed foraging area fidelity (FAF) over time (N = 22 in USA, N = 2 in Mexico). Multiple turtles foraged along their migratory route, prior to arrival at their “final” foraging sites. We identified new foraging “hotspots” where adult female Kemp's ridley turtles spent 44% of their time during tracking (i.e., 2641/6009 tracking days in foraging mode). Nearshore Gulf of Mexico waters served as foraging habitat for all turtles tracked in this study; final foraging sites were located in water <68 m deep and a mean distance of 33.2 km (±25.3 SD) from the nearest mainland coast. Distance to release site, distance to mainland shore, annual mean sea surface temperature, bathymetry, and net primary production were significant predictors of sites where turtles spent large numbers of days in foraging mode. Spatial similarity of particular foraging sites selected by different turtles over the 13‐year tracking period indicates that these areas represent critical foraging habitat, particularly in waters off Louisiana. Furthermore, the wide distribution of foraging sites indicates that a foraging corridor exists for Kemp's ridleys in the Gulf. Our results highlight the need for further study of environmental and bathymetric components of foraging sites and prey resources contained therein, as well as international cooperation to protect essential at‐sea foraging habitats for this imperiled species.     

The coralline genera Sporolithon and Heydrichia (Sporolithales,Rhodophyta) clarified by sequencing type material of their generitypes and other species

Interspecific systematics in the red algal order Sporolithales remains problematic. To re‐evaluate its species, DNA analyses were performed on historical type material and recently collected specimens assigned to the two genera Sporolithon and Heydrichia. Partial rbcL sequences from the lectotype specimens of Sporolithon ptychoides (the generitype species) and Sporolithon molle, both from El Tor, Egypt, are exact matches to field‐collected topotype specimens. Sporolithon crassum and Sporolithon erythraeum also have the same type locality; material of the former appears to no longer exist, and we were unable to PCR amplify DNA from the latter. A new species, Sporolithon eltorensis, is described from the same type locality. We have not found any morpho‐anatomical characters that distinguish these three species. No sequenced specimens reported as S. ptychoides from other parts of the world represent this species, and likely reports of S. ptychoides and S. molle based on morpho‐anatomy are incorrect. A partial rbcL sequence from the holotype of Sporolithon dimotum indicates it is not a synonym of S. ptychoides, and data from the holotype of S. episporum confirm its specific recognition. DNA sequences from topotype material of Heydrichia woelkerlingii, the generitype species, and isotype material of Heydrichia cerasina confirm that these are distinct species; the taxon reported to be H. woelkerlingii from New Zealand is likely an undescribed species. Type specimens of all other Sporolithon and Heydrichia species need to be sequenced to confirm that they are distinct species; morpho‐anatomical studies have proved inadequate for this task.     

What did the “Unossified zone” of the non‐mammalian therapsid braincase house?

Most nonmammalian synapsids possess a mid‐dorsal depression in the brain cavity known as the “unossified zone.” It remains obscure which structures this zone contained, and, as candidates, the vermis of the cerebellum, the superior sagittal sinus, a junction of several blood vessels, the pineal gland or other midbrain structures were considered. Neutron tomography of a skull of Diictodon feliceps (Therapsida, Anomodontia) revealed some clear impressions of canals in this region of the brain cavity. Furthermore, the prootic sinus probably ran on the internal surface of the pila antotica and had a similar course in anomodonts as it has been proposed for cynodonts and Mesozoic mammals. Comparisons with the vascular systems of nonmammalian synapsids and mammals suggest that the unossified zone is best interpreted as a terminal chamber of the anterior segment of the medial head vein, which housed the junction of the superior sagittal sinus and the transverse sinuses. Consequently, the system of cranial vessels in Diictodon reveals a partial division of the medial head vein system into an anterior and a posterior segment at an early stage of synapsid evolution, which is consistent with the well‐known common pattern of early ontogenetic development in amniotes. J. Morphol., 2017. © 2017 Wiley Periodicals, Inc.     

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.     

Observations on torquaratorid acorn worms (Hemichordata,Enteropneusta) from the North Atlantic with descriptions of a new genus and three new species

Enteropneusts in the family Torquaratoridae were imaged using still and video cameras in the deep North Atlantic and then collected by remotely operated vehicles. From this material, we describe Yoda purpurata n. gen, n. sp., Tergivelum cinnabarinum n. sp., and Allapasus isidis n. sp. Individuals of the first two species were browsing completely exposed on the sea floor, whereas the specimen of the last species was encountered floating ~1 m above the sea floor. Living specimens of Y. purpurata were 12–19 cm long and had a dark reddish‐purple proboscis, collar, and genital wings (folded dorsally over the anterior region of the trunk). Members of this species were hermaphrodites (the first ever discovered in the phylum Hemichordata), with numerous separate testes and ovaries in the genital wings. Living specimens of T. cinnabarinum were 12–26 cm long and had a cinnabar‐colored proboscis, collar, and back veils (arising from the anterior region of the trunk); sexes were separate, and body shape and internal morphology closely resemble those of its brown congener, T. baldwinae, from the eastern Pacific. The only specimen of A. isidis collected was a male 13 cm long and pale yellow when alive. Its body shape was proportionally shorter and broader than that of its orange congener, A. aurantiacus, from the eastern Pacific, but the internal anatomy of the two species is virtually identical. [Correction made after online publication August 21, 2012 to correct species name in preceding sentence.]     

Integrating telemetry with a predictive model to assess habitat preferences and juvenile survival in an endangered freshwater turtle

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Next‐generation DNA barcoding: using next‐generation sequencing to enhance and accelerate DNA barcode capture from single specimens

DNA barcoding is an efficient method to identify specimens and to detect undescribed/cryptic species. Sanger sequencing of individual specimens is the standard approach in generating large‐scale DNA barcode libraries and identifying unknowns. However, the Sanger sequencing technology is, in some respects, inferior to next‐generation sequencers, which are capable of producing millions of sequence reads simultaneously. Additionally, direct Sanger sequencing of DNA barcode amplicons, as practiced in most DNA barcoding procedures, is hampered by the need for relatively high‐target amplicon yield, coamplification of nuclear mitochondrial pseudogenes, confusion with sequences from intracellular endosymbiotic bacteria (e.g. Wolbachia) and instances of intraindividual variability (i.e. heteroplasmy). Any of these situations can lead to failed Sanger sequencing attempts or ambiguity of the generated DNA barcodes. Here, we demonstrate the potential application of next‐generation sequencing platforms for parallel acquisition of DNA barcode sequences from hundreds of specimens simultaneously. To facilitate retrieval of sequences obtained from individual specimens, we tag individual specimens during PCR amplification using unique 10‐mer oligonucleotides attached to DNA barcoding PCR primers. We employ 454 pyrosequencing to recover full‐length DNA barcodes of 190 specimens using 12.5% capacity of a 454 sequencing run (i.e. two lanes of a 16 lane run). We obtained an average of 143 sequence reads for each individual specimen. The sequences produced are full‐length DNA barcodes for all but one of the included specimens. In a subset of samples, we also detected Wolbachia, nontarget species, and heteroplasmic sequences. Next‐generation sequencing is of great value because of its protocol simplicity, greatly reduced cost per barcode read, faster throughout and added information content.     

Morphological characterization and phylogenetic relationships of Indochinese box turtles—The Cuora galbinifrons complex

The members of the Indochinese box turtle complex, namely Cuora galbinifrons, Cuora bourreti, and Cuora picturata, rank the most critically endangered turtle species on earth after more than three decades of over‐harvesting for food, traditional Chinese medicine, and pet markets. Despite advances in molecular biology, species boundaries and phylogenetic relationships, the status of the C. galbinifrons complex remains unresolved due to the small number of specimens observed and collected in the field. In this study, we present analyses of morphologic characters as well as mitochondrial and nuclear DNA data to reconstruct the species boundaries and systematic relationships within the C. galbinifrons complex. Based on principal component analysis (PCA) and statistical analysis, we found that phenotypic traits partially overlapped among galbinifrons, bourreti, and picturata, and that galbinifrons and bourreti might be only subspecifically distinct. Moreover, we used the mitochondrial genome, COI, and nuclear gene Rag1 under the maximum likelihood criteria and Bayesian inference criteria to elucidate whether C. galbinifrons could be divided into three separate species or subspecies. We found strong support for a sister relationship between picturata and the other two species, and consequently, we recommend maintaining picturata as a full species, and classifying bourreti and galbinifrons as subspecies of C. galbinifrons. These findings provide evidence for a better understanding of the evolutionary histories of these critically endangered turtles.     

A new cajaro catfish (Siluriformes: Pimelodidae:Phractocephalus) from the Late Miocene of southwestern Amazonia and its relationship to °Phractocephalus nassi of the Urumaco Formation

A new fossil species of the living catfish genusPhractocephalus is described from fluvial Sediments of late Miocene age in Acre State, Brazil and the Madre de Dios region, Peru. †Phractocephalus acreornatus n. sp., is known from a complete neurocranium with associated Weberian complex vertebrae and posttemporal-supracleithra, and several isolated skeletal elements. °Phractocephalus acreornatus is diagnosed by the following combination of characters: 1) anterior half of supraoccipital, frontals and sometimes mesethmoid with coarse parallel ridges and sulci in addition to reticulating ridges and subcircular pits; 2) mesethmoid very broad and coarsely ornamented; 3) lateral ethmoid projecting anteriorly above palatine condyle into olfactory capsule, its anterolateral margin convex and fluted, and its orbital notch reduced; 4) supraoccipital process long, concealing Weberian vertebrae in dorsal view; 5) opercle covered with rough, reticulating ridges and pits; 6) interopercle relatively deep, its outer side coarsely ornamented; 7) pectoral spine shaft ornamented with reticulating ridges and pits. Variability of the form of the much expanded supraoccipital process inPhractocephalus is evaluated for its taxonomic significance. Although °P.acreornatus is distinct from both modernP. hemloliopterus and fossil °P. nassi, like most Miocene fossil fishes from South America, this extinct species is closely similar to its relatives. Available characters provide evidence for a close relationship between °P. acreornatus and °P. nassi from the Urumaco Formation, Venezuela. The provenance of these late Miocene catfishes in lowland western Amazonia and north-central South America is congruent with paleogeographic modeis positing a large, north flowing “Paleo-Amazon-Orinoco” river System in the Andean foreland basin during the Neogene.      

The pineal-paraphyseal complex of sea turtles. I. Light microscopic description

The pineal-paraphyseal complex of sea turtles is an impressively large structure which projects dorsally and anteriorly above the prosencephalon. The complex was examined by light microscopy in several age classes of green sea turtles (Chelonia mydas) and from juvenile loggerhead turtles (Caretta caretta). The paraphysis is extensively fused to the distal portion of the pineal body, suggesting an interrelated function for these two tissues. No duct or canal was observed connecting the pineal lumen to the third ventricle. Two pineal cell types are described which appear to correspond to the neuroglial supportive cells and the secretory rudimentary photoreceptor cells of other amniotic vertebrates. A possible luminal secretion in the form of apical protrusions is produced by the latter cell type. No typical photoreceptive outer segments were observed.     

Characteristics of paxilline-sensitive calcium-dependent potassium current in isolated intestine myocytes

An inward current in smooth muscle cells (SMCs) of the taenia coli is known to be transferred via potassium channels and nonselective cation channels. The outward current is of a potassium nature and includes several components, Ca-dependent potassium current (I _K(Ca)) and delayed rectifying potassium current (I _K(V)) in particular. Applications of 100 nM paxilline to SMCs of the guinea-pig taenia coli suppressed considerably the outward current and decreased its oscillations; the effect of paxilline reached its maximum in 2 to 3 min from the beginning of application. Analysis of the current-voltage (I-V) relationship observed under conditions of such applications showed that the paxilline-sensitive current is highly dependent on the intracellular Ca²⁺ concentration; a change in the I-V slope within a segment of the maximum activation of the calcium current is indicative of this peculiarity. Application of paxilline against the background of the action of 1 mM tetraethylammonium (a nonselective blocker of potassium channels) evoked no additional suppression of the outward current. In most cells, we observed spontaneous outward currents (SOCs). Application of 100 nM paxilline nearly completely blocked high-amplitude SOCs (>10 pA) formed due to activation of big-conductance Ca-dependent potassium channels. At the same time, the frequency of small-amplitude SOCs (<10 pA) practically did not change. Thus, according to the pharmacological and time characteristics, voltage dependence, and sensitivity to the intracellular Ca²⁺ concentration, we identified a voltage-operated paxilline-sensitive component in I _K(Ca) that is transferred via big-conductance Ca-dependent potassium channels. Neirofiziologiya/Neurophysiology, Vol. 39, No. 3, pp. 201–207, May–June, 2007.