Resurrecting extinct cephalopods with biomimetic robots to explore hydrodynamic stability, maneuverability, and physical constraints on life habits.

Externally shelled cephalopods with coiled, planispiral conchs were ecologically successful for hundreds of millions of years. These animals displayed remarkable morphological disparity, reflecting comparable differences in physical properties that would have constrained their life habits and ecological roles. To investigate these constraints, self-propelling, neutrally buoyant, biomimetic robots were 3D-printed for four disparate morphologies. These robots were engineered to assume orientations computed from virtual hydrostatic simulations while producing Nautilus-like thrusts. Compressed morphotypes had improved hydrodynamic stability (coasting efficiency) and experienced lower drag while jetting backwards. However, inflated morphotypes had improved maneuverability while rotating about the vertical axis. These differences highlight an inescapable physical tradeoff between hydrodynamic stability and yaw maneuverability, illuminating different functional advantages and life-habit constraints across the cephalopod morphospace. This tradeoff reveals there is no single optimum conch morphology, and elucidates the success and iterative evolution of disparate morphologies through deep time, including non-streamlined forms.

Stability-Maneuverability Tradeoffs Provided Diverse Functional Opportunities to Shelled Cephalopods.

Stability-maneuverability tradeoffs impose various constraints on aquatic locomotion. The fossil record houses a massive morphological dataset that documents how organisms have encountered these tradeoffs in an evolutionary framework. Externally shelled cephalopods (e.g., ammonoids and nautiloids) are excellent targets to study physical tradeoffs because they experimented with numerous conch morphologies during their long-lived evolutionary history (around 0.5 billion years). The tradeoff between hydrostatic stability and maneuverability was investigated with neutrally buoyant biomimetic models, engineered to have the same mass distributions computed for their once-living counterparts. Monitoring rocking behavior with 3D motion tracking reveals how stability influenced the life habits of these animals. Cephalopods with short body chambers and rapid whorl expansion (oxycones) more quickly attenuate rocking, while cephalopods with long body chambers (serpenticones and sphaerocones) had improved pitch maneuverability. Disparate conch morphologies presented broad functional opportunities to these animals, imposing several advantages and consequences across the morphospace. These animals navigated inescapable physical constraints enforced by conch geometry, illuminating key relationships between functional diversity and morphological disparity in aquatic ecosystems. Our modeling techniques correct for differences in material properties between physical models and those inferred for their living counterparts. This approach provides engineering solutions to the obstacles created by buoyancy, mass distributions, and moments of inertia, permitting more lifelike, free-swimming biomechanical models and aquatic robots.

Detecting Mismatch in Functional Narratives of Animal Morphology: a Test Case With Fossils.

A boom in technological advancements over the last two decades has driven a surge in both the diversity and power of analytical tools available to biomechanical and functional morphology research. However, in order to adequately investigate each of these dense datasets, one must often consider only one functional narrative at a time. There is more to each organism than any one of these form-function relationships. Joint performance landscapes determined by maximum likelihood are a valuable tool that can be used to synthesize our understanding of these multiple functional hypotheses to further explore an organism's ecology. We present an example framework for applying these tools to such a problem using the morphological transition of ammonoids from the Middle Triassic to the Early Jurassic. Across this time interval, morphospace occupation shifts from a broad occupation across Westermann Morphospace to a dense occupation of a region emphasizing an exposed umbilicus and modest frontal profile. The hydrodynamic capacities and limitations of the shell have seen intense scrutiny as a likely explanation of this transition. However, conflicting interpretations of hydrodynamic performance remain despite this scrutiny, with scant offerings of alternative explanations. Our analysis finds that hydrodynamic measures of performance do little to explain the shift in morphological occupation, highlighting a need for a more robust investigation of alternative functional hypotheses that are often intellectually set aside. With this we show a framework for consolidating the current understanding of the form-function relationships in an organism, and assess when they are insufficiently characterizing the dynamics those data are being used to explain. We aim to encourage the broader adoption of this framework and these ideas as a foundation to bring the field close to comprehensive synthesis and reconstruction of organisms.

Vertical escape tactics and movement potential of orthoconic cephalopods.

Measuring locomotion tactics available to ancient sea animals can link functional morphology with evolution and ecology over geologic timescales. Externally-shelled cephalopods are particularly important for their central roles in marine trophic exchanges, but most fossil taxa lack sufficient modern analogues for comparison. In particular, phylogenetically diverse cephalopods produced orthoconic conchs (straight shells) repeatedly through time. Persistent re-evolution of this morphotype suggests that it possesses adaptive value. Practical lateral propulsion is ruled out as an adaptive driver among orthoconic cephalopods due to the stable, vertical orientations of taxa lacking sufficient counterweights. However, this constraint grants the possibility of rapid (or at least efficient) vertical propulsion. We experiment with this form of movement using 3D-printed models of Baculites compressus, weighted to mimic hydrostatic properties inferred by virtual models. Furthermore, model buoyancy was manipulated to impart simulated thrust within four independent scenarios (Nautilus-like cruising thrust; a similar thrust scaled by the mantle cavity of Sepia; sustained peak Nautilus-like thrust; and passive, slightly negative buoyancy). Each model was monitored underwater with two submerged cameras as they rose/fell over ~2 m, and their kinematics were computed with 3D motion tracking. Our results demonstrate that orthocones require very low input thrust for high output in movement and velocity. With Nautilus-like peak thrust, the model reaches velocities of 1.2 m/s (2.1 body lengths per second) within one second starting from a static initial condition. While cephalopods with orthoconic conchs likely assumed a variety of life habits, these experiments illuminate some first-order constraints. Low hydrodynamic drag inferred by vertical displacement suggests that vertical migration would incur very low metabolic cost. While these cephalopods likely assumed low energy lifestyles day-to-day, they may have had a fighting chance to escape from larger, faster predators by performing quick, upward dodges. The current experiments suggest that orthocones sacrifice horizontal mobility and maneuverability in exchange for highly streamlined, vertically-stable, upwardly-motile conchs.

The limits of convergence: the roles of phylogeny and dietary ecology in shaping non-avian amniote crania.

Cranial morphology is remarkably varied in living amniotes and the diversity of shapes is thought to correspond with feeding ecology, a relationship repeatedly demonstrated at smaller phylogenetic scales, but one that remains untested across amniote phylogeny. Using a combination of morphometric methods, we investigate the links between phylogenetic relationships, diet and skull shape in an expansive dataset of extant toothed amniotes: mammals, lepidosaurs and crocodylians. We find that both phylogeny and dietary ecology have statistically significant effects on cranial shape. The three major clades largely partition morphospace with limited overlap. Dietary generalists often occupy clade-specific central regions of morphospace. Some parallel changes in cranial shape occur in clades with distinct evolutionary histories but similar diets. However, members of a given clade often present distinct cranial shape solutions for a given diet, and the vast majority of species retain the unique aspects of their ancestral skull plan, underscoring the limits of morphological convergence due to ecology in amniotes. These data demonstrate that certain cranial shapes may provide functional advantages suited to particular dietary ecologies, but accounting for both phylogenetic history and ecology can provide a more nuanced approach to inferring the ecology and functional morphology of cryptic or extinct amniotes.

Buoyancy control in ammonoid cephalopods refined by complex internal shell architecture.

The internal architecture of chambered ammonoid conchs profoundly increased in complexity through geologic time, but the adaptive value of these structures is disputed. Specifically, these cephalopods developed fractal-like folds along the edges of their internal divider walls (septa). Traditionally, functional explanations for septal complexity have largely focused on biomechanical stress resistance. However, the impact of these structures on buoyancy manipulation deserves fresh scrutiny. We propose increased septal complexity conveyed comparable shifts in fluid retention capacity within each chamber. We test this interpretation by measuring the liquid retained by septa, and within entire chambers, in several 3D-printed cephalopod shell archetypes, treated with (and without) biomimetic hydrophilic coatings. Results show that surface tension regulates water retention capacity in the chambers, which positively scales with septal complexity and membrane capillarity, and negatively scales with size. A greater capacity for liquid retention in ammonoids may have improved buoyancy regulation, or compensated for mass changes during life. Increased liquid retention in our experiments demonstrate an increase in areas of greater surface tension potential, supporting improved chamber refilling. These findings support interpretations that ammonoids with complex sutures may have had more active buoyancy regulation compared to other groups of ectocochleate cephalopods. Overall, the relationship between septal complexity and liquid retention capacity through surface tension presents a robust yet simple functional explanation for the mechanisms driving this global biotic pattern.

Assessing the Morphological Impacts of Ammonoid Shell Shape through Systematic Shape Variation.

A substantial body of research has been accumulated around ammonoids over several decades. A core aspect of this research has been attempting to infer their life mode from analysis of the morphology of their shells and the drag they incur as that shell is pushed through the water. Tools such as Westermann Morphospace have been developed to investigate and scaffold hypotheses about the results of these investigations. We use computational fluid dynamics to simulate fluid flow around a suite of 24 theoretical ammonoid morphologies to interrogate systematic variations within this space. Our findings uphold some of the long-standing expectations of drag behavior; conch inflation has the greatest influence over ammonoid drag. However, we also find that other long-standing assumptions, such as oxyconic ammonoids being the best swimmers, are subject to substantial variation and nuance resulting from their morphology that is not accounted for through simple drag assessment.

Microbial-caddisfly bioherm association from the Lower Cretaceous Shinekhudag Formation, Mongolia: Earliest record of plant armoring in fossil caddisfly cases.

Caddisfly larvae construct underwater protective cases using surrounding materials, thus providing information on environmental conditions in both modern and ancient systems. Microbial bioherms associated with caddisfly cases are found in the Berriassian-Hauterivian (~140-130 Ma) Shinekhudag Formation of Mongolia, and yield new insights into aspects of lacustrine paleoecosystems and paleoenvironments. This formation contains the earliest record of plant-armored caddisfly cases and a rare occurrence of microbial-caddisfly association from the Mesozoic. The bioherms are investigated within the context of stratigraphic correlations, depositional environment interpretations, and basin-evolution models of the sedimentary fill. The bioherms form 0.5-2.0 m diameter mound-shaped bodies and are concentrated within a single, oil shale-bound stratigraphic interval. Each bioherm is composed of up to 40% caddisfly cases along with stromatolites of millimeter-scale, micritic laminations. Petrographic analyses reveal these bioherms are composed of non-systematic associations of columnar and oncoidal microbialites, constructed around colonies of caddisfly cases. The cases are straight to curved, slightly tapered, and tube-shaped, with a progressively increasing length and width trend (7-21 mm by 1.5-2.5 mm). Despite these variations, the case architectures reveal similar construction materials; the particles used for cases are dominated by plant fragments, ostracod valves, carbonate rocks, and rare mica and feldspar grains. Allochems within the bioherms include ooids, ostracods, plant fragments, rare gastropods, feldspar grains bound in micritic matrices, and are consolidated by carbonate dominated cements. The combination of microbial-caddisfly association, plant fragment case particles, and ooids/oncoids are indicative of a shallow, littoral lake setting. Stratigraphic juxtaposition of nearshore bioherms and the bounding distal oil-shale facies suggests that the bioherms developed in an underfilled lake basin, resulting from an abrupt and short-lived lake desiccation event. Lake chemistry is believed to have been relatively alkaline, saline to hypersaline, and rich in Ca, Mg, and HCO3 ions. Through analyzing bioherm characteristics, caddisfly case architecture, carbonate microfacies, and stratigraphic variability, we infer larger-scale processes that controlled basin development during their formation.

Mercury anomalies and the timing of biotic recovery following the end-Triassic mass extinction.

The end-Triassic mass extinction overlapped with the eruption of the Central Atlantic Magmatic Province (CAMP), and release of CO2 and other volcanic volatiles has been implicated in the extinction. However, the timing of marine biotic recovery versus CAMP eruptions remains uncertain. Here we use Hg concentrations and isotopes as indicators of CAMP volcanism in continental shelf sediments, the primary archive of faunal data. In Triassic-Jurassic strata, Muller Canyon, Nevada, Hg levels rise in the extinction interval, peak before the appearance of the first Jurassic ammonite, remain above background in association with a depauperate fauna, and fall to pre-extinction levels during significant pelagic and benthic faunal recovery. Hg isotopes display no significant mass independent fractionation within the extinction and depauperate intervals, consistent with a volcanic origin for the Hg. The Hg and palaeontological evidence from the same archive indicate that significant biotic recovery did not begin until CAMP eruptions ceased.