Thomas Claverie

MODULARITY AND SCALING IN FAST MOVEMENTS: POWER AMPLIFICATION IN MANTIS SHRIMP

Extremely fast animal actions are accomplished with mechanisms that reduce the duration of movement. This process is known as power amplification. Although many studies have examined the morphology and performance of power‐amplified systems, little is known about their development and evolution. Here, we examine scaling and modularity in the powerful predatory appendages of a mantis shrimp, Gonodactylaceus falcatus (Crustacea, Stomatopoda). We propose that power‐amplified systems can be divided into three units: an engine (e.g., muscle), an amplifier (e.g., spring), and a tool (e.g., hammer). We tested whether these units are developmentally independent using geometric morphometric techniques that quantitatively compare shapes. Additionally, we tested whether shape and several mechanical features are correlated with size and sex. We found that the morphological regions that represent the engine, amplifier, and tool belong to independent developmental modules. In both sexes, body size was positively correlated with the size of each region. Shape, however, changed allometrically with appendage size only in the amplifier (both sexes) and tool (males). These morphological changes were correlated with strike force and spring force (amplifier), but not spring stiffness (amplifier). Overall, the results indicate that each functional unit belongs to different developmental modules in a power‐amplified system, potentially allowing independent evolution of the engine, amplifier, and tool.

A morphospace for reef fishes: elongation is the dominant axis of body shape evolution.

Tropical reef fishes are widely regarded as being perhaps the most morphologically diverse vertebrate assemblage on earth, yet much remains to be discovered about the scope and patterns of this diversity. We created a morphospace of 2,939 species spanning 56 families of tropical Indo-Pacific reef fishes and established the primary axes of body shape variation, the phylogenetic consistency of these patterns, and whether dominant patterns of shape change can be accomplished by diverse underlying changes. Principal component analysis showed a major axis of shape variation that contrasts deep-bodied species with slender, elongate forms. Furthermore, using custom methods to compare the elongation vector (axis that maximizes elongation deformation) and the main vector of shape variation (first principal component) for each family in the morphospace, we showed that two thirds of the families diversify along an axis of body elongation. Finally, a comparative analysis using a principal coordinate analysis based on the angles among first principal component vectors of each family shape showed that families accomplish changes in elongation with a wide range of underlying modifications. Some groups such as Pomacentridae and Lethrinidae undergo decreases in body depth with proportional increases in all body regions, while other families show disproportionate changes in the length of the head (e.g., Labridae), the trunk or caudal region in all combinations (e.g., Pempheridae and Pinguipedidae). In conclusion, we found that evolutionary changes in body shape along an axis of elongation dominates diversification in reef fishes. Changes in shape on this axis are thought to have immediate implications for swimming performance, defense from gape limited predators, suction feeding performance and access to some highly specialized habitats. The morphological modifications that underlie changes in elongation are highly diverse, suggesting a role for a range of developmental processes and functional consequences.

Elastic energy storage in the mantis shrimp's fast predatory strike

SUMMARY Storage of elastic energy is key to increasing the power output of many biological systems. Mantis shrimp (Stomatopoda) must store considerable elastic energy prior to their rapid raptorial strikes; however, little is known about the dynamics and location of elastic energy storage structures in this system. We used computed tomography (CT) to visualize the mineralization patterns in Gonodactylaceus falcatus and high speed videography of Odontodactylus scyllarus to observe the dynamics of spring loading. Using a materials testing apparatus, we measured the force and work required to contract the elastic structures in G. falcatus. There was a positive linear correlation between contraction force and contraction distance; alternative model tests further supported the use of a linear model. Therefore, we modeled the system as a Hookean spring. The force required to fully compress the spring was positively correlated with body mass and appendage size, but the spring constant did not scale with body size, suggesting a possible role of muscle constraints in the scaling of this system. One hypothesized elastic storage structure, the saddle, only contributed approximately 11% of the total measured force, thus suggesting that primary site of elastic energy storage is in the mineralized ventral bars found in the merus segment of the raptorial appendages. Furthermore, the intact system exhibited 81% resilience and severing the saddle resulted in a non-significant reduction to 77% resilience. The remarkable shapes and mineralization patterns that characterize the mantis shrimps raptorial appendage further reveal a highly integrated mechanical power amplification system based on exoskeletal elastic energy storage.

MODULARITY AND RATES OF EVOLUTIONARY CHANGE IN A POWER-AMPLIFIED PREY CAPTURE SYSTEM

The dynamic interplay among structure, function, and phylogeny form a classic triad of influences on the patterns and processes of biological diversification. Although these dynamics are widely recognized as important, quantitative analyses of their interactions have infrequently been applied to biomechanical systems. Here we analyze these factors using a fundamental biomechanical mechanism: power amplification. Power‐amplified systems use springs and latches to generate extremely fast and powerful movements. This study focuses specifically on the power amplification mechanism in the fast raptorial appendages of mantis shrimp (Crustacea: Stomatopoda). Using geometric morphometric and phylogenetic comparative analyses, we measured evolutionary modularity and rates of morphological evolution of the raptorial appendages biomechanical components. We found that “smashers” (hammer‐shaped raptorial appendages) exhibit lower modularity and 10‐fold slower rates of morphological change when compared to non‐smashers (spear‐shaped or undifferentiated appendages). The morphological and biomechanical integration of this system at a macroevolutionary scale and the presence of variable rates of evolution reveal a balance between structural constraints, functional variation, and the “roles of development and genetics” in evolutionary diversification.

Reconstructing Greenland ice sheet runoff using coralline algae

The Greenland ice sheet (GrIS) contains the largest store of fresh water in the Northern Hemisphere, equivalent to ∼7.4 m of eustatic sea-level rise, but its impacts on current, past, and future sea level, ocean circulation, and European climate are poorly understood. Previous estimates of GrIS melt, from 26 yr of satellite observations and temperature-driven melt models over 48 yr, show increasing melt trends. There are, however, no runoff data of comparable duration with which to validate the relationship between the spatial extent of melting and runoff or temperature-based runoff models. Further, longer runoff records are needed to extend the melt pattern of Greenland to centennial timescales, enabling recent observations and trends to be put into a better historical context. We have developed a new GrIS runoff proxy by extracting information on relative salinity changes from annual growth bands of red coralline algae. We observed significant negative relationships between historic runoff, relative salinity, and marine summer temperature in Sondre Stromfjord, Greenland. We produce the first reconstruction of runoff from a section of the GrIS that discharges into Sondre Stromfjord over several decades (1939–2002) and record a trend of increasing reconstructed runoff since the mid 1980s. In situ summer marine temperatures followed an equivalent trend. We suggest that since A.D. 1939, atmospheric temperatures have been important in forcing runoff. These results show that our technique has significant potential to enhance understanding of runoff from large ice sheets as it will enable melt reconstruction over centennial to millennial timescales.

Gearing for speed slows the predatory strike of a mantis shrimp

SUMMARY The geometry of an animal’s skeleton governs the transmission of force to its appendages. Joints and rigid elements that create a relatively large output displacement per unit input displacement have been considered to be geared for speed, but the relationship between skeletal geometry and speed is largely untested. The present study explored this subject with experiments and mathematical modeling to evaluate how morphological differences in the raptorial appendage of a mantis shrimp (Gonodactylus smithii) affect the speed of its predatory strike. Based on morphological measurements and material testing, we computationally simulated the transmission of the stored elastic energy that powers a strike and the drag that resists this motion. After verifying the model’s predictions against measurements of strike impulse, we conducted a series of simulations that varied the linkage geometry, but were provided with a fixed amount of stored elastic energy. We found that a skeletal geometry that creates a large output displacement achieves a slower maximum speed of rotation than a low-displacement system. This is because a large displacement by the appendage causes a relatively large proportion of its elastic energy to be lost to the generation of drag. Therefore, the efficiency of transmission from elastic to kinetic energy mediates the relationship between the geometry and the speed of a skeleton. We propose that transmission efficiency plays a similar role in form–function relationships for skeletal systems in a diversity of animals.

LEVERS AND LINKAGES: MECHANICAL TRADE-OFFS IN A POWER-AMPLIFIED SYSTEM

Mechanical redundancy within a biomechanical system (e.g., many‐to‐one mapping) allows morphologically divergent organisms to maintain equivalent mechanical outputs. However, most organisms depend on the integration of more than one biomechanical system. Here, we test whether coupled mechanical systems follow a pattern of amplification (mechanical changes are congruent and evolve toward the same functional extreme) or independence (mechanisms evolve independently). We examined the correlated evolution and evolutionary pathways of the coupled four‐bar linkage and lever systems in mantis shrimp (Stomatopoda) ultrafast raptorial appendages. We examined models of character evolution in the framework of two divergent groups of stomatopods—“smashers” (hammer‐shaped appendages) and “spearers” (bladed appendages). Smashers tended to evolve toward force amplification, whereas spearers evolved toward displacement amplification. These findings show that coupled biomechanical systems can evolve synergistically, thereby resulting in functional amplification rather than mechanical redundancy.

Phylogenetic insights into the history and diversification of fishes on reefs

Studies of the phylogenetic history of fishes on reefs and the impact of reefs on fish diversification have, to date, been limited to relatively small clades. We take advantage of a recent multi-locus, time-calibrated phylogeny of acanthomorph fishes and a broad-scale morphological dataset of body shape in reef acanthomorphs to explore the history and diversification of fish on reefs at the family level. We find that no reef family exhibits exceptional species diversity for their stem age and some, such as Aulostomidae, Zanclidae, Menidae, and Triodontidae may in fact be species poor. The inferred history of reef colonization is highly dependent on how a reef family is defined; one classification scheme raises the possibility that most modern acanthomorph families originated on reefs. We find that most reef families occupy surprisingly distinct regions of morphospace and yet, some of the most diverse reef families occupy central and highly overlapping positions within the body shape morphospace. To the extent that proximity in morphospace reflects ecological similarity, these results imply that most reef fish families have diversified in adaptive zones away from other families. In contrast, a few of the most successful (e.g., Labridae and Pomacentridae) have achieved dominance while potentially facing stronger interactions with other lineages. Finally, we find no relationship between species diversity and body shape diversity. Assuming neither are diversity dependent, this result suggests that morphological and ecological diversification within families of reef fish may not be linked to the accumulation of species. Time-calibrated phylogenies provide the means for generating a greater understanding of the macroevolutionary processes influencing reef fish diversification, but we are currently limited by the lack of robust crown-group ages for many reef fish families.

Acoustic Ecology of the California Mantis Shrimp (Hemisquilla californiensis)

Acoustic communication plays a major role in the behavioral ecology of various marine organisms (Busnel 1963), especially marine mammals and fish. However, little attention has been given to acoustic communication in marine crustaceans (Popper et al. 2001). Furthermore, the interplay between anthropogenic noise and the acoustic ecology of marine crustaceans remains virtually unexplored. In this study, we investigated the acoustic environment of a benthic stomatopod crustacean, the California mantis shrimp (Hemisquilla californiensis, Crustacea, Stomatopoda).