Time-dependent Changes in Shrimp Armor and Escape Kinematics under Ocean Acidification and Warming.

Pandalid shrimp use morphological and behavioral defenses against their numerous fish and invertebrate predators. Their rapid tail-flip escape and rigid exoskeleton armor may be sensitive to changes in ocean temperature and carbon chemistry in ways that alter their efficacy and impact mortality. Here we tested the hypothesis that ocean warming and acidification conditions affect the antipredator defenses of Pandalus gurneyi. To test this hypothesis, we exposed shrimp to a combination of pH (8.0, 7.7, 7.5) and temperature (13°C, 17°C) treatments and assessed their tail-flip escape and exoskeleton armor after short-term (2 weeks) and medium-term (3 months) exposure. Results revealed complex effects on escape kinematics, with changes in different variables explained by either pH, temperature, and/or their interaction; decreased pH, for instance, primarily explains reduced acceleration while cold temperature explains increased flexion duration. Carapace mineral content (Ca and Mg) was unaffected, but warmer temperatures primarily drove enhanced mechanical properties (increased hardness and stiffness). No effects were observed in the stiffness and strength of the rostrum. Furthermore, most of the observed effects were temporary, as they occurred after short-term exposure (2 weeks), but disappeared after longer exposure (3 months). This demonstrates that P. gurneyi defenses are affected by short-term exposure to temperature and pH variations; however, they can acclimate to these conditions over time. Nonetheless, changes in the tail-flip escape kinematics may be disadvantageous when trying to flee predators and the enhanced exoskeleton armor could make them more resistant to predation during short periods of environmental change.

From Telson to Attack in Mantis Shrimp: Bridging Biomechanics and Behavior in Crustacean Contests.

In the spirit of this symposium on the physical mechanisms of behavior, we review mantis shrimp ritualized fighting, from the telson to the attack, as an inspiring example of how the integration of biomechanics and behavioral research can yield a penetrating narrative for how animals accomplish important activities, including agonistic actions. Resolving conflicts with conspecifics over valuable resources is an essential task for animals, and this takes an unusual form in mantis shrimp due to their powerful raptorial appendages. Decades of field and laboratory research have provided key insights into the natural agonistic interactions of diverse mantis shrimp species, including how they use their raptorial weapons against one another in telson sparring matches over cavities. These insights provided the foundation for functional morphologists, biomechanists, and engineers to work through different levels of organization: from the kinematics of how the appendages move to the elastic mechanisms that power the strike, and down to the structure, composition, and material properties that transmit and protect against high-impact forces. Completing this narrative are studies on the defensive telson and how this structure is biomechanically matched to the weapon and the role it plays in ritualized fighting. The biomechanical understanding of the weapon and defense in mantis shrimp has, in turn, enabled a better understanding of whether mantis shrimp assess one another during contests and encouraged questions of evolutionary drivers on both the arsenal and behavior. Altogether, the body of research focused on mantis shrimp has presented perhaps the most comprehensive understanding of fighting, weapons, and defenses among crustaceans, from morphology and biomechanics to behavior and evolution. While this multi-level analysis of ritualized fighting in mantis shrimp is comprehensive, we implore the need to include additional levels of analysis to obtain a truly holistic understanding of this and other crustacean agonistic interactions. Specifically, both molting and environmental conditions are often missing from the narrative, yet they greatly affect crustacean weapons, defenses, and behavior. Applying this approach more broadly would generate a similarly profound understanding of how crustaceans carry out a variety of important tasks in diverse habitats.

Growling from the gut: co-option of the gastric mill for acoustic communication in ghost crabs.

Animal acoustic communication systems can be built upon co-opted structures that become specialized for sound production or morphological novelties. The ghost crab, Ocypode quadrata, evolved a novel stridulation apparatus on the claws that is used during agonistic interactions, but they also produce a rasping sound without their claw apparatus. We investigated the nature of these sounds and show that O. quadrata adopted a unique and redundant mode of sound production by co-opting the gastric mill (grinding teeth of the foregut). Acoustic characteristics of the sound are consistent with stridulation and are produced by both male and female crabs during aggressive interactions. Laser Doppler vibrometry localized the source of maximum vibration to the gastric region and fluoroscopy showed movement of the gastric mill that coincided with stridulation. The lateral teeth of the gastric mill possess a series of comb-like structures that rub against the median tooth to produce stridulation with dominant frequencies below 2 kHz. This previously undescribed gastric stridulation can be modulated and provide a means of assessment during aggressive interactions, similar to the use of the claw stridulation apparatus. This functional redundancy of stridulation in crabs offers unique insights into the mechanisms of evolution of acoustic communication systems.

Evolution of mantis shrimp telson armour and its role in ritualized fighting.

Mantis shrimp possess both formidable weapons and impact-resistant armour that clash during ritualized combat. The telson is one of few biological structures known to withstand the repeated high impact forces of smashing mantis shrimp strikes, and it is hypothesized that this pairing of armour and weapon is associated with the evolution of telson sparring. We carried out a comparative analysis of telson impact mechanics across 15 mantis shrimp species to assess if the telsons of sparring species (i) are consistently specialized for impact-resistance, (ii) are more impact-resistant than those of non-sparring species, and (iii) have impact parameters that correlate with body size, and thereby useful for assessment. Our data from ball drop tests show that the telsons of all species function like a stiff spring that dissipates most of the impact energy, but none of the measured impact parameters are correlated with the occurrence of sparring behaviour. Impact parameters were correlated with body mass for only some species, suggesting that it is not broadly useful for size assessment during ritualized fighting. Contrary to expectation, sparring mantis shrimp do not appear to have coevolved telson armour that is more robust to impact than non-sparring species. Rather, telson structure is inherently impact-resistant.

No compromise between metabolism and behavior of decorator crabs in reduced pH conditions.

Many marine calcifiers experience metabolic costs when exposed to experimental ocean acidification conditions, potentially limiting the energy available to support regulatory processes and behaviors. Decorator crabs expend energy on decoration camouflage and may face acute trade-offs under environmental stress. We hypothesized that under reduced pH conditions, decorator crabs will be energy limited and allocate energy towards growth and calcification at the expense of decoration behavior. Decorator crabs, Pelia tumida, were exposed to ambient (8.01) and reduced (7.74) pH conditions for five weeks. Half of the animals in each treatment were given sponge to decorate with. Animals were analyzed for changes in body mass, exoskeleton mineral content (Ca and Mg), organic content (a proxy for metabolism), and decoration behavior (sponge mass and percent cover). Overall, decorator crabs showed no signs of energy limitation under reduced pH conditions. Exoskeleton mineral content, body mass, and organic content of crabs remained the same across pH and decoration treatments, with no effect of reduced pH on decoration behavior. Despite being a relatively inactive, osmoconforming species, Pelia tumida is able to maintain multiple regulatory processes and behavior when exposed to environmental pH stress, which underscores the complexity of responses within Crustacea to ocean acidification conditions.

Aquatic versus terrestrial crab skeletal support: morphology, mechanics, molting and scaling.

The transition from aquatic to terrestrial environments places significant mechanical challenges on skeletal support systems. Crabs have made this transition multiple times and are the largest arthropods to inhabit both environments. Furthermore, they alternate between rigid and hydrostatic skeletons, making them an interesting system to examine mechanical adaptations in skeletal support systems. I hypothesized that terrestrial crabs have modified morphology to enhance mechanical stiffness and that rigid and hydrostatic skeletons scale differently from each other, with stronger allometric relationships on land. Using the aquatic blue crab, Callinectes sapidus, and the terrestrial blackback land crab, Gecarcinus lateralis, I measured and compared body mass, merus morphology (dimensions, cuticle thickness and the second moment of area I) and mechanics (flexural stiffness EI, elastic modulus E, critical stress and hydrostatic pressure) of rigid and hydrostatic stage crabs encompassing a range of sizes (C. sapidus: 1.5-133 g, N≤24; G. lateralis: 22-70 g, N≤15). The results revealed that rigid G. lateralis has similar morphology (limb length to diameter L/D and cuticle thickness to limb diameter T/D ratio) to C. sapidus, and the mechanics and most scaling relationships are the same. Hydrostatic land crabs differ from aquatic crabs by having different morphology (thinner cuticle), mechanics (greater internal pressures) and scaling relationship (cuticle thickness). These results suggest that the rigid crab body plan is inherently overbuilt and sufficient to deal with the greater gravitational loading that occurs on land, while mechanical adaptations are important for hydrostatically supported crabs. Compared with other arthropods and hydrostatic animals, crabs possess distinct strategies for adapting mechanically to life on land.

Stress physiology and weapon integrity of intertidal mantis shrimp under future ocean conditions.

Calcified marine organisms typically experience increased oxidative stress and changes in mineralization in response to ocean acidification and warming conditions. These effects could hinder the potency of animal weapons, such as the mantis shrimp's raptorial appendage. The mechanical properties of this calcified weapon enable extremely powerful punches to be delivered to prey and aggressors. We examined oxidative stress and exoskeleton structure, mineral content, and mechanical properties of the raptorial appendage and the carapace under long-term ocean acidification and warming conditions. The predatory appendage had significantly higher % Mg under ocean acidification conditions, while oxidative stress levels as well as the % Ca and mechanical properties of the appendage remained unchanged. Thus, mantis shrimp tolerate expanded ranges of pH and temperature without experiencing oxidative stress or functional changes to their weapons. Our findings suggest that these powerful predators will not be hindered under future ocean conditions.

A Protocol for Bioinspired Design: A Ground Sampler Based on Sea Urchin Jaws.

Bioinspired design is an emerging field that takes inspiration from nature to develop high-performance materials and devices. The sea urchin mouthpiece, known as the Aristotle's lantern, is a compelling source of bioinspiration with an intricate network of musculature and calcareous teeth that can scrape, cut, chew food and bore holes into rocky substrates. We describe the bioinspiration process as including animal observation, specimen characterization, device fabrication and mechanism bioexploration. The last step of bioexploration allows for a deeper understanding of the initial biology. The design architecture of the Aristotle's lantern is analyzed with micro-computed tomography and individual teeth are examined with scanning electron microscopy to identify the microstructure. Bioinspired designs are fabricated with a 3D printer, assembled and tested to determine the most efficient lantern opening and closing mechanism. Teeth from the bioinspired lantern design are bioexplored via finite element analysis to explain from a mechanical perspective why keeled tooth structures evolved in the modern sea urchins we observed. This circular approach allows for new conclusions to be drawn from biology and nature.

Structure and mechanical properties of selected protective systems in marine organisms.

Marine organisms have developed a wide variety of protective strategies to thrive in their native environments. These biological materials, although formed from simple biopolymer and biomineral constituents, take on many intricate and effective designs. The specific environmental conditions that shape all marine organisms have helped modify these materials into their current forms: complete hydration, and variation in hydrostatic pressure, temperature, salinity, as well as motion from currents and swells. These conditions vary throughout the ocean, being more consistent in the pelagic and deep benthic zones while experiencing more variability in the nearshore and shallows (e.g. intertidal zones, shallow bays and lagoons, salt marshes and mangrove forests). Of note, many marine organisms are capable of migrating between these zones. In this review, the basic building blocks of these structural biological materials and a variety of protective strategies in marine organisms are discussed with a focus on their structure and mechanical properties. Finally, the bioinspired potential of these biological materials is discussed.

Effects of CO2-induced pH reduction on the exoskeleton structure and biophotonic properties of the shrimp Lysmata californica.

The anticipated effects of CO2-induced ocean acidification on marine calcifiers are generally negative, and include dissolution of calcified elements and reduced calcification rates. Such negative effects are not typical of crustaceans for which comparatively little ocean acidification research has been conducted. Crustaceans, however, depend on their calcified exoskeleton for many critical functions. Here, we conducted a short-term study on a common caridean shrimp, Lysmata californica, to determine the effect of CO2-driven reduction in seawater pH on exoskeleton growth, structure, and mineralization and animal cryptic coloration. Shrimp exposed to ambient (7.99 ± 0.04) and reduced pH (7.53 ± 0.06) for 21 days showed no differences in exoskeleton growth (percent increase in carapace length), but the calcium weight percent of their cuticle increased significantly in reduced pH conditions, resulting in a greater Ca:Mg ratio. Cuticle thickness did not change, indicating an increase in the mineral to matrix ratio, which may have mechanical consequences for exoskeleton function. Furthermore, there was a 5-fold decrease in animal transparency, but no change in overall shrimp coloration (red). These results suggest that even short-term exposure to CO2-induced pH reduction can significantly affect exoskeleton mineralization and shrimp biophotonics, with potential impacts on crypsis, physical defense, and predator avoidance.

Mechanical properties of the rigid and hydrostatic skeletons of molting blue crabs, Callinectes sapidus Rathbun.

Molting in crustaceans involves significant changes in the structure and function of the exoskeleton as the old cuticle is shed and a new one is secreted. The flimsy new cuticle takes several days to harden and during this time crabs rely on a hydrostatic skeletal support system for support and movement. This change from a rigid to a hydrostatic skeletal support mechanism implies correlated changes in the function, and thus mechanical properties, of the cuticle. In particular, it must change from primarily resisting compression, bending and torsional forces to resisting tension. This study was designed to explore the changes in the mechanical properties of the crustacean cuticle as the animals switch between two distinct skeletal support mechanisms. Samples of cuticle were removed from blue crabs, Callinectes sapidus, at 1 h (soft-shell stage), 12 h (paper-shell stage), and 7 days (hard-shell stage) following molting. We measured and compared the flexural stiffness, Young's modulus of elasticity (in tension), and tensile strength for each postmolt stage. We found that the hard-shell cuticle has a flexural stiffness fully four orders of magnitude greater than the soft-shell and paper-shell cuticle. Although the soft-shell cuticle has a Young's modulus significantly lower than that of the paper-shell and hard-shell cuticle, it has the same tensile strength. Thus, the soft-shell and paper-shell cuticles are unable to resist the significant bending forces associated with a rigid skeletal support system, but can resist the tensile forces that characterize hydrostatic support systems. The mechanical properties of the cuticle thus change dramatically during molting in association with the change in function of the cuticle. These results emphasize the significant role that mechanics plays in the evolution of the molting process in arthropods, and possibly other ecdysozoans.

Biomechanics: a pneumo-hydrostatic skeleton in land crabs.

Like their aquatic counterparts, terrestrial crabs repeatedly shed their rigid exoskeleton during moulting. But in the case of land crabs, little water is available to provide a temporary hydrostatic skeleton before the new skeleton hardens, and air does not provide the buoyancy necessary to support the animal. Here we show that whenever its exoskeleton is shed, the blackback land crab Gecarcinus lateralis relies on an unconventional type of hydrostatic skeleton that uses both gas and liquid (a 'pneumo-hydrostat'). To our knowledge, this is the first experimental evidence for a locomotor skeleton that depends on a gas. It establishes a new category of hydrostatic skeletal support and possibly a critical adaptation to life on land for the Crustacea.

Switching skeletons: hydrostatic support in molting crabs.

Skeletal support systems are essential for support, movement, muscular antagonism, and locomotion. Crustaceans shed their rigid exoskeleton at each molt yet are still capable of forceful movement. We hypothesize that the soft water-inflated body of newly molted crabs may rely on a hydrostatic skeleton, similar to that of worms and polyps. We measured internal hydrostatic pressure and the force exerted during claw adduction and observed a strong correlation between force and hydrostatic pressure, consistent with hydrostatic skeletal support. This alternation between the two basic skeletal types may be widespread among arthropods.