The integument of Psittacosaurus from Liaoning Province, China: taphonomy, epidermal patterns and color of a ceratopsian dinosaur

Preserved skin of small dinosaurs is rare. Here, a specimen of the ceratopsian dinosaur, Psittacosaurus, presents some of the best preserved epidermal scales observed to date in a relatively small dinosaur, over wide areas extending from the head to the tail. We study the preserved epidermis of SMF R 4970, the different types of scales, color, and patterns, and their respective locations in the body. We use modern application of high-power digital imaging for close-up analysis of the tubercles and fragments of preserved color. Three types of scales are preserved, large plate-like scales, smaller polygonal scales or tubercles, and round pebble-like scales. The sizes of the plate-like scales vary in different parts of the body and vanish altogether posteriorly. Light and dark cryptic patterns are created by the associations of the tubercle and plate-like scales, and there is also evidence of countershading in the proximal caudal region, the body darker dorsally and lighter ventrally. Perhaps most impressive are the distinctive pigmented impressions of scales over most of the skeletal elements. The pigmentation follows the curvature of the bones implying that when it was deposited, the skin was still pliable and able to wrap around the visible parts of the elements. The present record of color is the first in a non-theropod dinosaur and only the second record in a non-avian dinosaur. Because of its resistance to degradation and ability to produce various color tones from yellows to blacks, we suggest that melanin was the dominant chemical involved in the coloration of Psittacosaurus. The data here enable us to reconstruct the colors of Psittacosaurus as predominantly black and amber/brown, in cryptic patterns, somewhat dull, but useful to a prey animal. Indeed, skin pigment within a partially degraded bone indicates that Psittacosaurus was scavenged shortly after death. The theropod dinosaur Sinosauropteryx has recently been reported to have naturally pigmented integumental structures, which the authors interpret as proof that they are protofeathers and not support fibers of collagen. Our findings in Psittacosaurus, on the other hand, indicate a more parsimonious and less profound alternative explanation, i.e., decomposition of the skin releases pigments that readily permeate underlying structures.     

Evolution of birds: ichthyosaur integumental fibers conform to dromaeosaur protofeathers

Filamentous integumentary structures have been reported as protofeathers in dromaeosaurs (non-avian dinosaurs). This hypothesis is considered against data on the complex architecture of dermal and subdermal collagenous fibers widely prevalent in living and extinct animals. Ichthyosaur integumental fibers, as dromaeosaur "protofeathers", are the most external structures preserved. Marked similarities are shown in branching patterns of these fibers compared with those of the dromaeosaur Sinornithosaurus; hence distinguishing between aberrant and primary features is difficult. Analysis of a pterosaur specimen shows that bent and straight fibers on the wings have functional implications. The fibers conform to the twofold shape of collagen and contradict the notion that bent integumental structures in the dinosaur Sinosauropteryx indicate softness and pliability. A suggestion also concerning Sinosauropteryx is that integumental structures with darker edges, compared with the middle, imply that they were hollow. Investigation of a similar condition in an ichthyosaur shows that it is more likely a consequence of mineralization. Dermal collagen fibers in, for example, sharks, dolphins, snakes, and turtles are shown to be grouped in bundles of varying sizes. Degradation of the dermis results in the breakdown of the fiber bundles and formation of myriad patterns of the disrupted fibers, as noted in decomposed dolphin skin. The overall findings of the study are that the thesis of dinosaur "protofeathers" requires more substantial support than exists at present.     

Ancient specimens and DNA contamination: a case study from the 12S rRNA gene sequence of the "Linh Duong" bovid (Pseudonovibos spiralis)

In 1993, several unusual horn sheaths, collected in the South of Vietnam, were regarded as evidence for a new mammal species, Pseudonovibos spiralis. However, the taxonomic status of P. spiralis remains a highly controversial subject: firstly, it has been related to three different groups of the family Bovidae: Antilopini (gazelles), Bovini (oxen, bisons, and buffaloes), and Caprini sensu lato (goats, sheep and allies). Secondly, certain horns have been shown to be faked. Most recently, it has been suggested, on the basis of 12S rRNA gene sequences, that P. spiralis was a new species of buffalo. I demonstrate here that this conclusion was inaccurate, and base this on the grounds that: (1) the putative sequence of P. spiralis is shown to be a chimera obtained from three different species: Bos taurus, Bubalus bubalis and Saiga tatarica, and (2) several factors indicate that the specimen used was not authentic. This new study confirms earlier suggestions that the horns used to formally describe P. spiralis were bogus and were in fact derived from the horns of domesticated cattle (Bos taurus). The data suggest that P. spiralis never existed.     

Split-second escape decisions in blue tits (Parus caeruleus)

Bird mortality is heavily affected by birds of prey. Under attack, take-off is crucial for survival and even minor mistakes in initial escape response can have devastating consequences. Birds may respond differently depending on the character of the predator's attack and these split-second decisions were studied using a model merlin (Falco columbarius) that attacked feeding blue tits (Parus caeruleus) from two different attack angles in two different speeds. When attacked from a low attack angle they took off more steeply than when attacked from a high angle. This is the first study to show that escape behaviour also depends on predator attack speed. The blue tits responded to a high-speed attack by dodging sideways more often than when attacked at a low speed. Escape speed was not significantly affected by the different treatments. Although they have only a split-second before escaping an attack, blue tits do adjust their escape strategy to the prevailing attack conditions.     

A novel sex-specific and inducible monoterpene synthase activity associated with a pine bark beetle,the pine engraver,<Emphasis Type="Italic"> Ips pini</Emphasis>

Ecological interactions of conifers and coniferophagous bark beetles are determined in part by terpenoids (isoprenoids), which are major defense metabolites of conifer oleoresin. Curiously, similar compounds are important aggregation pheromones of conifer-attacking bark beetles. Terpene synthases are responsible for generating the enormous variety of terpenoid carbon skeletons found in nature. These catalysts convert short-chain prenyl diphosphates to a diverse assortment of hemiterpene, monoterpene, sesquiterpene, and diterpene natural products. While terpene synthases have frequently been characterized from plant and microbial sources, they have not yet been described in animals. Here we report the discovery of a monoterpene synthase activity in an insect, the pine engraver, Ips pini (Say) (Coleoptera: Scolytidae). Cell-free assays of I. pini revealed that geranyl diphosphate (GDP) is converted to the acyclic monoterpene myrcene in whole-body extracts from males, but not females. Furthermore, the monoterpene synthase activity in males can be induced by prior treatment with juvenile hormone III (JH III) or by feeding on phloem from the host trees, Jeffrey pine (Pinus jeffreyi Grev. &; Balf.) or red pine (Pinus resinosa Ait.). The sex-specificity and endocrine induction of this activity argue for its involvement in the biosynthesis of monoterpenoid pheromones mediated by enzymes from insect tissue. This discovery is the first example of a monoterpene synthase in the Metazoa and evokes exciting new questions about the origin, evolution, and occurrence of terpene synthases.     

Microbial spheres: a novel cyanobacterial–diatom symbiosis

Cyanobacteria, algae and bacteria are widespread inhabitants of North Sea microbial mats. Our studies of these populations showed uncommon modes of living and extraordinary structures, which have not been described before. The structures are spherical objects covering a community of cyanobacteria, diatoms and bacteria. The cultivation of these communities in the laboratory and intensive observations of their exceptional movement has led to some spectacular findings. The sphere formations go through different phases with variation in the dominance of different microorganisms. The role of the bacteria is the most important in the first phase, and can be increased by the addition of signal substances. Spheres surrounded by envelopes of unknown composition and permeability appear, with numerous bacteria and sporadic diatoms inside. Then the cyanobacteria penetrate the spheres and arrange themselves at the surface. The communities proliferate over some weeks and are finally released. Laboratory expositions of the microbial communities to different parameters pinpoint the limits of sphere formation. The metabolic products of the sphere communities are concentrated in the spheres and lead to a different kind of compound compared with the surrounding environment. In this way, the microbial communities strongly influence the structure of the sediments. Uncommon circular structures, which develop into spheres between 0.08 and 3 mm in size were found in subcultures of non-axenic filamentous cyanobacteria enrichments from North Sea microbial mats. These filamentous cyanobacteria (Phormidium sp.) together with associated benthic diatoms of the genus Navicula and associated heterotrophic bacteria were held as reproducible synergistic cultures. Phormidium sp. filaments tightly intertwined with each other, formed the surface of the spheres, trapping diatoms inside. The formation of "spheres" was the result of radial and synchronous movements of the cyanobacteria. In old cultures, the direction of the cyanobacterial movement has turned in the opposite direction, away from the sphere. The integrity of large "spheres" was influenced by chemotactic phenomena and maintained by some type of trichome-trichome interaction. This suggests the presence of metabolic secondary products, which attract cyanobacteria and influence their movement in a form of chemotactic response.     

Structural differences in the drone olfactory system of two phylogenetically distant Apis species, A. florea and A. mellifera

Male insects that are attracted by sex pheromones to find their female mates over long distances have specialized olfactory subsystems. Morphologically, these subsystems are characterized by a large number of receptor neurons sensitive to components of the female's pheromones and hypertrophied glomerular subunits ('macroglomeruli' or 'macroglomerular complexes') in the antennal lobes, in which the axons of the receptor neurons converge. The olfactory subsystems are adapted for an increased sensitivity to perceive minute amounts of pheromones. In Apis mellifera, drones have 18,600 olfactory poreplate sensilla per antenna, each equipped with receptor neurons sensitive to the queen's sex pheromone, and four voluminous macroglomeruli (MG1-MG4) in the antennal lobes. In contrast, we show that drones of the phylogenetically distant species, Apis florea, have only 1,200 poreplate sensilla per antenna and only two macroglomeruli in their antennal lobes. These macroglomeruli are homologous in anatomical position to the two most prominent macroglomeruli in A. mellifera, the MG1 and MG2, but they are much smaller in size. The morphological and anatomical differences described here suggest major modifications in the sex-pheromone processing subsystem of both species: (1) less pheromone sensitivity in A. florea and (2) a more complex sex-pheromone processing and thus a more complex sex-pheromone communication in A. mellifera.     

Facultative and obligate slave making in Formica ants

Here we show for the first time that the presumed facultative slave-making ant Formica subintegra does not activate outside its nest until July and August, when it raids slaves. A comparative behavioral study of seasonal and daily activities, retrieval of prey, and nest maintenance of F. subintegra, the obligate slavemaker Polyergus breviceps, and the facultative Formica subnuda, shows that the behavioral repertory of F. subintegra closely resembles that of P. breviceps and clearly differs from the repertory of F. subnuda. Unlike P. breviceps, F. subintegra has retained some nest-building activity which, owing to lack of competence, does not contribute to nest maintenance. We suggested earlier that F. subintegra is probably an obligate slavemaker, because it always has in its colonies a large proportion of slaves of the total workforce, whereas F. subnuda fares well even without slaves. This, coupled with no foraging in early summer and a raiding period later on, strongly suggests that F. subintegra is an obligate slave-making ant.     

Cycads: their evolution,toxins, herbivores and insect pollinators

Palaeobiological evidence indicates that gymnosperms were wind-pollinated and that insect pollination began in angiosperms in the Lower Cretaceous (ca. 135 mya) leading to close associations between higher plants and their pollinators. Cycads, which were widespread and pervasive throughout the Mesozoic (250-65 mya) are among the most primitive living seed-plants found today. Because pollination by beetles and by thrips has now been detected in several modern cycads, it is attractive to speculate that some insects and cycads had already developed similar mutualistic interactions in the Triassic (250-205 mya), long before the advent of angiosperms. We also draw attention to another key factor in this insect-plant relationship, namely secondary, defensive plant substances which must always have controlled interspecific interactions. Cycads mainly produce toxic azoglucosides and neurotoxic non-protein amino acids (e.g. BMAA), which apparently are crucial elements in the development and maintenance of mutualism (pollination) and parasitism (herbivory) by cycad-linked herbivores. We now add new results on the uptake and storage of the main toxin, cycasin, of the Mexican cycad Zamia furfuracea by its pollinator, the weevil Rhopalotria mollis, and by a specialist herbivore of Zamia integrifolia, the aposematic Atala butterfly Eumaeus atala.     

Tracing the diet of the monitor lizard Varanus mabitang by stable isotope analyses (delta(15)N,delta(13)C)

In this study, we used analyses of stable isotopes of nitrogen ('¹⁵N) and carbon ('¹³C) to determine the trophic ecology of the monitor lizard Varanus mabitang. Stable isotopes from claws, gut contents, and soft tissues were measured from the type specimen. Samples from Varanus olivaceus, Varanus prasinus, Varanus salvator, the herbivorous agamid lizard Hydrosaurus pustulatus, and some plant matter were included for comparison. Our data show a rapid decrease in '¹³C (about10‰) from food plants towards gut contents and soft tissues of herbivorous species. For the varanids, we found a significant linear correlation of decreasing '¹³C and increasing '¹⁵N from herbivorous towards carnivorous species. In terms of trophic isotope ecology, the type specimen of V. mabitang is a strict herbivore. Thus it differs significantly in its isotopic composition from the morphologically next closest related species V. olivaceus. The most highly carnivorous species is V. salvator, while '¹⁵N values for V. prasinus and V. olivaceus are intermediate. Claws provide very valuable samples for such measurements, because they can be sampled from living animals without harm. Additionally, their range of variability is relatively small in comparison with measurements from soft tissues.     

A non-policing honey bee colony (Apis mellifera capensis)

In the Cape honey bee Apis mellifera capensis, workers lay female eggs without mating by thelytokous parthenogenesis. As a result, workers are as related to worker-laid eggs as they are to queen-laid eggs and therefore worker policing is expected to be lower, or even absent. This was tested by transferring worker- and queen-laid eggs into three queenright A. m. capensis discriminator colonies and monitoring their removal. Our results show that worker policing is variable in A. m. capensis and that in one colony worker-laid eggs were not removed. This is the first report of a non-policing queenright honey bee colony. DNA microsatellite and morphometric analysis suggests that the racial composition of the three discriminator colonies was different. The variation in policing rates could be explained by differences in degrees of hybridisation between A. m. capensis and A. m. scutellata, although a larger survey is needed to confirm this.     

"Venom" of the slow loris: sequence similarity of prosimian skin gland protein and Fel d 1 cat allergen

Bites inflicted on humans by the slow loris (Nycticebus coucang), a prosimian from Indonesia, are painful and elicit anaphylaxis. Toxins from N. coucang are thought to originate in the brachial organ, a naked, gland-laden area of skin situated on the flexor surface of the arm that is licked during grooming. We isolated a major component of the brachial organ secretions from N. coucang, an approximately 18 kDa protein composed of two 70-90 amino-acid chains linked by one or more disulfide bonds. The N-termini of these peptide chains exhibit nearly 70% sequence similarity (37% identity, chain 1; 54% identity, chain 2) with the two chains of Fel d 1, the major allergen from the domestic cat (Felis catus). The extensive sequence similarity between the brachial organ component of N. coucang and the cat allergen suggests that they exhibit immunogenic cross-reactivity. This work clarifies the chemical nature of the brachial organ exudate and suggests a possible mode of action underlying the noxious effects of slow loris bites.     

The use of olfaction in the foraging behaviour of the golden-mantled flying fox,<Emphasis Type="Italic"> Pteropus pumilus</Emphasis>, and the greater musky fruit bat,<Emphasis Type="Italic"> Ptenochirus jagori</Emphasis> (Megachiroptera: Pteropodidae)

Double-choice experiments with three adult males of the little golden-mantled flying fox, Pteropus pumilus, and ten adult greater musky fruit bats, Ptenochirus jagori (both Megachiroptera: Pteropodidae), demonstrate that they are able to discriminate accurately between an empty dish and a dish containing fruits of one of several species by odour alone. Tests were run using fruits of six fruit species for Pteropus pumilus and five fruit species for Ptenochirus jagori. The fruit species used are known to be consumed in the wild by Ptenochirus jagori and are, with two exceptions, species of the natural rain-forest habitat. This is the first study to show that fruit bats are also able to assess the ripeness of a fruit exclusively by its odour. The bats preferred ripe over unripe fruits of the same species. Thus, both Pteropus pumilus and Ptenochirus jagori can not only locate fruits by their odour but can also discriminate between ripe and unripe fruits of the same species by olfaction. The results confirm and expand earlier findings on the role of olfactory cues in the orientation of foraging pteropodids.     

Is the contribution of bacteria to terrestrial carbon budget greatly underestimated?

Some commonly found species of soil bacteria use low molecular weight organic acids as their sole source of carbon and energy. This study shows that acids such as citrate and oxalate (produced in large amounts by fungi and plants) can rapidly be consumed by these bacteria. Two strains, Ralstonia eutropha and Xanthobacter autotrophicus, were cultured on acetate- and citrate-rich media. The resulting CO₂ and/or HCO₃^- reacted with calcium ions to precipitate two polymorphs of calcium carbonate (CaCO₃), calcite and vaterite, depending on the quantity of slime produced by the strains. This production of primary calcium carbonate crystals by oxalate- and citrate-degrading bacteria from soil organic carbon sources highlights the existence of an important and underestimated potential carbon sink.     

Thermoregulation and ventilation of termite mounds

Some of the most sophisticated of all animal-built structures are the mounds of African termites of the subfamily Macrotermitinae, the fungus-growing termites. They have long been studied as fascinating textbook examples of thermoregulation or ventilation of animal buildings. However, little research has been designed to provide critical tests of these paradigms, derived from a very small number of original papers. Here I review results from recent studies on Macrotermes bellicosus that considered the interdependence of ambient temperature, thermoregulation, ventilation and mound architecture, and that question some of the fundamental paradigms of termite mounds. M. bellicosus achieves thermal homeostasis within the mound, but ambient temperature has an influence too. In colonies in comparably cool habitats, mound architecture is adapted to reduce the loss of metabolically produced heat to the environment. While this has no negative consequences in small colonies, it produces a trade-off with gas exchange in large colonies, resulting in suboptimally low nest temperatures and increased CO₂ concentrations. Along with the alteration in mound architecture, the gas exchange/ventilation mechanism also changes. While mounds in the thermally appropriate savannah have a very efficient circular ventilation during the day, the ventilation in the cooler forest is a less efficient upward movement of air, with gas exchange restricted by reduced surface exchange area. These results, together with other recent findings, question entrenched ideas such as the thermosiphon-ventilation mechanism or the assumption that mounds function to dissipate internally produced heat. Models trying to explain the proximate mechanisms of mound building, or building elements, are discussed.     

The dinosaurian origin of feathers: perspectives from dolphin (Cetacea) collagen fibers

The early origin of birds is a hotly disputed debate and may be broadly framed as a conflict between paleontologists and ornithologists. The paleontological emphasis has shifted from Archaeopteryx and its origins to recent finds of Cretaceous birds and feathered dinosaurs from China. The identification of alleged feathers has, however, relied principally on the visual image. Some workers have interpreted these integumentary structures as collagen fibers. To test the latter hypothesis, using light microscopy, collagen from the hypodermis (blubber) and subdermal connective tissue sheath was examined from a dolphin that had been buried for a year as part of an experiment. Within the blubber, toward the central thicker parts of the material, the collagen fibers had compacted and the three-dimensional latticework of normal blubber had more or less collapsed. Chromatographic analysis of the blubber revealed pronounced oxidation of the unsaturated lipids, probably accounting for the collapse of the latticework. Fibers normally bound together in bundles became separated into individual fibers or smaller bundles by degradation of the glue-like substance binding them together. These degraded collagen fibers show, in many instances, feather-like patterns, strikingly reminiscent of many of those identified as either protofeathers or modern feathers in dromaeosaurid dinosaurs. The findings throw serious doubt on the virtually complete reliance on visual image by supporters of the feathered dinosaur thesis and emphasize the need for more rigorous methods of identification using modern feathers as a frame of reference. Since collagen is the main fiber type found in most supporting tissues, the results have wide implications regarding the degradation and fossilization of vertebrate integument, such as that of the ichthyosaurs, dinosaurs and birds.     

Alcoholism in cockchafers: orientation of male Melolontha melolontha towards green leaf alcohols

Chemical orientation of the European cockchafer, Melolontha melolontha L., a serious pest in agriculture and horticulture, was investigated by field tests and electrophysiological experiments using plant volatiles. In total, 16 typical plant volatiles were shown to elicit electrophysiological responses in male cockchafers. Funnel trap field bioassays revealed that green leaf alcohols (i.e. (Z)-3-hexen-1-ol, (E)-2-hexen-1-ol and 1-hexanol) attracted males, whereas the corresponding aldehydes and acetates were behaviourally inactive. Furthermore, male cockchafers were attracted by volatiles from mechanically damaged leaves of Fagus sylvatica L., Quercus robur L. and Carpinus betulus L. However, volatiles emitted by damaged leaves of F. sylvatica attracted significantly more males than those from the other host plants. Odour from intact F. sylvatica leaves was not attractive to M. melolontha males. Females were not attracted by any of the tested volatile sources. The results suggest that plant volatiles play a similar role as a sexual kairomone in mate finding of M. melolontha, as has been shown for the forest cockchafer, Melolontha hippocastani F. Nevertheless, both species show remarkable differences in their reaction to green leaf alcohols.     

Mutations for activity level in Drosophila jambulina perturbed its pacemaker that controls circadian eclosion rhythm

Mutations for activity level, designated hpa and hra, in Drosophila jambulina altered properties of the pacemaker controlling eclosion rhythm. Entrainment of eclosion rhythm was studied in light-dark (LD) cycles of 12:12 h at 28°C. The wild type strain entrained to LD cycles but the hpa or hra strain did not. When these strains were released from constant light (LL) to constant darkness (DD), the wild type strain free-ran while other two strains were arrhythmic. Temperature cycles entrained the wild type and hpa strain in DD and LL, and when transferred to constant temperature following thermoperiodic entrainment, the wild type strain free-ran in DD, while the hpa strain free-ran in LL as if the input of LL was essential for its free-running state. Temperature cycles entrained the hra strain in DD but not in LL, and free-running rhythmicities were never established, suggesting that the hra mutation has altered the basic properties of its pacemaker.     

Largest bird from the Early Cretaceous and its implications for the earliest avian ecological diversification

With only one known exception, early Cretaceous birds were smaller than their closest theropod dinosaur relatives. Here we report on a new bird from the Early Cretaceous feathered-dinosaur-bearing continental deposits of Liaoning, northeast China, which is not only larger than Archaeopteryx but is nearly twice as large as the basal dromaeosaur Microraptor. The new taxon, Sapeornis chaoyangensis gen. et sp. nov., has a more basal phylogenetic position than all other birds except for Archaeopteryx. Its exceptionally long forelimbs, well-developed deltoid crest of the humerus, proximally fused metacarpals, relatively short hindlimbs and short pygostyle indicate powerful soaring capability and further suggest that by the Early Cretaceous ecological diversification of early birds was greater than previously assumed. Electronic supplementary material to this paper can be obtained by using the Springer LINK server located at http://dx.doi.org/10.1007/s00114-001-0276-9.