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

Abstract

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.

Size, but not sex, predicts pinch force and exoskeleton mechanical properties in crayfish of the genus Faxonius

“…The exoskeleton of the claw was thicker, and consequently had greater compressive strength, than the exoskeleton of another body region, the carapace. We argue that studies of biomechanical performance in arthropods, and indeed of behavior more broadly, should include consideration of the mechanical properties of the exoskeleton (deVries et al, 2021).…”

Meta‐analysis suggests negative, but pCO2‐specific, effects of ocean acidification on the structural and functional properties of crustacean biomaterials

“…Crustaceans encompass a diverse and cosmopolitan group of organisms which are often considered to be less susceptible to ocean acidification than other taxonomic groups (Harvey et al, 2013 ; Kroker et al, 2010 ; Kroeker et al, 2013 ; Whitely, 2011 ). The success of crustaceans is largely attributed to their robust physiological regulation, in part driven by physical and chemical use of their calcified exoskeletons (deVries et al, 2021 ; Whiteley, 2011 ). Here, we present the results from a systematic review and meta‐analysis on the effects of elevated p CO 2 seawater on structural and functional properties of the crustacean exoskeleton.…”

“…Micron‐scale hardness testing typically scales with “whole‐shell” mechanical assessments (Currey & Brear, 1990 ), but cuticle thickness and geometry will also affect these responses. Previous changes in whole exoskeleton biomechanics of anatomical regions used for predation, feeding, or conflict, such as the highly mineralized decapod chelae (deVries et al, 2021 ; Fabritius et al, 2016 ; Luquet, 2012 ), pose direct ecological risks to crustaceans. Further mesocosm and field experiments are needed to determine whether crustaceans exposed to high p CO 2 seawater for set amounts of time experience different ecological outcomes based on their exoskeleton stability, such as in conflict resolution with other organisms (deVries et al, 2021 ).…”

“…Previous changes in whole exoskeleton biomechanics of anatomical regions used for predation, feeding, or conflict, such as the highly mineralized decapod chelae (deVries et al, 2021 ; Fabritius et al, 2016 ; Luquet, 2012 ), pose direct ecological risks to crustaceans. Further mesocosm and field experiments are needed to determine whether crustaceans exposed to high p CO 2 seawater for set amounts of time experience different ecological outcomes based on their exoskeleton stability, such as in conflict resolution with other organisms (deVries et al, 2021 ). Application of our results in these experiments is particularly crucial for management of wild‐caught crustacean species already vulnerable to population decline, such as economically important red king crabs and Tanner crabs (Armstrong et al, 1998 ; Seung et al, 2015 ).…”

“…The mineral‐bearing exoskeletons are a departure from the predominantly chitin‐ and protein‐enforced structures of terrestrial arthropods (Murdock, 2020 ). Instead, the calcified exoskeletons of crustaceans provide a line of defense from physical insults (deVries et al, 2021 ) and play a potential role in ionic regulation (Boßelmann et al, 2007 ). Indeed, Crustaceans are typically able to successfully osmoregulate within the variable physical and chemical conditions found in their marine and coastal environments (Baumann et al, 2014 ; Whiteley et al, 2018 ).…”