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.

External Reinfection of a Fungal Pathogen Does not Contribute to Pathogen Growth.

Chytridiomycosis is an emerging infectious disease of amphibians caused by the fungal pathogen Batrachochytrium dendrobatidis (Bd), which has led to devastating declines in amphibian populations worldwide. Current theory predicts that Bd infections are maintained through both reproduction on the host's skin and reinfection from sources outside of the host. To investigate the importance of external reinfection on pathogen burden, we infected captive-bred individuals of the highly susceptible Panamanian Golden Frog, Atelopus glyphus, and wild-caught glass frogs, Espadarana prosoblepon, with Bd. We housed the animals in one of three treatments: individually, in heterospecific pairs, and in conspecific pairs. For 8 weeks, we measured the Bd load and shedding rate of all frogs. We found that Atelopus had high rates of increase in both Bd load and shedding rate, but pathogen growth rates did not differ among treatments. The infection intensity of Espadarana co-housed with Atelopus was indistinguishable from those housed singly and those in conspecific pairs, despite being exposed to a large external source of Bd zoospores. Our results indicate that Bd load in both species is driven by pathogen replication within an individual, with reinfection from outside the host contributing little to the amplification of host fungal load.

The role of feeding morphology and competition in governing the diet breadth of sympatric stomatopod crustaceans.

Competition for food drives divergence and specialization in feeding morphology. Stomatopod crustaceans have two kinds of highly specialized feeding appendages: either elongate spear-like appendages (spearers) used to ambush soft-bodied evasive prey or hammer-like appendages (smashers) that produce extremely high forces used both to break hard-shelled prey and to capture evasive prey. To evaluate associations between appendage type and feeding ecology, the diet of two small smasher and spearer species (size range: 21-27 mm) that co-occur were compared. Stable isotope analysis and the Bayesian mixing model MixSIAR were used to estimate the proportional contributions of prey types to the diet. Both species had relatively wide diets that included hard-shelled and soft-bodied prey, albeit in different proportions; the smasher consumed a greater proportion of hard-shelled prey, and the spearer consumed mostly soft-bodied prey. Appendage kinematics in stomatopods is known to scale linearly across species. These two small species may produce similar kinematics allowing them both to capture evasive prey and hammer hard-shelled prey, thereby widening their diets. Yet, the spearer species is more highly adept at capturing evasive prey, indicating that small spearers are stronger competitors for soft-bodied prey. These findings suggest that a smasher's ability to access hard prey reduced competition for soft prey, and therefore conferred an important benefit favouring the evolution of the impressive smashing strike.

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.

Specialized morphology corresponds to a generalist diet: linking form and function in smashing mantis shrimp crustaceans.

Many animals are considered to be specialists because they have feeding structures that are fine-tuned for consuming specific prey. For example, "smasher" mantis shrimp have highly specialized predatory appendages that generate forceful strikes to break apart hard-shelled prey. Anecdotal observations suggest, however, that the diet of smashers may include soft-bodied prey as well. Our goal was to examine the diet breadth of the smasher mantis shrimp, Neogonodactylus bredini, to determine whether it has a narrow diet of hard-shelled prey. We combined studies of prey abundance, feeding behavior, and stable isotope analyses of diet in both seagrass and coral rubble to determine if N. bredini's diet was consistent across different habitat types. The abundances of hard-shelled and soft-bodied prey varied between habitats. In feeding experiments, N. bredini consumed both prey types. N. bredini consumed a range of different prey in the field as well and, unexpectedly, the stable isotope analysis demonstrated that soft-bodied prey comprised a large proportion (29-53 %) of the diet in both habitats. Using a Bayesian mixing model framework (MixSIAR), we found that this result held even when we used uninformative, or generalist, priors and informative priors reflecting a specialist diet on hard-shelled prey and prey abundances in the field. Thus, contrary to expectation, the specialized feeding morphology of N. bredini corresponds to a broad diet of both hard-shelled and soft-bodied prey. Using multiple lines of study to describe the natural diets of other presumed specialists may demonstrate that specialized morphology often broadens rather than narrows diet breadth.

Isotopic incorporation rates and discrimination factors in mantis shrimp crustaceans.

Stable isotope analysis has provided insights into the trophic ecology of a wide diversity of animals. Knowledge about isotopic incorporation rates and isotopic discrimination between the consumer and its diet for different tissue types is essential for interpreting stable isotope data, but these parameters remain understudied in many animal taxa and particularly in aquatic invertebrates. We performed a 292-day diet shift experiment on 92 individuals of the predatory mantis shrimp, Neogonodactylus bredini, to quantify carbon and nitrogen incorporation rates and isotope discrimination factors in muscle and hemolymph tissues. Average isotopic discrimination factors between mantis shrimp muscle and the new diet were 3.0 ± 0.6 ‰ and 0.9 ± 0.3 ‰ for carbon and nitrogen, respectively, which is contrary to what is seen in many other animals (e.g. C and N discrimination is generally 0-1 ‰ and 3-4 ‰, respectively). Surprisingly, the average residence time of nitrogen in hemolymph (28.9 ± 8.3 days) was over 8 times longer than that of carbon (3.4 ± 1.4 days). In muscle, the average residence times of carbon and nitrogen were of the same magnitude (89.3 ± 44.4 and 72.8 ± 18.8 days, respectively). We compared the mantis shrimps' incorporation rates, along with rates from four other invertebrate taxa from the literature, to those predicted by an allometric equation relating carbon incorporation rate to body mass that was developed for teleost fishes and sharks. The rate of carbon incorporation into muscle was consistent with rates predicted by this equation. Our findings provide new insight into isotopic discrimination factors and incorporation rates in invertebrates with the former showing a different trend than what is commonly observed in other animals.