Oxygen Isotope Variability within Nautilus Shell Growth Bands

Nautilus is often used as an analogue for the ecology and behavior of extinct externally shelled cephalopods. Nautilus shell grows quickly, has internal growth banding, and is widely believed to precipitate aragonite in oxygen isotope equilibrium with seawater. Pieces of shell from a wild-caught Nautilus macromphalus from New Caledonia and from a Nautilus belauensis reared in an aquarium were cast in epoxy, polished, and then imaged. Growth bands were visible in the outer prismatic layer of both shells. The thicknesses of the bands are consistent with previously reported daily growth rates measured in aquarium reared individuals. In situ analysis of oxygen isotope ratios using secondary ion mass spectrometry (SIMS) with 10 μm beam-spot size reveals inter- and intra-band δ18O variation. In the wild-caught sample, a traverse crosscutting 45 growth bands yielded δ18O values ranging 2.5‰, from +0.9 to -1.6 ‰ (VPDB), a range that is larger than that observed in many serial sampling of entire shells by conventional methods. The maximum range within a single band (~32 μm) was 1.5‰, and 27 out of 41 bands had a range larger than instrumental precision (±2 SD = 0.6‰). The results from the wild individual suggest depth migration is recorded by the shell, but are not consistent with a simple sinusoidal, diurnal depth change pattern. To create the observed range of δ18O, however, this Nautilus must have traversed a temperature gradient of at least ~12°C, corresponding to approximately 400 m depth change. Isotopic variation was also measured in the aquarium-reared sample, but the pattern within and between bands likely reflects evaporative enrichment arising from a weekly cycle of refill and replacement of the aquarium water. Overall, this work suggests that depth migration behavior in ancient nektonic mollusks could be elucidated by SIMS analysis across individual growth bands

Controlled Chaos of Polymorphic Mucins in a Metazoan Parasite (Schistosoma mansoni) Interacting with Its Invertebrate Host (Biomphalaria glabrata)

Invertebrates were long thought to possess only a simple, effective and hence non-adaptive defence system against microbial and parasitic attacks. However, recent studies have shown that invertebrate immunity also relies on immune receptors that diversify (e.g. in echinoderms, insects and mollusks (Biomphalaria glabrata)). Apparently, individual or population-based polymorphism-generating mechanisms exists that permit the survival of invertebrate species exposed to parasites. Consequently, the generally accepted arms race hypothesis predicts that molecular diversity and polymorphism also exist in parasites of invertebrates. We investigated the diversity and polymorphism of parasite molecules (Schistosoma mansoni Polymorphic Mucins, SmPoMucs) that are key factors for the compatibility of schistosomes interacting with their host, the mollusc Biomphalaria glabrata. We have elucidated the complex cascade of mechanisms acting both at the genomic level and during expression that confer polymorphism to SmPoMuc. We show that SmPoMuc is coded by a multi-gene family whose members frequently recombine. We show that these genes are transcribed in an individual-specific manner, and that for each gene, multiple splice variants exist. Finally, we reveal the impact of this polymorphism on the SmPoMuc glycosylation status. Our data support the view that S. mansoni has evolved a complex hierarchical system that efficiently generates a high degree of polymorphism—a “controlled chaos”—based on a relatively low number of genes. This contrasts with protozoan parasites that generate antigenic variation from large sets of genes such as Trypanosoma cruzi, Trypanosoma brucei and Plasmodium falciparum. Our data support the view that the interaction between parasites and their invertebrate hosts are far more complex than previously thought. While most studies in this matter have focused on invertebrate host diversification, we clearly show that diversifying mechanisms also exist on the parasite side of the interaction. Our findings shed new light on how and why invertebrate immunity develops

Catálogo Taxonômico da Fauna do Brasil: setting the baseline knowledge on the animal diversity in Brazil

The limited temporal completeness and taxonomic accuracy of species lists, made available in a traditional manner in scientific publications, has always represented a problem. These lists are invariably limited to a few taxonomic groups and do not represent up-to-date knowledge of all species and classifications. In this context, the Brazilian megadiverse fauna is no exception, and the Catálogo Taxonômico da Fauna do Brasil (CTFB) (http://fauna.jbrj.gov.br/), made public in 2015, represents a database on biodiversity anchored on a list of valid and expertly recognized scientific names of animals in Brazil. The CTFB is updated in near real time by a team of more than 800 specialists. By January 1, 2024, the CTFB compiled 133,691 nominal species, with 125,138 that were considered valid. Most of the valid species were arthropods (82.3%, with more than 102,000 species) and chordates (7.69%, with over 11,000 species). These taxa were followed by a cluster composed of Mollusca (3,567 species), Platyhelminthes (2,292 species), Annelida (1,833 species), and Nematoda (1,447 species). All remaining groups had less than 1,000 species reported in Brazil, with Cnidaria (831 species), Porifera (628 species), Rotifera (606 species), and Bryozoa (520 species) representing those with more than 500 species. Analysis of the CTFB database can facilitate and direct efforts towards the discovery of new species in Brazil, but it is also fundamental in providing the best available list of valid nominal species to users, including those in science, health, conservation efforts, and any initiative involving animals. The importance of the CTFB is evidenced by the elevated number of citations in the scientific literature in diverse areas of biology, law, anthropology, education, forensic science, and veterinary science, among others

Oxygen Isotope Variability within Nautilus Shell Growth Bands

Nautilus is often used as an analogue for the ecology and behavior of extinct externally shelled cephalopods. Nautilus shell grows quickly, has internal growth banding, and is widely believed to precipitate aragonite in oxygen isotope equilibrium with seawater. Pieces of shell from a wild-caught Nautilus macromphalus from New Caledonia and from a Nautilus belauensis reared in an aquarium were cast in epoxy, polished, and then imaged. Growth bands were visible in the outer prismatic layer of both shells. The thicknesses of the bands are consistent with previously reported daily growth rates measured in aquarium reared individuals. In situ analysis of oxygen isotope ratios using secondary ion mass spectrometry (SIMS) with 10 μm beam-spot size reveals inter- and intra-band δ18O variation. In the wild-caught sample, a traverse crosscutting 45 growth bands yielded δ18O values ranging 2.5‰, from +0.9 to -1.6 ‰ (VPDB), a range that is larger than that observed in many serial sampling of entire shells by conventional methods. The maximum range within a single band (~32 μm) was 1.5‰, and 27 out of 41 bands had a range larger than instrumental precision (±2 SD = 0.6‰). The results from the wild individual suggest depth migration is recorded by the shell, but are not consistent with a simple sinusoidal, diurnal depth change pattern. To create the observed range of δ18O, however, this Nautilus must have traversed a temperature gradient of at least ~12°C, corresponding to approximately 400 m depth change. Isotopic variation was also measured in the aquarium-reared sample, but the pattern within and between bands likely reflects evaporative enrichment arising from a weekly cycle of refill and replacement of the aquarium water. Overall, this work suggests that depth migration behavior in ancient nektonic mollusks could be elucidated by SIMS analysis across individual growth bands

Mechanistic Thermal Modeling of Late Triassic Terrestrial Amniotes Predicts Biogeographic Distribution

The biogeography of terrestrial amniotes is controlled by historical contingency interacting with paleoclimate, morphology and physiological constraints to dispersal. Thermal tolerance is the intersection between organismal requirements and climate conditions which constrains modern organisms to specific locations and was likely a major control on ancient tetrapods. Here, we test the extent of controls exerted by thermal tolerance on the biogeography of 13 Late Triassic tetrapods using a mechanistic modeling program, Niche Mapper. This program accounts for heat and mass transfer into and out of organisms within microclimates. We model our 13 tetrapods in four different climates (cool and warm at low and high latitudes) using environmental conditions that are set using geochemical proxy-based general circulation models. Organismal conditions for the taxa are from proxy-based physiological values and phylogenetic bracketing. We find that thermal tolerances are a sufficient predictor for the latitudinal distribution of our 13 test taxa in the Late Triassic. Our modeled small mammaliamorph can persist at high latitudes with nocturnal activity and daytime burrowing but large pseudosuchians are excluded because they cannot seek nighttime shelter in burrows to retain elevated body temperatures. Our work demonstrates physiological modeling is useful for quantitative testing of the thermal exclusion hypothesis for tetrapods in deep time

Recent advances in heteromorph ammonoid palaeobiology

Heteromorphs are ammonoids forming a conch with detached whorls (open coiling) or non‐planispiral coiling. Such aberrant forms appeared convergently four times within this extinct group of cephalopods. Since Wiedmann's seminal paper in this journal, the palaeobiology of heteromorphs has advanced substantially. Combining direct evidence from their fossil record, indirect insights from phylogenetic bracketing, and physical as well as virtual models, we reach an improved understanding of heteromorph ammonoid palaeobiology. Their anatomy, buoyancy, locomotion, predators, diet, palaeoecology, and extinction are discussed. Based on phylogenetic bracketing with nautiloids and coleoids, heteromorphs like other ammonoids had 10 arms, a well‐developed brain, lens eyes, a buccal mass with a radula and a smaller upper as well as a larger lower jaw, and ammonia in their soft tissue. Heteromorphs likely lacked arm suckers, hooks, tentacles, a hood, and an ink sac. All Cretaceous heteromorphs share an aptychus‐type lower jaw with a lamellar calcitic covering. Differences in radular tooth morphology and size in heteromorphs suggest a microphagous diet. Stomach contents of heteromorphs comprise planktic crustaceans, gastropods, and crinoids, suggesting a zooplanktic diet. Forms with a U‐shaped body chamber (ancylocone) are regarded as suspension feeders, whereas orthoconic forms additionally might have consumed benthic prey. Heteromorphs could achieve near‐neutral buoyancy regardless of conch shape or ontogeny. Orthoconic heteromorphs likely had a vertical orientation, whereas ancylocone heteromorphs had a near‐horizontal aperture pointing upwards. Heteromorphs with a U‐shaped body chamber are more stable hydrodynamically than modern Nautilus and were unable substantially to modify their orientation by active locomotion, i.e. they had no or limited access to benthic prey at adulthood. Pathologies reported for heteromorphs were likely inflicted by crustaceans, fish, marine reptiles, and other cephalopods. Pathologies on Ptychoceras corroborates an external shell and rejects the endocochleate hypothesis. Devonian, Triassic, and Jurassic heteromorphs had a preference for deep‐subtidal to offshore facies but are rare in shallow‐subtidal, slope, and bathyal facies. Early Cretaceous heteromorphs preferred deep‐subtidal to bathyal facies. Late Cretaceous heteromorphs are common in shallow‐subtidal to offshore facies. Oxygen isotope data suggest rapid growth and a demersal habitat for adult Discoscaphites and Baculites. A benthic embryonic stage, planktic hatchlings, and a habitat change after one whorl is proposed for Hoploscaphites. Carbon isotope data indicate that some Baculites lived throughout their lives at cold seeps. Adaptation to a planktic life habit potentially drove selection towards smaller hatchlings, implying high fecundity and an ecological role of the hatchlings as micro‐ and mesoplankton. The Chicxulub impact at the Cretaceous/Paleogene (K/Pg) boundary 66 million years ago is the likely trigger for the extinction of ammonoids. Ammonoids likely persisted after this event for 40–500 thousand years and are exclusively represented by heteromorphs. The ammonoid extinction is linked to their small hatchling sizes, planktotrophic diets, and higher metabolic rates than in nautilids, which survived the K/Pg mass extinction event

Mechanistic Thermal Modeling of Late Triassic Terrestrial Amniotes Predicts Biogeographic Distribution

The biogeography of terrestrial amniotes is controlled by historical contingency interacting with paleoclimate, morphology and physiological constraints to dispersal. Thermal tolerance is the intersection between organismal requirements and climate conditions which constrains modern organisms to specific locations and was likely a major control on ancient tetrapods. Here, we test the extent of controls exerted by thermal tolerance on the biogeography of 13 Late Triassic tetrapods using a mechanistic modeling program, Niche Mapper. This program accounts for heat and mass transfer into and out of organisms within microclimates. We model our 13 tetrapods in four different climates (cool and warm at low and high latitudes) using environmental conditions that are set using geochemical proxy-based general circulation models. Organismal conditions for the taxa are from proxy-based physiological values and phylogenetic bracketing. We find that thermal tolerances are a sufficient predictor for the latitudinal distribution of our 13 test taxa in the Late Triassic. Our modeled small mammaliamorph can persist at high latitudes with nocturnal activity and daytime burrowing but large pseudosuchians are excluded because they cannot seek nighttime shelter in burrows to retain elevated body temperatures. Our work demonstrates physiological modeling is useful for quantitative testing of the thermal exclusion hypothesis for tetrapods in deep time

Modeling Dragons: Using linked mechanistic physiological and microclimate models to explore environmental, physiological, and morphological constraints on the early evolution of dinosaurs.

We employed the widely-tested biophysiological modeling software, Niche Mapper™ to investigate the metabolic function of the Late Triassic dinosaurs Plateosaurus and Coelophysis during global greenhouse conditions. We tested a variety of assumptions about resting metabolic rate, each evaluated within six microclimate models that bound paleoenvironmental conditions at 12° N paleolatitude, as determined by sedimentological and isotopic proxies for climate within the Chinle Formation of the southwestern United States. Sensitivity testing of metabolic variables and simulated "metabolic chamber" analyses support elevated "ratite-like" metabolic rates and intermediate "monotreme-like" core temperature ranges in these species of early saurischian dinosaur. Our results suggest small theropods may have needed partial to full epidermal insulation in temperate environments, while fully grown prosauropods would have likely been heat stressed in open, hot environments and should have been restricted to cooler microclimates such as dense forests or higher latitudes and elevations. This is in agreement with the Late Triassic fossil record and may have contributed to the latitudinal gap in the Triassic prosauropod record

The outer prismatic layer of a portion of the polished surface from <i>Nautilus macromphalus</i> (AMNH 105621) imaged by four different techniques: A) SE, B) CLFM, C) Plain light dissecting microscope, D) UV.

<p>The oldest shell precipitated is in the upper right corner of all images. Growth proceeds to the lower left. All images are of the same portion of the shell. Five bands are highlighted with white lines. A) SE image showing the polished shell surface. Lines of pores in the SE image (A) correlate to low fluorescence in CLFM (B), bright portions of the band in the plain light correlate to dissecting microscope image (C) and dark portions in the long wavelength UV (~360 nm) fluorescence image (D). These cavities are the same as those intersected by some SIMS analysis pits (<a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0153890#pone.0153890.g004" target="_blank">Fig 4</a>). B) CLFM (true color) image showing growth bands. Growth bands extend from the exterior surface of the outer prismatic layer (top of the image) to the interior boundary with the nacreous layer. Note that the banding closer to the nacreous boundary is more pronounced than the banding toward the exterior of the shell. C) Plain-light dissecting microscope image (true color) of polished shell surface. Banding is apparent but discontinuous. D) UV fluorescence (true color) image of the shell. Faint banding is present with an orientation equal to that found in other imaging techniques. CLFM images on the uncoated sample mount were made using a Bio-Rad MRC-1024 scanning confocal microscope at the W. M. Keck Laboratory for Biological Imaging at UW-Madison operated with a 40 mW laser at a wavelength of 488 nm. Images of banding within the outer prismatic layer were best expressed through an emission filter that detects visible green light (λ = 505 to 539 nm). Growth-band orientation in the prismatic layer was used to place SIMS transects.</p

SIMS results and CLFM brightness for transects perpendicular to banding in the outer prismatic layer of the wild-caught <i>Nautilus macromphalus</i> (AMNH 105621).

<p>SIMS analysis and CLFM imaging was done on this 8 mm long portion of vacuum roasted and polished <i>Nautilus macromphalus</i> shell. The background grayscale is based on the residual CLFM brightness after lowess regression to correct for differences in brightness within and between images. Oxygen isotope ratios are plotted against hours of growth, assuming that each dark-light-dark cycle is 24 hours. The most recently precipitated shell is at time 0. Overlapping transects are color coded to show where correlation across the shell was carried out to produce the composite record. Transect locations are highlighted on the CLFM image of the outer prismatic layer. Correlation shows agreement within instrumental precision between transects correlated across the shell. There is considerable oxygen isotope variability within daily individual growth bands and across multiple bands. A higher resolution map of the shell surface is available in the supplementary information (<a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0153890#pone.0153890.s001" target="_blank">S1 Fig</a>).</p