Insect wing damage: causes, consequences and compensatory mechanisms

Insects are the most diverse animal taxon on Earth, in terms of both the number of species and the number of individuals (Misof et al., 2014). The number of described insect species exceeds 1 million (May, 1988), which is greater than the total number of recorded species of all other taxa combined (Mora et al., 2011); the total number of insects is estimated to be as high as 1 million trillion (Wilson, 2002). The success of insects, compared with other taxa, has been attributed to a number of characteristics including their small size (Grebennikov, 2008), robust exoskeleton (Kennedy, 1927), enormous reproductive potential (Ritcher, 1976), strong adaptability (Tipton, 1976), diverse defensive strategies (Stevens, 2013), metamorphosis (Johnston and Rolff, 2015) and flight, which provides them with an efficient form of locomotion. Among all these, however, the last seems to play the most vital role (Daly et al., 1978) – insects became markedly successful only after they obtained the ability to fly (Wagner and Liebherr, 1992).

The term ‘flight’ has been used in the literature to describe a wide range of aerial behaviours, such as the passive windborne dispersal of thrips and aphids (Sorensen, 2009), free-falling of wood ants (Haemig, 1997), aerial descent of canopy ants (Yanoviak et al., 2005) and parachuting of Lepidoptera larvae (Yamazaki, 2010). However, neither of these behaviours is as sophisticated as the flapping flight demonstrated by flies, bees, dragonflies and butterflies, among others. Flapping flight, which is the focus of this Commentary, is an active muscle-powered form of flight. It is characterized by complex, unsteady aerodynamic effects, which enable insects to generate lift that is much higher than that expected by conventional steady-state aerodynamics (Srygley and Thomas, 2002). Among all invertebrates, insects are the only group that are capable of flapping flight (Pradhan, 1969). This ability has given them obvious advantages in terms of foraging, mating, dispersal and escaping predators, compared with other, flightless species.

The act of flight in insects is achieved through outgrowths of the thoracic exoskeleton, known as wings. Wings are complicated structures (Wootton and Newman, 2008; Young et al., 2009) and consist of components that are both compositionally and structurally very complex (Wootton, 1981, 1992; Gorb, 1999; Fig. 1). The structural components, such as veins and membrane, provide insect wings with full functionality and distinguish them from typical aerofoils. In contrast to the wings of bats and birds, insect wings do not contain flight muscles. Hence, in insects, wing deformability, including the ability to twist and form a cambered shape during flight, is passively controlled by the structural components (Ennos, 1988, 1995; Wootton, 1993; Rajabi et al., 2016a). The deformations determine the capacity of the wings to produce aerodynamic lift (Young et al., 2009; Mountcastle and Combes, 2013). The level of ‘passive shape control’ achieved by the wing components is the characteristic that makes insect wings unique among both natural and engineered systems (Wootton, 1999; Smith et al., 2000).

The biomechanics of insect wings have been subjected to much scrutiny in the last three to four decades. Researchers have utilized a variety of methods, including imaging techniques (Newman, 1982; Gorb et al., 2009; Appel et al., 2015; Rajabi et al., 2018), high-speed filming (Rüppell, 1989; Ellington et al., 1996), mechanical testing (Ennos, 1988; Wootton, 1993; Smith et al., 2000; Combes and Daniel, 2003a,b; Dirks and Taylor, 2012), numerical simulation (Kesel et al., 1998; Jongerius and Lentink, 2010; Rajabi et al., 2011) and theoretical modelling (Sunada et al., 1998) to establish a link between the structural design of insect wings and their functionality. These studies have shed light on how single wing components, such as veins (Fig. 1A,B; Combes and Daniel, 2003b; Appel et al., 2015; Rajabi et al., 2016b), membranes (Fig. 1C; Wootton et al., 2000; Rajabi et al., 2016c), microjoints (see Glossary; Fig. 1D–G; Donoughe et al., 2011; Rajabi et al., 2015a, 2016d), nodi (see Glossary; Fig. 1H; Newman, 1982; Fauziyah et al., 2014; Rajabi et al., 2017a, 2018), spikes (Fig. 1I,J; D'Andrea and Carfi, 1988, 1989), patches of the protein resilin (see Glossary; Fig. 1K; Gorb et al., 2009; Rajabi et al., 2016e) and flexion lines (Wootton, 1981; Wootton et al., 2003) influence the response of the wing to aerodynamic forces that it produces when used in flight (Box 1). However, how these components interact with each other is still unknown.

Insect wings not only have to withstand aerodynamic forces during flight but they also experience frequent mechanical stresses due to accidental collisions (Higginson and Gilbert, 2004; Foster and Cartar, 2011). The risk of collisions is especially high during foraging (Toth et al., 2009), mating (Ragland and Sohal, 1973), inter- and intra-sexual fights (Alcock, 1996; Rüppell and Hilfert-Rüppell, 2013), predatory attacks (Shapiro, 1974; Robbins, 1981) and egg laying (e.g. in female dragonflies; H.R., personal observations). According to Wootton (1992) and Rueppell et al. (2005), wings collide with objects in the environment and the wings and bodies of conspecifics. Collision with vegetation, however, is one of the most frequently reported sources of unexpected stresses on insect wings (Newman and Wootton, 1986; Wootton, 1992; Higginson and Gilbert, 2004; Foster and Cartar, 2011).

Considering the challenges associated with capturing wing collisions in natural settings, there is at present only one study in the literature that has quantified the frequency of such collisions in flying insects (Foster and Cartar, 2011). Based on this study, in foraging bumble bees, the frequency of wing collisions with vegetation varies between 50 and 96 times per minute across different species. This indicates a very high frequency of wing collisions ̶ roughly once per second. Given a lifespan of 36 days (Roman and Szczesna, 2008) and 3 h flight time every day (Foster and Cartar, 2011), the number of such physical interactions between wings and vegetation can reach ∼400,000 over the lifespan of a foraging bumble bee.

In this Commentary, we consider data from the literature in order to understand (i) the effects of frequent accidental collisions on the structural integrity of insect wings, (ii) how insects compensate for the damage caused by collisions and (iii) the design strategies that could prevent wing damage or slow down its progression. We further discuss our findings in an evolutionary context and outline future research directions.

The mechanical stress exerted on insect wings during collisions can result in irreversible wing damage (Foster and Cartar, 2011). Collision stress is, in fact, the most likely source of damage in insect wings (other sources of damage include stresses induced during regular flight, frictional stresses applied to the wing surface by the air and stresses associated with flight initiation and cessation; Foster and Cartar, 2011). Based on our own observations and previous reports (Hedenström et al., 2001; Burkhard et al., 2002; Foster and Cartar, 2011; Rajabi et al., 2017b; Rudolf et al., 2019), the most frequent types of damage in insect wings seem to be: (i) wear, i.e. removal of material from the wing surface without a reduction in surface area (Fig. 2A), (ii) cracking, i.e. damage/cracks with no loss of wing area (Fig. 2B,D) and (iii) fracture, i.e. cracking that has led to area loss (Fig. 2C). Among these modes of material failure, wear and cracking are likely to have only a minor influence on the wing aerodynamics. This is because they do not reduce the wing area and are likely to influence the flow of air over the wing only locally, rather than altering its global pattern. In contrast, fracture is the only mode of failure that directly affects the wing surface area. Hence, it is likely to have the greatest impact on aerodynamic performance.

Recent studies measured the frequency of wing area loss as a result of wing fracture in Sympetrum vulgatum and Sympetrum striolatum dragonflies (Rajabi et al., 2017b; Rudolf et al., 2019). According to the results, although ∼75% of the examined wings contained cracks and fractures, in the majority of cases damage resulted in the loss of far less than 5% of the whole wing area. This finding indicates that insect wings are highly resistant to damage. Wing material is mostly lost from the tip and trailing margin of the wings, suggesting that these regions may be less damage resistant than other wing regions. This was interpreted to be due to the presence of fewer flexible microjoints in the wing tip and trailing edge, which can increase the local stress concentration in collisions (see below).

Previous studies have attempted to assess the influence of wing damage on insect flight (see Box 2 for a comparison between insects, birds and bats). To this end, both field observations and laboratory experiments have been used to track changes in flight performance in response to manually induced wing fractures. In general, fractures decrease the manoeuvrability of insects (Jantzen and Eisner, 2008; Combes et al., 2010; Foster and Cartar, 2011; Mountcastle et al., 2016), reduce both their reproductive (Vance and Roberts, 2014) and predatory success (Combes et al., 2010), and increase the risk of predation (Rodd et al., 1980; Jantzen and Eisner, 2008; Vance and Roberts, 2014). Fractures are also thought to increase mortality rate in both honey bees (Rueppell et al., 2005; Dukas and Dukas, 2011) and tsetse flies (Allsopp, 1985).

Studies of the influence of wing damage on energy expenditure, however, have yielded conflicting results (Cartar, 1992; Hedenström et al., 2001). Although Cartar (1992) suggested that wing area loss may increase the rate of energy expenditure by foraging insects, a later study showed no significant relationship between these two parameters (Hedenström et al., 2001); this is thought to be due to the need for a lesser profile power (see Glossary) for flapping a fractured wing that has a smaller area compared with that of an intact wing. This might also be attributed to the changes in the wing utility associated with wing damage; insects with higher wing area loss have significantly lower load-lifting ability (Johnson and Cartar, 2014). It is important to point out that these studies were performed on bumblebees, which have asynchronous flight muscles (see Glossary). It remains unclear how much of a role the resonance of the flight system plays in the energy expenditure of insects with asynchronous muscles, but wing damage could have very different energetic consequences for insects with synchronous flight muscles, which flap their wings at much lower frequencies.

Although an increase in the flapping frequency appears to be a common strategy among insects suffering from wing damage, the extent of other kinematic adjustments varies between species, and somehow depends on the degree of symmetry of the induced damage (Kassner et al., 2016; Muijres et al., 2017). In the moth Manduca sexta, for example, the flapping amplitude does not change significantly when wing area is reduced symmetrically (Fernández et al., 2012). In contrast, when wing area is reduced asymmetrically, only the flapping amplitude of the clipped wing increases. In the fruit fly Drosophila hydei, the increase in the flapping amplitude of the clipped wing is associated with the opposite adjustment of the intact wing (Muijres et al., 2017). The adjustments associated with asymmetric removal of wing area balance roll torques, which would otherwise spin the insect body about the roll axis (Muijres et al., 2017).

Damselflies, which possess direct flight muscles (see Glossary), show even greater resilience to wing damage (Kassner et al., 2016). In the damselfly Ischnura elegans, complete removal of a hindwing results in a decrease in the flapping amplitude of the hindwing on the opposite side, whereas that of the forewings remains unchanged. By contrast, the stroke plane angle of the contralateral hindwing remains the same as before the treatment, but that of forewings on the same and opposite sides decreases and increases, respectively. This differs from the flight behaviour observed in moths with wing damage, which exhibit a decrease in the stroke plane angle of the clipped wing in any state (Fernández et al., 2012). Kinematic strategies allow the damselfly I. elegans to fly even after removal of 50% of the whole wing area; the four-winged insect can fly with two wings only (Kassner et al., 2016). This is an interesting finding, which indicates the robustness of flying insects to the wing injuries; it suggests that insect wings are capable of resisting forces much higher than those normally exerted during flight. This finding mirrors the fact that the average number of legs of terrestrial insects is fewer than six, revealing the robustness of insects to leg loss (Hu, 2020).

Damage accumulation plays an important role in the evolutionary adaptation of biological materials (Taylor et al., 2007; Meyers et al., 2008; Amini and Miserez, 2013; Labonte et al., 2017). Typical examples are human bone and woody plants: although weaker than many engineering materials, bone and wood are very capable of resisting long-term mechanical stress; in fact, they are better at this than most artificial materials (Taylor et al., 2007; Taylor, 2014). One reason for this is their ability to repair themselves after being damaged (Wegst et al., 2015).

Although previous studies have shown the presence of limited healing in the cuticle of the abdomen of beetles and legs of locusts (Lai-Fook, 1968; Parle et al., 2016a,b), the cuticle of insect wings seems to lack this ability (Newman, 1982). However, wings need to withstand millions of cycles of dynamic stress and numerous mechanical collisions during the lifespan of a flying insect. This gives rise to the question of how the material and structural properties of insect wings allow them to resist damage or mitigate the effects of any damage that occurs.

The limited data available in the literature suggest that the damage resistance of insect wings is based on two complementary strategies that (i) prevent damage initiation and (ii) reduce the rate of damage progression. A recent study showed that the flexibility resulting from the presence of resilin-bearing microjoints, so-called ‘flexible microjoints’, reduces the risk of wing damage by reducing stress concentrations (Rajabi et al., 2016e). This effect is facilitated by the contribution of the soft, resilin-rich core of the veins (Fig. 1B). A similar design strategy has been shown to prevent collision-associated damage in the wings of yellowjacket wasps (Mountcastle and Combes, 2014). These insects have a flexible microjoint, known as costal break, in their forewings. The flexible joint allows the wings to reversibly bend at this point during an induced collision and minimizes wing wear.

Whereas the flexible microjoints prevent or reduce the risk of damage initiation, cross-veins (see Glossary) are likely to inhibit damage propagation. An experimental study on the hindwings of the desert locust Schistocerca gregaria revealed that cross-veins act as obstacles to crack propagation (Dirks and Taylor, 2012). They temporarily stop or deflect a growing crack and, therefore, increase the effective fracture toughness of the wings by ∼50%. Cross-veins distribute the stress ahead of the crack tip over a larger area, and transfer it to neighbouring veins and membranes (Rajabi et al., 2015b, 2017c). A number of other factors are also expected to provide cross-veins with enhanced fracture toughness. In comparison to membranes, cross-veins are thicker and, thus, presumably stronger. They also have pronounced layered structures (Appel et al., 2015), which could trap growing cracks at the interface of the layers. Furthermore, they often contain soft resilin-rich cores (Fig. 1B); this material can arrest propagating cracks, as a result of its high deformability. Our recent investigation of damage in dragonfly wings in nature (Rajabi et al., 2017b; Rudolf et al., 2019) confirmed the results of the laboratory experiments by Dirks and Taylor (2012). Fig. 2D shows several cracks in the hindwing of the dragonfly S. vulgatum that were initiated in a wing cell, but stopped behind veins in the same or adjacent cells (white arrowheads).

Although the existing data suggest that flexible microjoints and cross-veins play an important role in mitigating wing damage, we cannot claim with any certainty that damage control has been the main driving force in the evolution of these wing components. As shown by several previous studies, many wing components, including flexible microjoints, also play a significant role in the deformability of insect wings during flight and, therefore, have aerodynamic functions (Donoughe et al., 2011; Mountcastle and Combes, 2013; Rajabi et al., 2015a, 2016d). Flight is the primary function of insect wings, and it is therefore likely that the main evolutionary advantage of flexible microjoints is enhanced aerodynamic performance of the wings. Therefore, mitigation of wing damage could be a by-product of these wing components.

In contrast to that of the joints, it is likely that damage control played a more important role in the evolution of cross-veins. Cross-veins play only a minor role in wing deformations during flight (Rajabi et al., 2016c). In fact, cross-veins might even reduce the mechanical performance of insect wings, by decreasing their stiffness to weight ratio (Dirks and Taylor, 2012). This means that wings with cross-veins may be less efficient than those lacking cross-veins in providing resistance to elastic deformation, where light-weight wings are required. Hence, by considering the important role of cross-veins in increasing wing toughness (Dirks and Taylor, 2012), we suggest that the mitigation of wing damage might be relatively more important than improvements in flight performance as a driving force in their evolution.

As discussed in this Commentary, the wings of flying insects undergo frequent collisions with objects in the environment (Foster and Cartar, 2011). Excessive stress due to collisions gives rise to wing damage, which can take the form of wear, tear and fracture. Wing damage has a negative impact on insect fitness, primarily as a result of reduced flight ability. There are two strategies that may serve to deal with the negative consequences of wing damage: (i) the initiation and progression of damage are avoided by the evolution of damage-tolerant wings and (ii) when damage leads to area loss, insects adjust their flight kinematics to produce more lift per unit wing area.

Five directions for future research seem particularly worth following (Fig. 3). At present, our knowledge of the relationship between the structural design of insect wings and the damage that they accumulate is very limited. Apart from the studies on the role of flexible microjoints and cross-veins (Dirks and Taylor, 2012; Rajabi et al., 2015b, 2016e; Mountcastle and Combes, 2014), there are, to our knowledge, no further studies that have investigated the presence of other potential mechanisms of damage tolerance in insect wings. The absence of data in this area does not imply that understanding the nature of wing damage is unimportant; rather, it shows the need for new studies.

Future research should focus on quantitative analyses of wing damage based on long-term field observations. We need to know how wing damage is initiated under natural conditions and how it propagates over time. Such analyses could be combined with video recording and analysis of collision events in different flight contexts, as done for bumble bees during foraging (Foster and Cartar, 2011). The data thus obtained could be used to analyse the frequency of collisions in different wing regions. This could help us to understand whether some wing regions are more damage tolerant than others. The results could be verified by mechanical tests on isolated wing regions, similar to those previously done for locust wings (Dirks and Taylor, 2012). The results of such experiments are likely to explain the higher frequency of damage in some wing regions compared with others, as shown for the dragonfly S. vulgatum (Rajabi et al., 2017b; Rudolf et al., 2019). The data could further be used to assess the contribution of different structural components in the damage tolerance of insect wings.

In addition to providing insights into biologically relevant questions, understanding the mechanics of insect wing damage could inform the design of wings of flapping-wing robots. In fact, the lifetime of existing bioinspired flapping robots is still partly limited by the durability of their wings (Bontemps et al., 2012; Ma et al., 2013). According to studies of insect wing biomechanics, incorporating microjoints into the design of artificial wings not only improves their aerodynamic performance (Nakata and Liu, 2011; Mountcastle and Combes, 2013; Rajabi et al., 2016d) but also provides them with the compliance required to withstand accidental collisions (Mountcastle and Combes, 2014; Rajabi et al., 2016e; Mountcastle et al., 2019). In addition, the use of veins is likely to enhance both the fracture and fatigue resistance of the wings (Dirks and Taylor, 2012; Rajabi et al., 2015b, 2017c). Durable wings would facilitate the use of flapping robots in long-range operations, something which has not yet been achieved (Floreano and Wood, 2015).

It is our hope that this Commentary will provide a new perspective for research on the biomechanics of insect wings. Although the existing literature pays considerable attention to wing aerodynamics, we suggest that insect wings might be structurally adapted to meet a variety of functional demands, rather than only flight performance. Therefore, future studies should not view insect wings only as aerofoils, but should also consider fracture mechanics.

We are extremely grateful to David Labonte (Imperial College London) for his valuable comments and suggestions. We would also like to thank Julia Rudolf (Kiel University) and Tom Liessmann (Kiel University) for their assistance with scanning electron microscopy. We would particularly like to thank JEB Reviews Editor, Charlotte Rutledge, for her incredible support, comments and suggestions. We are also grateful to our three anonymous reviewers for their insightful suggestions.