Microanatomical and Histological Features in the Long Bones of Mosasaurine Mosasaurs (Reptilia,Squamata) – Implications for Aquatic Adaptation and Growth Rates

Background

During their evolution in the Late Cretaceous, mosasauroids attained a worldwide distribution, accompanied by a marked increase in body size and open ocean adaptations. This transition from land-dwellers to highly marine-adapted forms is readily apparent not only at the gross anatomic level but also in their inner bone architecture, which underwent profound modifications.

Methodology/Principal Findings

The present contribution describes, both qualitatively and quantitatively, the internal organization (microanatomy) and tissue types and characteristics (histology) of propodial and epipodial bones in one lineage of mosasauroids; i.e., the subfamily Mosasaurinae. By using microanatomical and histological data from limb bones in combination with recently acquired knowledge on the inner structure of ribs and vertebrae, and through comparisons with extant squamates and semi-aquatic to fully marine amniotes, we infer possible implications on mosasaurine evolution, aquatic adaptation, growth rates, and basal metabolic rates. Notably, we observe the occurrence of an unusual type of parallel-fibered bone, with large and randomly shaped osteocyte lacunae (otherwise typical of fibrous bone) and particular microanatomical features in Dallasaurus, which displays, rather than a spongious inner organization, bone mass increase in its humeri and a tubular organization in its femora and ribs.

Conclusions/Significance

The dominance of an unusual type of parallel-fibered bone suggests growth rates and, by extension, basal metabolic rates intermediate between that of the extant leatherback turtle, Dermochelys, and those suggested for plesiosaur and ichthyosaur reptiles. Moreover, the microanatomical features of the relatively primitive genus Dallasaurus differ from those of more derived mosasaurines, indicating an intermediate stage of adaptation for a marine existence. The more complete image of the various microanatomical trends observed in mosasaurine skeletal elements supports the evolutionary convergence between this lineage of secondarily aquatically adapted squamates and cetaceans in the ecological transition from a coastal to a pelagic lifestyle.     

Cryptic species,taxonomic inflation,or a bit of both? New species phenomenon in Sri Lanka as suggested by a phylogeny of dwarf geckos (Reptilia,Squamata, Gekkonidae,Cnemaspis)

We evaluated the status of 16 of 22 recognized Sri Lankan Cnemaspis Strauch species, and flagged overlooked diversity with two mitochondrial (cyt b & ND2) and two nuclear markers (RAG1 & PDC) totalling 2829 base pairs. A fossil-calibrated timetree and sampling of other South Asian Cnemaspis provide insights into the diversification of the genus in peninsular India and Sri Lanka. Phylogenetic analyses consistently inferred two broad clades within South Asian Cnemaspis, with Sri Lankan species in two clades, which we call the podihuna and kandiana clades. Each Sri Lankan clade as a whole is sister to Indian taxa and nested within Indian lineages. Cnemaspis modigliani Das from Indonesia is a member of the kandiana clade. This suggests a minimum of two dispersal events between India and Sri Lanka and one between Sri Lanka/India and South-east Asia. South Asian Cnemaspis date back to at least the Eocene, in Sri Lanka to the early Miocene, with late Miocene diversification in the kandiana clade. All but one of the named species we sampled is likely to be valid, and 10 divergent unnamed lineages may warrant specific recognition. A resolution of Sri Lankan Cnemaspis taxonomy will require thorough sampling and the use of both morphological and molecular data.     

The relationship between pink salmon biomass and the body condition of short-tailed shearwaters in the Bering Sea: can fish compete with seabirds?

Seabirds and large fishes are important top predators in marine ecosystems, but few studies have explored the potential for competition between these groups. This study investigates the relationship between an observed biennial change of pink salmon (Oncorhynchus gorbuscha) biomass in the central Bering Sea (23 times greater in odd-numbered than in even-numbered years) and the body condition and diet of the short-tailed shearwater (Puffinus tenuirostris) that spends the post-breeding season there. Samples were collected with research gill nets over seven summers. Both species feed on krill, small fishes and squid. Although the mean pink salmon catch per unit effort (in mass) over the study region was not related significantly with shearwater's stomach content mass or prey composition, the pink salmon biomass showed a negative and significant relationship with the shearwater's body mass and liver mass (proxies of energy reserve). We interpret these results as evidence that fishes can negatively affect mean prey intake of seabirds if they feed on a shared prey in the pelagic ecosystem.     

Integrative taxonomy and preliminary assessment of species limits in the Liolaemus walkeri complex (Squamata,Liolaemidae) with descriptions of?three?new species from Peru

Species delimitation studies based on integrative taxonomic approaches have received considerable attention in the last few years, and have provided the strongest hypotheses of species boundaries. We used three lines of evidence (molecular, morphological, and niche envelopes) to test for species boundaries in Peruvian populations of the Liolaemus walkeri complex. Our results show that different lines of evidence and analyses are congruent in different combinations, for unambiguous delimitation of three lineages that were “hidden” within known species, and now deserve species status. Our phylogenetic analysis shows that L. walkeri, L. tacnae and the three new species are strongly separated from other species assigned to the alticolor-bibronii group. Few conventional morphological characters distinguish the new species from closely related taxa and this highlights the need to integrate other sources of data to erect strong hypothesis of species limits. A taxonomic key for known Peruvian species of the subgenus Lioalemus is provided.     

Taxonomical revision of “Arctonyx” fossil remains from the Liucheng Gigantopithecus Cave (South China) by means of morphotype and morphometrics,and a review of Late Pliocene and Early Pleistocene Meles fossil records in China

“Arctonyx” fossil remains from the Liucheng Gigantopithecus Cave, Guangxi, are redescribed and analysed in details. Detailed tooth character differences between Arctonyx and Meles are analysed. It is shown that materials from the Liucheng Gigantopithecus Cave actually belong to two species of Meles: Meles minor and Meles magnus n. sp. At the same time, a review of Late Pliocene and Early Pleistocene Meles records in China is made. During Late Pliocene, Meles are only represented by M. chiai and one archaic form. During Early Pleistocene, Meles from northern and central part of China are represented by two nearly sympatric species Meles chiai and Meles teihardi. Meles from South China are represented by M. minor and M. magnus n. sp., though the distribution of the two species is still unclear. M. magnus n. sp. is so far only known from the Liucheng Gigantopithecus Cave, whereas M. minor is probably also known from Longgupo, Chongqing in the central part of China besides Liucheng. Great diversity of Meles in Early Pleistocene in China indicates that the genus radiated earlier than previously thought. Phylogenetic analysis suggests M. magnus n. sp. is sister group to living M. leucurus, whereas M. minor and M. chiai are early branches in Meles evolution.     

Nicotinamide–adenine dinucleotides in acute liver injury induced by ethionine, and a comparison with the effects of salicylate

1. The effects of single doses of ethionine or sodium salicylate on the nicotinamide-adenine dinucleotide content of rat liver have been studied. 2. There was no significant change in the sum of NAD+NADH(2) during the early period (0-2hr.) of the liver injury induced by ethionine but there was a decrease in this value of approx. 30% by 4hr. after administration. 3. Ethionine had no significant effect on the NADP+NADPH(2) during the first 2hr. period after administration. The sum then decreased to a value approx. 70% of the control by 3hr. after dosing but showed a partial recovery at the 4hr. period before decreasing again in later stages of the poisoning. 4. Salicylate produced a very rapid decrease in the NADP+NADPH(2) in the liver after intraperitoneal injection. After 1hr. the decrease was approx. 30% of the initial value; the sum slowly returned towards the normal range during the following 4hr. 5. A high parenteral dose of salicylate was found to cause only a small depression in the concentration of ATP in rat liver in contrast with the rapid depletion produced by ethionine. 6. These results are discussed in terms of the liver disturbances produced by ethionine and salicylate.     

Changes in fish condition and mercury vary by region,not Bythotrephes invasion: a result of climate change?

We compared changes in body condition (relative weight) and mercury concentrations ([Hg]) in two species of coregonid fish (lake herring Coregonus artedi, lake whitefish C. clupeaformis) among discrete populations in Ontario between 1967 and 2006. Temporal comparisons among populations were made to determine whether 1) the establishment of Bythotrephes longimanus had affected coregonid populations, or 2) if changes in body condition or [Hg] were related to regional differences in the degree of climate change during the time period investigated. Climate data from northwestern, northeastern and southern Ontario showed a general warming trend in all regions over the period of study. However, greater temporal changes in climate were observed in the northwest where growing degree days >5°C (GDD) increased and precipitation declined over the study period compared with relatively little change in southern or northeastern Ontario. Correspondingly, northwestern Ontario coregonid populations demonstrated significantly greater declines in body condition relative to those from northeastern or southern Ontario. Declines in [Hg] of both species were also greater among northwestern populations compared with those from northeastern or southern Ontario but only significantly so for lake herring. These declines were independent of the invasion of non‐native Bythotrephes, and declines in [Hg] were opposite predictions based on the hypothesis that Bythotrephes invasion lengthened aquatic food chains. Based on our findings and further evidence from the literature, we propose that warming regional climates are capable of contributing to declines in both condition and [Hg] of fishes. Because fish condition affects both reproductive success and overwinter survival, observed condition declines of the magnitude reported here could have profound implications for the structure of future aquatic ecosystems in a warming climate.     

Termite ecology in a dry evergreen forest in Thailand in terms of stable (δ 13C and δ 15N) and radio (14C, 137Cs and 210Pb) isotopes

Stable (¹³C and ¹⁵N) and radio- (¹⁴C, ¹³⁷Cs and ²¹⁰Pb) isotopes were determined for termites that have been sampled from a dry evergreen forest in Thailand. A wood-feeding termite, Microcerotermes crassus, was separated from soil-feeders: Termes propinquus, Termes comis and Dicuspiditermes makhamensis by ¹³C and ¹⁵N values. The Termes group in Thailand had less diverse values in ¹³C and ¹⁵N than those in Australia, where the feeding habits of the Termes group are more diverse. Other soil-feeding termites produced similar ¹³C values, but a larger range in ¹⁵N values. ¹⁴C-percent modern carbon (pMC) values suggest that the soil-feeding termites used younger carbon than the wood-feeding termites, and this was consistent with the termites from Cameroon, central Africa. Values of ¹³C and ¹⁴C-pMC indicate that surface soil was used by a soil-feeding termite, D. makhamensis, in making the nest mounds, and deeper soil (10–30 cm) by a fungus-growing termite, Macrotermes carbonarius. ²¹⁰Pb and ¹³⁷Cs were scarcely incorporated into the termites, although ²¹⁴Pb was recovered from the workers. The results suggest that stable- and radioisotopes are useful in the study of detritivorous animals, organic matter decomposition and ecosystem engineering.Takuya Abe - deceased.     

Influence of body mass, age, and maturation on specific oxygen consumption in a freshwater cichlid fish, Cichlasoma nigrofasciatum (Günther, 1869)

The oxygen consumption of a freshwater convict cichlid (Cichlasoma nigrofasciatum) was determined throughout the fish development from age 74 days to 403 days, covering the period before and after maturation. The specific oxygen consumption decreases with increasing age. The decrease in metabolic rate appears rather in distinct phases. A small increase in the average specific metabolic rate (mainly from the bigger fish) around age 200 days suggests an involvement of internal changes in the fish during a transition period from "young" state to "mature" state. The relationship between the specific oxygen consumption and body mass is determined by maturation and age. Before reaching maturation (before age 200 days) the correlation between specific oxygen consumption and body mass is negative for "young" fish of the same age. After age 200 days, no correlation between both parameters could be found. We suggest from this study that both factors "age" and "size" of the organism have to be considered for determining the metabolism, especially in fish. This study indicates that even in fish, which retain a continuous growing capability until they die, the decrease in the specific oxygen consumption is related to the aging process.     

Diversity,consistency, and seasonality in parasite assemblages of two sympatric marine fish Pagrus pagrus (Linnaeus, 1758) and Pagellus bogaraveo (Brünnich, 1768) (Perciformes: Sparidae) off the coast of Algeria in the western Mediterranean Sea

Various host characteristics (i. e., feeding habits, geographic distribution) and habitat characteristics (i.e., seasonality) influence the structure of parasite assemblages. To compare the parasite assemblages of hosts representatives of two genera of the same fish family, simultaneously occupying a geographic region, and to examine if seasonal variations influence parasite occurrence and abundance, we examined the parasite assemblages of two sympatric marine fish, Pagrus pagrus (n = 308) and Pagellus bogaraveo (n = 315) off the coast of Algeria in the western Mediterranean. Specimens were collected during summer and autumn over three consecutive years (2014–2016). Parasite assemblages were high in species richness and abundance. We compiled an inventory of 40 parasite taxa, including ectoparasitic monogeneans and crustaceans, and endoparasitic trematodes, cestodes, acanthocephalans, and nematodes. Endoparasite taxa primarily consisted of adult gastro-intestinal parasites and long lived larval helminths. Information on the parasite community structure and seasonal variations in parasite populations of these two hosts from the Mediterranean is here provided. Observed patterns of composition, diversity, dominance, and similarity indicate an overall consistency in assemblage structure. Although each host species harbored distinct parasite communities, they shared a high proportion of parasite species suggesting similar use of a common local pool of parasites. However, most shared species did not contribute to structuring the assemblages. Seasonal patterns in parasite abundance were observed for both hosts, with peak prevalence, abundance, and diversity in autumn. Results suggest that, regardless of a common pool of parasites being available to sympatric species, several ecological filters over time, led to distinct, independent variations in the parasite assemblages in each species.     

Circadian Phase-Dependent Protein and Tissular Binding of Three Local Anesthetics (Bupivacaine, Etidocaine, and Mepivacaine) in Mice: A Possible Mechanismof Their Chronotoxicokinetics?

The aim of this study was to investigate the possible influence of the time of administration on bupivacaine (B), etidocaine (E), and mepivacaine (M) protein and tissue (brain and heart) binding. For each anesthetic agent, a single dose of B (20 mg/kg), E (40 mg/kg), or M (60 mg/kg) was administered intraperito-neally at 10:00,16:00,22:00, and 04:00 h. Blood and tissue samples were collected 15 min after drug administration. This study documents significant circadian variations in protein and tissue binding of the three local anesthetic agents. We did not demonstrate a temporal relationship between the respective free and tissue levels. Thus, the temporal variations of free plasma, brain, and heart levels do not seem to be involved in the temporal changes of induced mortality.     

Circadian Phase-Dependent Protein and Tissular Binding of Three Local Anesthetics (Bupivacaine,Etidocaine, and Mepivacaine) in Mice: A Possible Mechanismof Their Chronotoxicokinetics?

The aim of this study was to investigate the possible influence of the time of administration on bupivacaine (B), etidocaine (E), and mepivacaine (M) protein and tissue (brain and heart) binding. For each anesthetic agent, a single dose of B (20 mg/kg), E (40 mg/kg), or M (60 mg/kg) was administered intraperito-neally at 10:00,16:00,22:00, and 04:00 h. Blood and tissue samples were collected 15 min after drug administration. This study documents significant circadian variations in protein and tissue binding of the three local anesthetic agents. We did not demonstrate a temporal relationship between the respective free and tissue levels. Thus, the temporal variations of free plasma, brain, and heart levels do not seem to be involved in the temporal changes of induced mortality.     

Why,when and how do fish populations decline,collapse and recover? The example of brown trout (Salmo trutta) in Rio Chaballos (northwestern Spain)

1. Around the year 2000, historically abundant populations of brown trout ( Salmo trutta ) and Atlantic salmon ( S. salar ) co-occurring in rivers flowing along the Cantabrian corridor of north-western Spain showed a dramatic decline to alarming levels. For one reason or another, fishing was not banned and fishing pressure continued to reduce the few survivors. Unexpectedly, the populations recovered 'naturally' in a very short time period to the extent that in 2004–06 numbers had attained population sizes comparable to those of the mid 1980s.
2. The population of brown trout in Rio Chaballos showed a boom-and-bust pattern concurrent with those observed across broader geographical scales. This study revisits a 22-year data set to explore the nature of the severe decline and rapid recovery of this population.
3. Recruitment was related to stream discharge in March that covers the emergence period and the earliest search stages for food. Coefficients of variation for discharge and recruitment increased over the years and were highly correlated with each other, demonstrating that increased temporal variability in recruitment is strongly linked to increased variability in stream discharge. In turn, recruitment appears to be the major determinant of year-class strength and hence, of population size.
4. A number of factors appeared to operate as resilience mechanisms, permitting the population to increase rapidly when environmental conditions are optimal. These include strong recruitment-discharge relationships, short life-span, small stocks of eggs or offspring required to fill the amount of space suitable for the youngest juveniles and a few females surviving to spawn for a second time.
5. Implications for fishery management and conservation are discussed in the context of the expectation that these populations will vary over the coming years within ranges similar to those in this study.     

Assimilation and nitrification in pelagic waters: insights using dual nitrate stable isotopes (δ<Superscript>15</Superscript>N, δ<Superscript>18</Superscript>O) in a shallow lake

Nitrate dual stable isotopes (δ¹⁵N and δ¹⁸O of NO₃ ^?) have proven to be a powerful technique to elucidate nitrogen (N) cycling pathways in aquatic systems. We applied this technique for the first time in the pelagic zone of a small temperate meso-eutrophic lake to identify the dominant N cycling pathways, and their spatial and temporal variability. We measured the lake NO₃ ^? δ¹⁵N and δ¹⁸O signatures over an annual cycle and compared them to that of the watershed. Both δ¹⁵N and δ¹⁸O of NO₃ ^? in the lake increased during summer relative to the inputs. Relationships between lake NO₃ ^? isotopic composition and concentrations were different across thermal strata with an apparent isotope effect in the epilimnion of ¹⁵ε_epi = 4.6‰ and ¹⁸ε_epi = 10.9‰. We found a strong deviation of the lake NO₃ ^? δ¹⁸O and δ¹⁵N from the expected 1:1 line for assimilation (slope = 1.73) suggesting that nitrification was co-occurring. We estimated that nitrification could support between 5 and 30% of nitrate-based production during the growing season, but was negligible in early spring and fall, and probably more dominant under ice. We showed that the technique is promising to study N processes at the ecosystem scale in shallow lakes, particularly during winter. Our results suggest that recycled NO₃ ^? could support primary productivity and influence phytoplankton composition in the surface waters of small lakes.     

Was there a second adaptive radiation of giant tortoises in the Indian Ocean? Using mitochondrial DNA to investigate speciation and biogeography of Aldabrachelys (Reptilia,Testudinidae)

A radiation of five species of giant tortoises (Cylindraspis) existed in the southwest Indian Ocean, on the Mascarene islands, and another (of Aldabrachelys) has been postulated on small islands north of Madagascar, from where at least eight nominal species have been named and up to five have been recently recognized. Of 37 specimens of Madagascan and small-island Aldabrachelys investigated by us, 23 yielded significant portions of a 428-base-pair (bp) fragment of mitochondrial (cytochrome b and tRNA-Glu), including type material of seven nominal species (A. arnoldi, A. dussumieri, A. hololissa, A. daudinii, A. sumierei, A. ponderosa and A. gouffei). These and nearly all the remaining specimens, including 15 additional captive individuals sequenced previously, show little variation. Thirty-three exhibit no differences and the remainder diverge by only 1-4 bp (0.23-0.93%). This contrasts with more widely accepted tortoise species which show much greater inter- and intraspecific differences. The non-Madagascan material examined may therefore only represent a single species and all specimens may come from Aldabra where the common haplotype is known to occur. The present study provides no evidence against the Madagascan origin for Aldabra tortoises suggested by a previous molecular phylogenetic analysis, the direction of marine currents and phylogeography of other reptiles in the area. Ancient mitochondrial DNA from the extinct subfossil A. grandidieri of Madagascar differs at 25 sites (5.8%) from all other Aldabrachelys samples examined here.     

Adherent-invasive Escherichia coli (AIEC): Cause or consequence of inflammation,dysbiosis, and rupture of cellular joints in patients with IBD?

There are many factors contributing to the development of gastrointestinal diseases, grouped into genetic, environmental, and lifestyle factors. In recent years attention has fallen on pathogens; in particular, Bacteroides fragilis, Fusobacterium nucleatum, Escherichia coli (E. coli) and Helicobacter pylori have been studied. Several points remain to be clarified, and above all, as regards the adherent-invasive E. coli strains of E. coli, one wonders if they are a cause or a consequence of the disease. In this review, we have tried to clarify some points by examining a series of recent publications regarding the involvement of the bacterium in the pathology, even if other studies are necessary.     

Evolution of self-fertilization at geographical range margins? A comparison of demographic, floral, and mating system variables in central vs. peripheral populations of Aquilegia canadensis (Ranunculaceae)

Biogeographic models predict that geographically peripheral populations should be smaller, more sparsely distributed, and have a lower per-capita reproductive rate than populations near the center of a species' range. Plants in peripheral populations may, therefore, receive less pollinator visitation and outcross pollination, which may select for self-fertilization to provide reproductive assurance. We tested these predictions by comparing population size, plant density, seed production, floral traits, and mating system parameters between 10 populations of Aquilegia canadensis near the northern margin of the range with 10 near the range center. Contrary to predictions, peripheral populations were not smaller, less dense, nor less productive than central populations. Nevertheless, we detected substantial regional differences in key floral traits. Plants in central populations produced larger flowers with 68% greater herkogamy and had 30% more flowers open simultaneously than plants in northern populations. However, there was no regional difference in the mating system. In northern populations, 73% (range = 60-88%) of seeds were self-fertilized compared to 76% (51-100%) in central populations. In both regions, adult inbreeding coefficients were near zero, indicating very strong inbreeding depression despite high selfing. Marked geographic variation in key floral traits does not reflect evolutionary differentiation in the mating system.