A Multi-Functional Armor: Carapaces’ Roles in Different Animals

Table of Contents

Abstract

The carapace is the dorsal section of the exoskeleton of many animals. This article discusses the multifunctionality of some animals’ carapaces. In the introduction, the necessity of the carapace and its potential hindrance is generally described. The body uses peer-reviewed research, experiments, and reviews to explain the structure and multifunctionality of the carapace in different animals. The uses of the carapace elaborated in this article are the turtle shell’s deformability, rigidity, and fracture resistance; the resistance to the weight of the beetle’s exoskeleton; the anti-erosion shell of scorpions; the overlapping structure and the thermoregulation of the armadillo’s carapace; and the stridulation/auditory feedback produced by both crab and lobster shells as a defensive technique and a communication method. In the discussion, the relationship between the carapace’s multifunctionality and energy efficiency is addressed, as well as some biomimetic applications of the carapaces. This paper concludes by reiterating the significance of the carapace and the benefits it creates for animals.

Introduction

A carapace, as defined by the Merriam-Webster dictionary (n.d.), is a “bony or chitinous case or shield covering the back or part of the back of an animal.” The word “shield” emphasizes one of the carapace’s main functions: protection. In fact, this structure can not only be used for protection, but also other functions. 

A carapace’s function will vary depending on the animal. The turtle’s carapace, for example, serves to protect itself against predators and against damage caused by falling or colliding with rocks in its environment (Achrai & Wagner, 2013). Similarly, the beetle’s carapace provides strong resistance to loading (Rivera et al., 2020). The scorpion’s carapace has a unique anti-erosion property against sand erosion from the environment it lives in (Zhang et al., 2020). The armadillo, on the other hand, takes advantage of this structure to protect itself from spiky vegetation and to decrease the probability of parasitic infections (Superina & Loughry, 2011). Lastly, crabs’ and lobsters’ carapaces serve as self-defense mechanisms, yet also play a significant role in communication by stridulation (Robinson et al., 1970). The multi-functional carapace is therefore an essential body part for many animals. 

However, this structure can come at a cost. For some, such as armadillos, having a carapace can impede on their metabolic rate and locomotion speed since they do not need to escape predators and thus do not need a rapid metabolism (Superina & Loughry, 2011). Additionally, carapaces can negatively impact the thermoregulation of armadillos because their ability to roll up into a ball affects their ability to store fat (Superina & Loughry, 2011).

Therefore, the physical analysis of carapaces emphasizes the importance of their various structures and functions and how they influence one another. 

Turtle Carapace Structure Overview – Ribs, Cortices, Interior, and Perisuture

A turtle’s carapace is an exoskeleton that protects the turtle from outside danger. The carapace is composed of around 50 plate-shaped ribs that are tightly connected to form a uniform, protective shell. Each rib has a sandwich-like structure: a hard, thin dorsal cortex on the top of the rib, a softer, thicker, more porous interior in the middle, and another hard, thin ventral cortex on the bottom, which directly touches the fragile organs of the turtle (Fig. 1). 

Fig. 1 (a) Ventral view of turtle’s carapace. The white arrow marks a piece of rib, while the yellow arrow marks the suture. (b) A section of the rib viewed horizontally. (c) A tomographic reconstruction of (b). The orientations (A-P: anterior–posterior; M-L: medial–lateral; D-V: dorsal–ventral) are marked (Achrai & Wagner, 2017).

The most amazing part of a turtle’s carapace is not only the fact that it is hard enough to protect the turtle from any violent external force such as a predator’s bite, but also that it can be deformable to weaker forces to allow the turtle’s essential living activities such as swimming, walking or even breathing. This property of the carapaces referred to as the interchangeability between the rigid and the deformable states, exists due to the perisuture. The perisuture is a complex of 3D zigzagging triangular bony tips that connects the adjacent ribs of the carapace (Fig. 2). These bony tips, composed of mineralized collagen fibers, interlock together to provide rigidity to the carapace. In between the opposite tips, there are unmineralized collagen fibers that ensure the deformability of the carapace. This section will discuss the following three questions: (1) How does the perisuture provide deformability to the turtle’s carapace? (2) Why does the perisuture enable the interchangeability of the carapace between its deformable state and its rigid state? (3) How does the soft keratin-collagen bilayer ensure the carapace’s resistance to fracture?

Fig. 2 Various microscopic features of the turtle carapace, including the interlocking suture, the cancellous interior, the ventral and dorsal cortices, and keratinous scutes and collagenous dermis (Achrai & Wagner, 2017).

A Deformable Carapace – Unmineralized Collagen Fibers

The carapace’s deformability is due to the perisuture connecting adjacent ribs. Turtles’ perisuture, just like their bone, is made of collagen fibers. However, the fibers composing the pointy triangular tips are mineralized, whereas the fibers connecting two opposite tips are unmineralized (Fig. 2). The main difference between the unmineralized and the mineralized collagen fibers is their deformability and hardness: Achrai and Wagner (2013) performed micro-mechanical measurements on the unmineralized collagen fibers and the mineralized collagen fibers. They discovered that the unmineralized collagen fibers are much more deformable than the mineralized fibers, since the unmineralized fibers have a mean elastic modulus E=1.6 ±0.9 GPa in dry conditions, whereas the mineralized fibers, represented by the dorsal cortex that shares the same material property, has a mean elastic modulus of E=16.6 ±2.2 GPa in dry conditions (Achrai & Wagner, 2013).

Elastic Modulus

The elastic modulus is the unit to measure the resistance of an object when being deformed elastically. An object with a higher elastic modulus is less deformable within its elastic range, whereas an object with a lower elastic modulus is floppier and stretches a lot when being pulled, (i.e., more deformable).In the case of turtles, unmineralized collagen fibers have lower elastic modulus, thus are more deformable due to their higher absorption of elastic potential energy when being pulled (Achrai & Wagner, 2017).Note that the elastic modulus is usually lower in wet conditions, due to the hydration that makes the organic structure floppier. Hence, it is important to compare different parts of the carapace (mineralized boney points and unmineralized collagen fibers) in the same humidity condition. In this section, only the data in dry conditions is used (Zhang et al., 2018). 

The geometric alignment of unmineralized and mineralized collagen fibers also contributes to the deformability of the carapace. Achrai and Wagner (2013) performed the SEM (scanning electron microscope) fractography on the red-eared slider turtle carapace and observed that in the perisuture between adjacent ribs, the mineralized boney fibers composing the triangular tips are roughly oriented along the A-P (anterior-posterior) direction, and the unmineralized collagen fibers are spanned across the gap between the opposite boney tips at an angle to the sinuous course of the gap (Fig. 3). The mineralized fibers and the unmineralized fibers can thus be said to be in approximately the same direction, which can enhance the carapace’s deformability (Achrai & Wagner, 2013).

This alignment of unmineralized and mineralized collagen fibers ensures the carapace deformability by maximally absorbing the potential energy upon compression on the turtle. When the carapace is compressed, the compression force on the carapace results in a bending force on the perisuture between the adjacent ribs (Achrai & Wagner, 2013).  This bending force is then translated to a tensile force through the A-P (anterior-posterior) axis, which pulls the two adjacent ribs apart. Since the mineralized pointy tips and the unmineralized collagen fibers are structured along the same A-P axis, the tension force is transmitted to the unmineralized fibers. As unmineralized collagen fibers are more deformable due to their lower elastic modulus, the tension force acting on the A-P axis is maximally absorbed by the unmineralized fibers in the same direction. Thus, the structure of the perisuture enhances the deformability of the carapace by the geometric alignment of the unmineralized and mineralized fibers. 

Fig. 3 (a) An SEM (scanning electron microscope) fractography of the carapace surface. The region bounded by the red box shows that mineralized boney fibers organized are roughly parallel to the A-P (anterior-posterior) axis. (b) The blue dashed line is the direction of the mineralized boney fibers, whereas the yellow line follows the unmineralized collagen fibers’ direction (Achrai & Wagner, 2013).

An Interchangeable Carapace – Unique Structure of Perisuture

The unique structure of turtles’ perisuture ensures the interchangeability of their carapace between the deformable and rigid state. Upon low-stress loading activities of the turtle (e.g., locomotion, swimming, respiration), the carapace exhibits deformability, whereas upon high-stress loading (e.g., predatory attacks, smashing against rocks), the carapace exhibits rigidity. This unique interchangeability can be shown experimentally by three-point bending tests and can also be proven mathematically by a geometric demonstration.

Krauss et al. (2009) showed turtle carapace’s interchangeability between deformability and rigidity by three-point bending tests. The researchers used two red-eared slider turtles (Chrysemys scripta elegans), each of them having a region where perisuture is present and another region where perisuture is absent to show the perisuture’s effect upon different forces. The results are shown by a load-displacement graph of both turtles under the three-point bending tests (Fig.4 (d)). It is clear that for all the samples, with or without perisuture, the displacement is in general proportional to the load, since the more load is put on the carapace, the more deformation it has. However, for the samples with perisuture, the first part of the curve is nearly flattened and then increases linearly, compared to the continuous linear increase of the curves for turtles without perisuture. This shows that for turtles with perisuture, if the load applied to the turtle’s shell is within a small range, the carapace will perform significant deformability (i.e., in its deformable state) because of the flattened load-displacement curve. If the load exceeds a certain threshold, the carapace will no longer have high deformability, but rather act similarly to a carapace without sutures (i.e., in its rigid state). This result from the three-point bending tests agrees with the phenomenon described before, which says that perisuture can provide deformability when receiving small compression but express rigidity when being compressed intensively. 

Fig. 4 (a) Simplified schematic of the perisuture, (b) The perisuture’s interlocking state upon compression, (c) A zoomed-in schematic of the two opposite tips, (d) The result from the three-point bending tests. The mathematically calculated central deflection of the beam (∆) is marked on the bottom (Krauss et al., 2009).

A mathematical model developed by the same researchers also proves the interchangeability of the carapace between its deformable state and rigid state (Krauss et al., 2009). 

The basic idea behind this model is that upon low compression, the unmineralized fibers express their deformability, however upon high compression, the unmineralized fibers can no longer be useful since the rigid boney pointy tips interlock with each other and provide rigidity to the carapace (Fig. 4(b)). 

The researchers defined the central deflection of the beam (∆) by the formula:

where T is the span of the bottom supports in the three-point bending tests, a constant that depends on the setting of the machine. The parameter α is the angle of deformation when the two adjacent ribs are bent (Fig. 4(b)). The central deflection of the beam (∆) represents the maximal deflection that the sutures can have in the deformable state before the two opposing mineralized tips interlock with each other in the rigid state. The relationship between the angles is shown by the following formula:

where 2θ is the angle of the pointy tip, and ∅ is the angle between the two edges of the opposite tips when they are in contact (Fig.4 (b)). D and L define the size of one pointy tip and is a geometric coefficient that facilitates the calculation. By trigonometry, the angles and ∅ can be represented in this way:

The constants D and L are measured directly from the turtles and they are D = 230 μm, L = 1400 μm, ε = 0.15 for Turtle 1, and D = 400 μm, L = 1000 μm, ε = 0.15 for Turtle 2. By plugging the constants, Equations (2), (3), and (4) into Equation (1), it is obtained that the central deflections of the beam (∆) are respectively ∆ ≈ 70 μm for Turtle 1 and ∆ ≈ 150 μm for Turtle 2. This means that the maximal deflection the suture can execute in the deformable state is 70 μm and 150 μm for Turtle 1 and Turtle 2. These two values calculated from the mathematical model are represented in (Fig. 4(d)), by the two arrows under the load-displacement curves. From the graph, the theoretical values coincide with the experimental data from the three-point bending tests, since the range at which the carapace with suture expresses deformability is also near the range of 70 μm to 150 μm. Thus, the mathematical model also proves the interchangeability of the carapace, and is also able to determine the theoretically exact value of central defection by calculation. 

Soft Keratin-Collagen Bilayer in the Turtle Carapace

The soft keratin-collagen bilayer (Fig. 5) plays an essential part in the turtle carapace’s resistance to fracture. In fact, when there are fractures that occur at the bone layer, it is most commonly due to a large amount of delaminations which are the separations of bone fragments into layers of the keratin-collagen and collagen-bone interface. Hence, it is rarely caused by the keratin-collagen bilayers fracturing. This strength is mainly a result of its bumper-buffer mechanism and the two materials’ property mismatch that results in fracture resistance (An et al., 2021).

Fig. 5 Structure of the soft keratin-collagen bilayer found in the skin of turtle carapaces (Adapted from Shelef & Bar-On, 2017).

As explored by Shelef & Bar-On (2017), the bumper-buffer mechanism allows the keratin-collagen bilayer to decrease the strain from the fractures on the bone layer. After a considerably strong force is applied to the carapace, there are plastic deformations on the bilayer. In fact, the keratin layer acts as a bumper as it can indent when it absorbs shock, while the collagen layer acts as a buffer between the bone layer and the keratin layer and therefore experiences compression. This mechanism results in helping restrict the damage from attaining the bone layer, thus keeping it within the keratin-collagen bilayer.

The mechanical property mismatch, specifically the difference in stiffness and in the overall stress levels between the keratin and collagen layers, serves to increase the toughness of the turtle carapace. According to the research done by An et al. (2021), the smaller the difference in stiffness between layers, the longer it will take for the bone layer to fracture. The crack growth in the bone layer is represented as a function of time (Fig. 6). The dependent variable, Δa/b, is the normalized crack extension where a is the length of the crack and b is the thickness of the bone layer. EC/EK represents the difference in stiffness. As it can be observed in the graph, the one with the most similar stiffness, EC/EK= 0.75, has the slowest crack growth. 

Fig. 6 Crack growth of the bone layer as a function of time for various stiffness differences between the keratin and collagen layer in the keratin-collagen bilayer of the turtle carapace (Adapted from An et al., 2021).

As for the stress difference between keratin and collagen, An et al. (2021) found that an intermediate contrast in stress is ideal to increase the toughness of the carapace. This is demonstrated in Fig. 7 where σ0c0k represents the stress difference. As observed in the graph, as σ0c0k increases, the size of the area affected by crack growth also increases. It is important to note that although an excess amount of delamination is harmful, this fracture phenomenon in the interfaces between the three layers of the carapace remains a crucial part of fracture resistance since it delays fracturing the bone layer. Thus, although a small σ0c0k results in a smaller area damaged, its plastic deformation also results in delaying delamination along the keratin-collagen interface, which in-turn decreases the fracture resistance. As for a large σ0c0k, this results in a larger area damaged. 

Fig. 7 Crack growth of the bone layer as a function of time for various stress differences between the keratin and collagen layer in the keratin-collagen bilayer of the turtle carapace (Adapted from An et al., 2021).

Therefore, the fracture resistance of the bone layer is influenced by stiffness and stress differences. Hence, it increases when the stiffness difference decreases and the stress difference reaches an intermediate amount of contrast between both layers. 

Beetle Carapace – Load Carrying Ability and Resistance

Beetles are popularly known for their stubborn and impressive resistance to being crushed. The beetle’s carapace significantly contributes to this phenomenon (Rivera et al., 2020). Studies have been performed on one beetle, in particular, the diabolical ironclad beetle who can withstand forces up to 36000 times its own body weight. Diabolical ironclad beetles are also flightless beetles (Rivera et al., 2020). Flying beetles have elytra. Elytra are the hardened forewings of the beetle exoskeleton which cover the beetles’ wings and move to allow the wings to move and fly (Rivera et al., 2020). Since diabolical beetles are flightless, they do not require mobile elytra and their elytra have fused at a medial joint with a small space underneath. The medial suture is sealed using ellipsoidal geometry like the seam between traditional puzzle pieces. These ellipsoidal ends that attach like puzzle pieces are called blades of the medial suture (Rivera et al., 2020). Studies have shown that as the number of blades increases, so does the amount of stress on each blade (Fig. 8). Therefore, the two-blade system has the highest toughness. When compressed, the diabolical beetle changes from 115N mm-1 to 291 N mm-1 at 0.64mm displacement (Rivera et al., 2020). Additionally, the beetle fractures at an average load of approximately 133 N and a maximum force was measured at 149 N (Rivera et al., 2020).

Fig. 8 (a) Comparison of sutures of different beetles with the diabolical ironclad beetle. (b) FE models of compression tests performed on sutures from (a). (c) Ellipsoidal blade geometry of the suture of the diabolical ironclad beetle. (d) Depiction of stress distribution on blades. (e) Graph showing the relationship between stress and number of blades (Rivera et al., 2020).

Influence of Scorpion’s Carapace on the Rate of Solid Particle Erosion

Solid particle erosion, caused by the transfer of kinetic energy from the collision of solid particles with material surfaces, results in the loss of mass. This therefore decreases the material’s life expectancy (Zhang et al., 2020). Various factors can influence this phenomenon, including the “size, shape, impact velocity and impact angle of the solid particles, hardness of the surface material and solid particles, and fracture toughness of the surface material” (Zhang et al., 2020). This leads many organisms in nature to evolve and have anti-erosion mechanisms in order to preserve the mass of their material surfaces. 

In fact, androctonus australis, commonly known as the desert scorpion, is an example of an animal that has a structure protecting it against solid particle erosion from its environment. Specifically, the desert scorpion’s cephalothorax, more precisely its carapace and mesosoma, has curves and bumps that reduce the erosion from the sand on its exterior surfaces (see Fig. 9) (Zhang et al., 2020).

Fig. 9 Dorsal view and structure of androctonus australis (Adapted from Salama & Sharshar, 2013 and Zhang et al., 2020).

The androctonus australis’ curved carapace decreases the erosion rate by modifying the impact angle of particles, which is the angle between the plane tangent to the surface where the collision occurs and the trajectory of the particle. When a particle impacts the surface of the carapace, the impact angle is most likely not equal to the angle of the particle’s initial trajectory (Zhang et al., 2020).  In fact, according to the model explored by Han et al. (2017), if one sets the maximizing impact angle at 30°, where the erosion rate is the most elevated, then particles colliding at a different impact angle results in minimizing the erosion rate. Hence, as seen in Fig. 10, α2 is set as the maximum impact angle. When a particle collides at an angle greater or smaller than α2 it helps decrease the erosion rate. The graph shows this as α1 representing an angle to the tangent line smaller than 30° and α3 representing an angle to the surface that is larger than 30° (Han et al., 2017). Therefore, the curvy structure of the carapace of androctonus australis allows the change of impact angles and therefore to protect the carapace against solid particle erosion. 

Fig. 10 A model of different impact angles from a particle’s trajectory when colliding with a curved surface (Adapted from Han et al., 2017).

The androctonus australis’ carapace also has bumps at the micrometer level. These bumps are formed by the increase of tissue cells that are fostered by the movement of sand in its environment (Zhang et al., 2020). Similar to the curvature, these bumps reduce the erosion rate by changing the impact angle of the collision particles. However, a part of the bump is not exposed to erosion. When the maximum impact angle is 30°, the bump is separated into three sections (Fig. 11). The red line on the figure represents the location of the maximum impact angle and S0 is the unaffected area. This results in decreasing the area exposed to erosion, and therefore a decrease in the erosion rate (Han et al., 2017).  In fact, according to Zhang et al. (2020), the area that is not exposed to impact particles increases when the maximum impact angle decreases. Hence, bumps on the carapace not only allow the change of impact angles, just like how a curved structure does but also lead to decreasing the erosion area which results in further protecting the scorpion.

Fig. 11 A model of different impact angles from a particle’s trajectory when colliding with a bump (Adapted from Han et al., 2017).

Although the studies found in this research have been principally for desert scorpions, this theory may be applied to other animals that have carapaces. Tortoises or armadillos, for example, have this curved carapace that serves as an anti-erosion mechanism, protecting them from their environment. 

The Mammalian Carapace: Armadillo 

Armadillos are characterized by their infamous armored carapace. The carapace is arguably the armadillo’s most defining feature considering that the name armadillo roughly translates to “little armored one” (Superina & Loughry, 2011). The armadillo carapace covers the dorsal and lateral areas of the body. It can be divided into five distinct structural components characterized by the areas of the body which they cover: the head, pectoral, vertebrae (banded), pelvic, and tail (Sedor et al., 2022). These five shields come together to form a virtually continuous mosaic (Fig. 12).

Fig. 12 Hierarchical structure of the armadillo carapace: (a) whole body; (b) triangular tiles; (c) hexagonal tiles with keratin; (d) osteoderm & Sharpey’s fibers (Adapted from Chen et al., 2011).

The armadillo carapace has a hierarchical complex structure (Sedor et al., 2022). A key structure is the osteoderm, common to many reptiles but unique to the mammalian armadillo (Sedor et al., 2022). Osteoderms are localized mineralizations inside the dermis and they are also known as dermal scutes. The osteoderms are connected by collagen fibers called Sharpey’s fibers (Chen et al., 2011). The body shells are the pectoral or forward shell, the banded shell and the pelvic or rear shell (Rhee et al., 2011). The band shell lies in between the forward and rear shell (Rhee et al., 2011). It has a complicated structure consisting of somewhat overlapping and connecting bands. This combination of overlap and connection points provides flexibility and protection. Additionally, the exterior surface of the shells is much denser with the interior being more sponge-like (Chen et al., 2011). This is similar to bone and the micromechanical test demonstrated considerable anisotropic behavior, like bone. Punch tests demonstrate that the tensile strength of the osteoderms (~20 MPa) was higher than that of Sharpey’s fibers (~16MPa). In both tensile and shear tests, the Sharpey’s fibers failed first (Fig. 13) (Chen et al., 2011).

Fig. 13 Results of a quasi-static compression test on armadillo shell specimens from the forward (a) and band (b) shells (Chen et al., 2011).

The Metabolic Cost of a Carapace

Considering how unique the mammalian carapace is to the armadillo, one can suggest that it had a key role in the evolution of armadillos and the entire group of Cingulata to which they belong (Superina & Loughry, 2011). The carapace has high thermal conductance (Vickaryous & Hall, 2006) and it covers the armadillo both dorsally and laterally (Rhee et al., 2011). Armadillos are known to have a high minimum conductance which may be partially attributed to their carapace. In fact, using a simple model of endothermy, armadillos have twice the expected thermal conductance for animals of that size. Armadillos have such a high minimum conductance that they can require 3 to 4 days to return to their regular temperature after exposure to cold (Vickaryous & Hall, 2006). Therefore, armadillos likely have thermoregulation methods to compensate for their carapaces and their own high thermal conductance.

Simple model of endothermy: this equation models the temperature differential maintained at the lower limit of thermoneutrality (Tl) as a function of basal rate VbO2 and minimal conductance (Cm) [N1] (Vickaryous & Hall, 2006). 

Burrowing is one of the armadillo’s thermoregulatory methods. Since armadillos are at risk of losing considerable amounts of energy to their environment, they rely on burrows in order to prevent heat loss (Superina & Loughry, 2011). Burrowing has its own consequences, one of which is the potential for overheating. This necessitates another thermoregulatory method, the armadillo’s low metabolic rate, to avoid overheating while in burrows (Vickaryous & Hall, 2006). The rigid carapace limits the armadillo from the common thermoregulatory method of fat stores (Superina & Loughry, 2011). Three-banded armadillos have been shown to be unable to add fat, likely because adding fat could prevent their defense mechanism of rolling up into a ball. Not only is the carapace thermally conductive, but it prevents the armadillos from growing thermally insulating fur. This is another reason why armadillos have high thermal conductance and are restricted to living in rather warm environments (Superina & Loughry, 2011). Additionally, reconsider the burrowing behavior of armadillos: the burrow is an environment with hypoxic conditions. Having a restrictive carapace covering the body both dorsally and laterally is restrictive and especially restrictive to the thorax. The common animal response to hypoxia is to take deep breaths; however due to their rigid carapace, in low oxygen environments, armadillos are forced to take many rapid and shallow breaths.

Communication via Crustacean Carapaces

Throughout history, organisms have adopted a vast variety of defense mechanisms to evade predators and increase their chances of survival. Often, large animals rely on their sensory organs, strength and brute force to challenge predators head-on, whereas smaller animals and invertebrates rely on guileful techniques and trickery, such as camouflage and echolocation. Despite its rarity, stridulation, which refers to the production of sound by rubbing bodily structures, has proved to be an effective defense mechanism for arthropods and, more specifically, decapods.

Stridulation

In spite of the limited research available on this topic, Robinson et al., (1970) provide evidence that crustaceans utilize auditory systems and receptors as a form of sonar communication to identify any potential mates or threats lurking nearby. Another study, focusing primarily on two species of crabs originating from Panama, was conducted to determine the nature of the sound produced during predatory attacks. It was observed that G. quadratus crabs rub the merus (region between first and second joint) of their chelipeds (limb containing the large claw) (Fig. 14) against their carapace to produce scratchy sounds, up to 16 Hz in frequency (Abele et al., 1973). This technique has been commonly adopted by other species of decapods, with minor variations in the types of ambulatory limbs involved.

Although hermit crabs do not have a carapace, and instead occupy vacant shells, they also exhibit stridulations by rubbing their appendages with each other and the shell (https://youtu.be/R2BduMQkiXY**).

Fig 14. Dorsal (A) and ventral (B) views of crab, detailing anatomy and structure. General terminology for body parts and carapace regions of crab (shown on Nectocarcinus integrifrons, Portunidae) (Adapted from Hale, 1927).

When stationary, the crab’s chelipeds appear retracted and held close to the anterior surface of the carapace. However, when faced with imminent threat, the crab’s senses are heightened and thus the crab assumes an elevated position, with chelipeds raised above their body, as a form of territorial display (meral spread) (Abele et al., 1973). As the chelipeds are closer to the subhepatic carapace when the crab is in its active stance, they are more likely to rub together. Together, these rapid movements contribute to the production of sound to intimidate and fend off predators.

Relationship Between Sound Propagation and Acoustic Attenuation

The degree of sound propagation is often influenced by the mode of vibration of the emitting source. There are two types of sources: monopole (pulsating sphere undergoing changes in volume) and dipole (vibrating sphere). This serves as a useful model for studying the sound-producing structures present in crustaceans as they exhibit both modes. According to Euler’s equations, the intensity of a sound can be calculated if certain parameters (mode of vibration, source size, frequency, etc.) are known. To determine the attenuation of sound, the study investigated the acoustic parameters of an American lobster and used the data to construct monopole and dipole equations (Fig. 15). Since the carapace cannot vary in volume, crustaceans typically behave as dipoles, producing sound by vibration, which can be felt easily when grasping the carapace.

Fig. 15 Diagrams representing flow fields (left) and attenuation of sound pressure and flow velocity with increasing distance from (a) (acoustic monopole) and (b) (acoustic dipole). Calculated using sound emission data of American lobster (Adapted from Breithaupt & Tautz, 1990).

In the case of lobsters, the sound is not produced from appendage stridulation, but rather from vibrations. European lobsters (Homarus Gammarus) use both chemical and mechanical defenses during combat and for communication. Jezequel et al. (2020) carried out an experimental study to detect vibrations in the carapace. The mechanisms involved in the production of these sounds were previously undocumented, with few sources acknowledging the acoustic behavior of crustaceans. The lobsters were placed in a behavioral tank equipped with hydrophones which contain piezoelectric crystals that generate electrical pulses when subjected to a change in pressure. As hydrophones match the acoustic impedance of water, they can pick up a vast range of frequencies and auditory feedback from sound waves. By coupling them with accelerometers, researchers were able to detect and record both sounds and vibrations. However, due to the high attenuation (reduction in amplitude) of sound waves in tanks, the data acquired was insufficient to draw comparisons. Nevertheless, there was an observed correlation between the size of the carapace and the frequency of vibrations (Jezequel et al., 2020). Contrary to G. quadratus, the Homarus americanus and Homarus gammarus rapidly contract the antagonistic internal muscles (remoter/promoter) beneath their antennae to produce vibrations, as opposed to the friction between merus and carapace (Henninger & Watson, 2005).

Another soniferous species, known for its agonistic behavior, is the spiny lobster, Panulirus interruptus. Surveillance of these creatures suggests that they produce raspy sounds as an ‘aposematic signal’ (Staaterman et al., 2010). These fricative sounds emanate from the base of their antennae, as their plectrum skids along the file of the carapace (Fig. 16). Although research suggests that stridulations do not influence intraspecific interactions and behavior, certain studies conclude that crustaceans’ responses to predator-prey interactions stem from the ability to detect and produce sounds using mechanoreceptors and their carapace. This mechanism was investigated using three-axial accelerometers, attached to the carapace, to detect auditory impulses and determine the nature of acoustic data (frequency, pressure, attenuation) (Zenone et al., 2019). It was noted that spiny lobsters employ three defense mechanisms, sound production, caridoid escape (tail-flip) and walking, all of which involve both vibrating carapaces and ambulatory legs, when encountering predators, in this case, Octopus briareus. Another study of the same species was used to analyze trends between carapace and antennular plate size to the degree of vibrations (Patek & Oakley, 2003). The results obtained were favorable and supported the researchers’ hypotheses.

Documentation of these experiments and observations have proved that carapace is essential for the survival of decapods. Even as crustaceans molt (a process of shedding their hardened calcified exoskeleton), these organisms can continue to stridulate even in a soft, unprotected and exposed state. Although the exact science behind this mechanism is unknown, primarily because studies of this nature have been largely undocumented, spiny lobsters, and their close-related counterparts, can continue to produce raspy sounds in moments of vulnerability and threaten any predators.

Fig. 16 Structures involved in the production of raspy, screeching sounds (Image courtesy of Natural History Magazine/Sally Bensusen).

Discussion

The multifunctionality of carapaces is a good example of the energy efficiency designed by nature. In all canalyzedis the animal’s protection for its fragile organs against external forces. At the same time, instead of evolving other body parts for some functions, the carapace’s multifunctionality ensures these functions and thus saves energy. In the case of the turtle, the interchangeability between the deformable state and the rigid state avoids any extra organs that facilitate the turtle’s locomotion, for example, an extra soft layer between the shell and the organs. In the case of the armadillo, the carapace’s high thermal conductance prevents the armadillo from overheating while in burrows. This avoids the evolution of other energy-costly thermoregulatory body parts. For example, armadillos possess only a few sweat glands. As in the case of the crabs and lobsters, the stridulation of their carapace replaces the sound production organs and thus saves energy. 

The carapace’s multifunctionality has inspired many biomimetic designs in materials and architecture.

The synthetic composite foam materials are inspired by the turtle’s carapace to ensure their resistance and capacity for energy absorption. Due to its sheer mechanical strength and ability to withstand high stress, the interlocking ridges and layers of the turtle carapace have served as a blueprint to design bio-inspired synthetic composites (Rhee et al., 2009). Further investigation into the structure and composition of the turtle carapace revealed the presence of bony fibers that provide multi-directional bending strength and micro-crack propagation, a process by which elastic strain energy, exerted by an applied load, is dissipated. In addition, the overall hexagonal layout of the scutes of the carapace allows for an increased surface area with a minimal number of scutes. By tessellating perfectly, the hexagonal plates maintain the uniform distribution of applied forces under compression and provide resistance. As the carapace has an increased energy absorption ability, scientists have considered designing composite foam materials using these properties as templates (Rhee et al., 2009).

As for the anti-erosion materials, Han et al. (2015) developed a bionic anti-erosion functional surface inspired by scorpions’ carapace. The surface has similar bumps, groove-shapes, and curvature of scorpions’ armor which help decrease the erosion rate of this new biomimetic material. The same material is also inspired by the turtle’s keratin-collagen bilayer, as it has a series of separable movable hard layers that lay on top of a soft layer, ensuring the resistance of this material upon impact (Han et al., 2015).

The armadillo carapace may inspire many designs due to its multifunctionality. Perhaps the most obvious application would be the armor inspired by the armadillo’s own armor, the carapace. The chain mail armor in the Xi Xia dynasty of Ancient China is an example of an early-age bioinspired design. As for architecture, former architects based in Singapore have been inspired by the armadillo for a function beyond mechanical defense. They designed a house called the armadillo house, whose exterior walls are inspired by the overlapping layers of the armadillo carapace. The purpose of the overlap is to block out noise pollution as the house is located near a noisy highway (Designboom, 2012).  

Conclusion

The carapace is clearly a significant biological structure with an incredible impact on the animals who have it. Despite the differences between reptiles, arthropods, and mammals, all three have evolved species with a carapace. The carapace offers physical protection and serves as a defense mechanism. Despite these clear defensive benefits, the carapace’s role appears to have expanded beyond purely being a defensive shield as the carapace has a multitude of functions. These functions include: the combination of deformability and rigidity allowing locomotion and protection in turtles (Achrai & Wagner, 2017); the high endurance to loading in beetles (Rivera et al., 2020); the protection from environmental particle erosion in scorpions (Zhang et al., 2020); the thermoregulatory and hypoxic responses in armadillos (Superina & Loughry, 2011); and the stridulation to communicate and to defend against predators in lobsters (Robinson et al., 1970). This impressive multifunctionality of the well-engineered carapace may inspire future designs requiring toughness, deformability, load resistance, thermoregulation as well as other functions. The evolution and survival of these animals with carapaces seem to encourage a consensus that the multifunctionality of the carapace is well worth its costs. 

References

Abele, L. G., Robinson, M. H., & Robinson, B. (1973). Observations on sound production by two species of crabs from Panama (decapoda, gecarcinidae and pseudothelphusidae). Crustaceana, 25(2), 147–152. https://doi.org/10.1163/156854073X00795

Achrai, B., & Wagner, H. D. (2013, April). Micro-structure and mechanical properties of the turtle carapace as a biological composite shield. Acta Biomaterialia, 9(4), 5890–5902. https://doi.org/10.1016/j.actbio.2012.12.023

Achrai, B., & Wagner, H. D. (2017, September). The turtle carapace as an optimized multi-scale biological composite armor – A review. Journal of the Mechanical Behavior of Biomedical Materials, 73, 50–67. https://doi.org/10.1016/j.jmbbm.2017.02.027

An, B., Sun, W., & Zhang, D. (2021). Role of soft bi-layer coating on the protection of Turtle Carapace. Journal of Biomechanics, 126, 110618. https://doi.org/10.1016/j.jbiomech.2021.110618 

Breithaupt, T., Tautz Jürgen, & Wiese, K. (1990). In The sensitivity of crayfish mechanoreceptors to hydrodynamic and acoustic stimuli (pp. 114–120). essay. https://doi.org/10.1007/978-3-0348-5689-8_12

Chen, I. H., Kiang, J. H., Correa, V., Lopez, M. I., Chen, P.-Y., McKittrick, J., & Meyers, M. A. (2011). Armadillo armor: Mechanical testing and micro-structural evaluation. Journal of the Mechanical Behavior of Biomedical Materials, 4(5), 713–722. https://doi.org/10.1016/j.jmbbm.2010.12.013

Designboom. (2012). Formwerkz architects: Armadillo House. designboom. Retrieved October 25, 2022. https://www.designboom.com/architecture/formwerkz-architects-armadillo-house/

Han, Z., Feng, H., Yin, W., Niu, S., Zhang, J., & Chen, D. (2015). An efficient bionic anti-erosion functional surface inspired by desert scorpion carapace. Tribology Transactions, 58(2), 357–364. https://doi.org/10.1080/10402004.2014.971996

Han, Z., Zhu, B., Yang, M., Niu, S., Song, H., & Zhang, J. (2017). The effect of the micro-structures on the scorpion surface for improving the anti-erosion performance. Surface and Coatings Technology, 313, 143–150. https://doi.org/10.1016/j.surfcoat.2017.01.061  

Henninger, H. P., & Watson, W. H. (2005). Mechanisms underlying the production of carapace vibrations and associated waterborne sounds in the American lobster, homarus americanus. The Journal of Experimental Biology, 208(Pt 17), 3421–9. https://doi.org/10.1242/jeb.01771

Jezequel, Y., Coston-Guarini, J., Chauvaud, L., & Bonnel, J. (2020). Acoustic behaviour of male European lobsters (Homarus gammarus) during agonistic encounters. Journal of Experimental Biology, 223(4). https://doi.org/10.1242/jeb.211276

Krauss, S., Monsonego-Ornan, E., Zelzer, E., Fratzl, P., & Shahar, R. (2009, January 26). Mechanical Function of a Complex Three-Dimensional Suture Joining the Bony Elements in the Shell of the Red-Eared Slider Turtle. Advanced Materials, 21(4), 407–412. https://doi.org/10.1002/adma.200801256

Merriam-Webster. (n.d.). Carapace definition & meaning. Merriam-Webster. Retrieved October 3, 2022, from https://www.merriam-webster.com/dictionary/carapace

Patek, S. N., & Oakley, T. H. (2003). Comparative tests of evolutionary trade-offs in a palinurid lobster acoustic system. Evolution, 57(9), 2082–2100. https://doi.org/10.1554/02-608

Rhee, H., Horstemeyer, M. F., Hwang, Y., Lim, H., El Kadiri, H., & Trim, W. (2009). A study on the structure and mechanical behavior of the terrapene carolina carapace: a pathway to design bio-inspired synthetic composites. Materials Science & Engineering C, 29(8), 2333–2339. https://doi.org/10.1016/j.msec.2009.06.002

Rhee, H., Horstemeyer, M. F., & Ramsay, A. (2011). A study on the structure and mechanical behavior of the Dasypus Novemcinctus Shell. Materials Science and Engineering: C, 31(2), 363–369. https://doi.org/10.1016/j.msec.2010.10.012

Rivera, J., Hosseini, M. S., Restrepo, D., Murata, S., Vasile, D., Parkinson, D. Y., Barnard, H. S., Arakaki, A., Zavattieri, P., & Kisailus, D. (2020). Toughening mechanisms of the elytra of the diabolical ironclad beetle. Nature, 586(7830), 543–548. https://doi.org/10.1038/s41586-020-2813-8

Robinson, M. H., Abele, L. G., & Robinson, B. (1970). Attack autotomy: a defense against predators. Science, 169(3942), 300–301. https://doi.org/10.1126/science.169.3942.300

Salama, W. M., & Sharshar, K. M. (2013). Surveillance study on scorpion species in Egypt and comparison of their crude venom protein profiles. The Journal of Basic & Applied Zoology, 66(2), 76–86. https://doi.org/10.1016/j.jobaz.2013.10.003  

Sedor, F. A., Klimeck, T. D. F., Dias, E. V., Oliveira, E. V., Ciancio, M. R., Vieira, K. T. P., Fernandes, L. A., & Angulo, R. J. (2022). The eocene armadillo utaetus buccatus (Euphractinae) in the Guabirotuba Formation (curitiba basin) and carapace morphological implications. Journal of South American Earth Sciences, 114, 103694. https://doi.org/10.1016/j.jsames.2021.103694

Shelef, Y., & Bar-On, B. (2017). Surface protection in bio-shields via a functional soft skin layer: Lessons from the Turtle Shell. Journal of the Mechanical Behavior of Biomedical Materials, 73, 68–75. https://doi.org/10.1016/j.jmbbm.2017.01.019  

Staaterman, E. R., Claverie, T., & Patek, S. N. (2010). Disentangling defense: the function of spiny lobster sounds. Behavior, 147(2), 235–258. https://doi.org/10.1163/000579509X12523919243428

Superina, M., & Loughry, W. J. (2011). Life on the half-shell: Consequences of a carapace in the evolution of armadillos (Xenarthra: Cingulata). Journal of Mammalian Evolution, 19(3), 217–224. https://doi.org/10.1007/s10914-011-9166-x

Vickaryous, M. K., & Hall, B. K. (2006). Osteoderm morphology and development in the nine-banded armadillo, dasypus novemcinctus (mammalia, Xenarthra, cingulata). Journal of Morphology, 267(11), 1273–1283. https://doi.org/10.1002/jmor.10475

Zenone, A., Ceraulo, M., Ciancio, J. E., Buscaino, G., D’Anna, G., Grammauta, R., Mazzola, S., & Giacalone, V. M. (2019). The use of 3-axial accelerometers to evaluate sound production in european spiny lobster, palinurus elephas. Ecological Indicators, 102, 519–527. https://doi.org/10.1016/j.ecolind.2019.02.064

Zhang, S., Zhang, J., Zhu, B., Niu, S., Han, Z., & Ren, L. (2020). Progress in bio-inspired anti-solid particle erosion materials: Learning from nature but going beyond nature. Chinese Journal of Mechanical Engineering, 33(1). https://doi.org/10.1186/s10033-020-00458-y  

Zhang, X., Cai, Z. B., Li, W., & Zhu, M. H. (2018, February). Understanding hydration effects on mechanical and impacting properties of turtle shell. Journal of the Mechanical Behavior of Biomedical Materials, 78, 116–123. https://doi.org/10.1016/j.jmbbm.2017.11.007