Morphological and structural characteristics of the elytra reduce impact damage to ladybird beetles

For millions of years, both environmental pressures and predator-prey relationships have led animals to develop smart structures that are remarkably mechanically robust (Rivera et al., 2020). For instance, the tapered spiral horn of bighorn sheep (Ovis canadensis) reduces ramming injuries by 125% during intraspecific fighting when compared with horns of different shapes (Geist, 1971, Alexander et al., 1977, Wheatley et al., 2023). Analogously to vertebrates, such functional structures also play an important role in the survival of invertebrates (Zhang et al., 2021b, Wang et al., 2022). In a classical example, mantis shrimp (Odontodactylus scyllarus) depend on their shells to endure numerous high-velocity strikes that are delivered by their prey (Patek et al., 2004, Weaver et al., 2012, Ling et al., 2018). The substantial impact forces that are endured by this biological structure, coupled with their ability to withstand them without catastrophic failure, indicate that they have undergone adaptations to handle excessive impact stresses.

Beetles are one of the most diverse insect orders with about 350 thousand species, and they have modified their forewings into hardened elytra (Hunt et al., 2007, Sun et al., 2018, Phan and Park, 2020). The sturdy elytra in some terrestrial species, such as Allomyrina dichotomus, Lethrus apterus, and Athous haemorrhoidalis, can effectively shield their fragile hindwings and abdominal spiracles within the sub-elytral space (Frantsevich et al., 2005, Dai et al., 2008, Dai and Yang, 2010, He et al., 2015). Recently, the protective properties of elytra have been attributed to the mechanical interactions between the internal layers and their sublayers and the distinct arrangements of the polysaccharide-protein fibers within each sublayer (Van de Kamp et al., 2016, Li et al., 2020, Goczał and Beutel, 2023). Moreover, previous studies have also revealed a honeycomb-trabecular structure in the elytra. The combination of hollow cylindrical columns and thin-walled structures serves an essential role in preventing fatal damage (Chen et al., 2015, Xiang et al., 2017, Hao and Du, 2018, Song et al., 2021). These specialized features enable beetles to access various ecological niches, such as soil, bark, wood, and water, resulting in a wide range of habitats and promoting significant adaptive radiation (Frantsevich et al., 2005).

Compared to the above beetles, seven-spot ladybird beetles (Coccinella septempunctata) living in clusters of vegetation may encounter additional challenges in avoiding damage due to their physiological characteristics and behaviors (Zhang et al., 2021a). When threatened by predators such as amphibians and reptiles, ladybird beetles usually employ self-protection attempts, namely death-feigning, to avoid being attacked (Evans, 2023, Hodek et al., 2012). Ladybird beetles exhibiting this behavior are more vulnerable to being affected by external factors because of their lightweight body mass (∼30.00 mg), which is more likely to result in them falling from the clusters of vegetation (Pettersson et al., 2005). Remarkably, the maximum height of the vegetation is about 0.50 m, which is an astounding 100 times the body length of a ladybird beetle. This is equivalent to a human falling from a height of 180 m. Thus, a fall poses a significant threat of damage to the hindwings of ladybird beetles. However, ladybird beetles do not suffer from damage after falling from such a height. Currently, the underlying mechanism that protects them from damage when they fall remains unexplored.

To understand this mechanism, we conducted a combined experimental, theoretical, and numerical investigation. In this study, the intentional falls of the ladybird beetles onto the ground were recorded with two high-speed cameras. We discovered that the falling ladybird beetles were more likely to hit the ground with the costal edge of their elytra with an occurrence rate of 59.52%. Next, a mathematical model was built to determine why the ladybird beetles tended to land on the ground with their elytra edge, and further elucidate the advantage of the biological morphology. Subsequently, scanning electron microscopy (SEM) and micro-computed tomography (micro-CT) were used to observe the hollow structure of the elytra edge. The numerical results revealed that the hollow structures of the elytra edge facilitated the absorption of residual impact energy during landing. This study enhances the understanding of the functions resulting from the morphology and microstructure of ladybird elytra, and could be used to inspire the development of next-generation energy-absorption technology.

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