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COMMENTARY
Insect wing damage: causes, consequences and compensatory mechanisms
Hamed Rajabi, Jan-Henning Dirks, Stanislav N. Gorb
Journal of Experimental Biology 2020 223: jeb215194 doi: 10.1242/jeb.215194 Published 4 May 2020
Hamed Rajabi
1Functional Morphology and Biomechanics, Institute of Zoology, Kiel University, Am Botanischen Garten 1-9, D-24098 Kiel, Germany
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  • For correspondence: harajabi@hotmail.com
Jan-Henning Dirks
2Biomimetics-Innovation-Centre, Hochschule Bremen–City University of Applied Sciences, 28199 Bremen, Germany
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Stanislav N. Gorb
1Functional Morphology and Biomechanics, Institute of Zoology, Kiel University, Am Botanischen Garten 1-9, D-24098 Kiel, Germany
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ABSTRACT

The evolution of wings has played a key role in the success of insect species, allowing them to diversify to fill many niches. Insect wings are complex multifunctional structures, which not only have to withstand aerodynamic forces but also need to resist excessive stresses caused by accidental collisions. This Commentary provides a summary of the literature on damage-reducing morphological adaptations in wings, covering natural causes of wing collisions, their impact on the structural integrity of wings and associated consequences for both insect flight performance and life expectancy. Data from the literature and our own observations suggest that insects have evolved strategies that (i) reduce the likelihood of wing damage and (ii) allow them to cope with damage when it occurs: damage-related fractures are minimized because wings evolved to be damage tolerant and, in the case of wing damage, insects compensate for the reduced aerodynamic efficiency with dedicated changes in flight kinematics.

Introduction

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).

Glossary

Asynchronous flight muscle

In this type of muscle, there is no synchrony between muscle electrical activity and muscle contraction. Asynchronous muscles generate higher mechanical power than synchronous muscles. Hence, flying insects with asynchronous muscles reach higher wing-beat frequencies than synchronous fliers.

Cross-vein

A vein that connects longitudinal veins.

Direct flight muscle

This type of flight muscle is directly connected to wing sclerites, in contrast to indirect flight muscles, which insert on the thorax.

Longitudinal vein

A vein that extends along the wing length.

Microjoint

A joint-like structure at the intersection of two, or more, veins.

Nodus

A highly conserved microjoint, situated at the leading edge of dragonfly and damselfly wings.

Profile power

The power required to overcome the drag of a flapping wing.

Resilin

A rubber-like, elastomeric protein that is typically found in the exoskeletons of arthropods.

Stroke plane angle

The angle between the horizontal plane and the stroke plane (the plane of the wing stroke obtained by regression analysis of the wing-tip path).

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).

Fig. 1.
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Fig. 1.

Structural components of the forewing of the dragonfly Sympetrum vulgatum. (A) Scanning electron microscopy (SEM) image showing the cross-section of a vein (Appel et al., 2015). Wing veins have complex multi-layered structures with hierarchical architectures. (B) Confocal laser scanning microscopy (CLSM) image of the cross-section of a longitudinal vein (see Glossary). The vein consists of regions with distinguishable material compositions. The blue, green and red colours in this image indicate the presence of resilin-rich, less sclerotized and highly sclerotized cuticle, respectively. (C) SEM image of the cross-section of a membrane from the trailing margin of the wing (Appel et al., 2015). (D–G) SEM images of different types of vein microjoints. There are a variety of microjoints in insect wings (Donoughe et al., 2011; Appel and Gorb, 2014; Mamat-Noorhidayah et al., 2018), which provide different levels of deformability at the connection of veins (Rajabi et al., 2015a): rigidly fused microjoints (D), fused microjoints (E), flexible microjoints (F) and bridge joints (G). The white arrowhead in F shows the mark caused by the spike on the adjacent vein. Spikes at the joints work as mechanical ‘stoppers’ that limit the joint deformability (Rajabi et al., 2015a, 2016e). (H) SEM image of the dorsal side of the wing nodus. (I,J) SEM images of spikes. Spikes are not only associated with vein microjoints but also widely distributed over the wing surface. They are hypothesized to have an aerodynamic function (Newman et al., 1977; D'Andrea and Carfi, 1988, 1989). (K) CLSM image of a resilin patch situated at the intersection of four veins. (L) CLSM image showing lines of resilin-rich cuticle at the junction of veins and membrane. (M) Forewing of the dragonfly S. vulgatum, showing the approximate position of each given image in A–L. Scale bars: 10 µm (A), 50 µm (B,F), 500 nm (C,H), 100 µm (D,E,G), 300 µm (I,L), 2 mm (J), 200 µm (K), 1 cm (M).

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.

Box 1. Balance between flexibility and stiffness: the secret behind wing functionality

Insect wings are not stiff aerofoils, but rather flexible structures. Wing flexibility, achieved by the specific wing design, improves the ability of the wings to form a cambered shape in flight, thereby enhancing their capacity to generate aerodynamic lift (Mountcastle and Combes, 2013). However, a very flexible wing would not be able to withstand forces generated during flight. Wings should be stiff enough not to simply bend under flight forces. Hence, a balance between flexibility and stiffness is required to ensure a fully functional wing (Wootton, 1981; Rajabi and Gorb, 2020). Structural components provide insect wings with this balance. Whereas some wing components, such as patches of the protein resilin and flexion lines, enhance wing flexibility, others, such as veins and membranes, provide wings with the required stiffness. Interestingly, there are other wing components, such as nodi and microjoints, that combine the two characteristics – they are originally flexible, but under increased loads they are stiffened by an interlocking effect (Rajabi et al., 2017a).

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.

Influence of collisions on the structural integrity of insect wings

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.

Fig. 2.
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Fig. 2.

Most frequent modes of material failure in the hindwing of the dragonfly S. vulgatum. (A) SEM image showing wear near the wing trailing margin (dashed area; Rajabi et al., 2017b). It appears that the waxy surface of the wing in this region has been completely removed. Numerous scratches are visible on the wing surface. (B) SEM image of a crack that was initiated at the wing margin (arrowhead) and is growing into the wing. (C) SEM image showing wing fracture. A part of the wing was completely removed from the region shown by the dashed line. (D) SEM image showing cracks that were stopped behind cross-veins (arrowheads). (E) Hindwing of the dragonfly S. vulgatum showing the approximate position of the images in A–D. Scale bars: 500 µm (A–D), 1 cm (E).

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).

Effects of wing damage and kinematic compensation

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).

Box 2. Wing area loss in birds, bats and insects: similarities and differences

Similar to insects, birds and bats frequently experience partial wing loss during their lifespan. In birds, wing area loss is caused by partial or complete removal of primary feathers as a result of excessive feather distortions (also referred to as wear, abrasion and damage in the feather biomechanics literature) and moulting, if not intrinsic developmental defects (Ginn and Melville, 1983; Francis and Wood, 1989; Swaddle and Witter, 1994). In bats, wing area loss often occurs in the form of membrane holes and membrane loss (Davis, 1968). The major causes of such defects are infections, collisions and predatory attacks (Davis, 1968; Warnecke et al., 2013). As in insects, wing area loss in birds and bats drastically reduces their manoeuvrability, mainly through reduced aerodynamic performance (Jehl, 1990; Hedenström and Sunada, 1999; Hedenström, 2003). Both groups are also able to compensate for the reduced wing area by behavioural adaptations to reduce energetic flight costs (Swaddle et al., 1996; Voigt, 2013). However, in contrast to that in insects, wing area loss in birds and bats can be largely recovered by regrowing moulted feathers and healing, respectively (Davis and Doster, 1972; Faure et al., 2009).

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 wing damage reduces flight performance, insects with damaged wings can adjust their flapping kinematics to maintain the ability to fly (Kassner et al., 2016). In other words, they appear to be able to produce more lift per unit wing area. Most frequently, insects appear to compensate for wing damage by increasing the flapping frequency (Hargrove, 1975; Kingsolver, 1999; Hedenström et al., 2001; Jantzen and Eisner, 2008; Fernández et al., 2012; Roberts and Cartar, 2015; Muijres et al., 2017), adjusting the flapping amplitude (Jantzen and Eisner, 2008; Fernández et al., 2012; Vance and Roberts, 2014; Roberts and Cartar, 2015; Kassner et al., 2016; Muijres et al., 2017) and changing the stroke plane angle (see Glossary) of the wings (Kassner et al., 2016). The increase in wing-beat frequency that is required in order to cope with a certain amount of damage can be estimated using the classical theory of aerodynamic forces. According to this theory, the lift experienced by a wing moving in the air can be calculated as follows:Embedded Image (1)where L is the lift, ρ is the density of the air, S is the wing area and U is the wind speed. CL is the lift coefficient and is constant, if the flow is steady. Now, assuming a 5% reduction in the total wing surface area, the insect could flap its wings 2.6% faster to generate the same lift:Embedded Image (2)However, as mentioned above, the loss of wing area can also be compensated for in other ways – the factors that determine the exact strategies used in response to the loss of wing area are not fully understood, and would be an interesting area for future investigation.

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).

Material and structural properties that prevent initiation and propagation of wing damage

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).

Factors affecting the evolution of insect wings

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.

Conclusions, implications and future directions

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.

Fig. 3.
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Fig. 3.

Directions for future research on wing fracture mechanics. Field observations and laboratory experiments should be performed in order to obtain data to explore wing design from the perspective of fracture mechanics. The results are expected to provide insights into the evolution of a wide variety of wing forms and further to inform the design of man-made structures with enhanced damage tolerance.

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.

Acknowledgements

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.

FOOTNOTES

  • Competing interests

    The authors declare no competing or financial interests.

  • Author contributions

    Conceptualization: H.R., J.-H.D., S.N.G.; Formal Analysis: H.R.; Investigation: H.R.; Data curation: H.R.; Writing - original draft: H.R.; Writing - review & editing: H.R., J.-H.D., S.N.G.; Visualization: H.R.; Supervision: J.-H.D., S.N.G.; Project Administration: S.N.G.

  • © 2020. Published by The Company of Biologists Ltd

References

  1. ↵
    1. Alcock, J.
    (1996). Male size and survival: the effects of male combat and bird predation in Dawson's burrowing bees, Amegilla dawsoni. Ecol. Entomol. 21, 309-316. doi:10.1046/j.1365-2311.1996.00007.x
    OpenUrlCrossRef
  2. ↵
    1. Allsopp, R.
    (1985). Wing fray in Glossina morsitans centralis Machado (Diptera: Glossinidae). Bull. Entomol. Res. 75, 1-11. doi:10.1017/S0007485300014127
    OpenUrlCrossRef
  3. ↵
    1. Amini, S. and
    2. Miserez, A.
    (2013). Wear and abrasion resistance selection maps of biological materials. Acta Biomater. 9, 7895-7907. doi:10.1016/j.actbio.2013.04.042
    OpenUrlCrossRef
  4. ↵
    1. Appel, E. and
    2. Gorb, S. N.
    (2014). Comparative Functional Morphology of Vein Joints in Odonata. Stuttgart: Schweizerbart Science Publishers.
  5. ↵
    1. Appel, E.,
    2. Heepe, L.,
    3. Lin, C.-P. and
    4. Gorb, S. N.
    (2015). Ultrastructure of dragonfly wing veins: composite structure of fibrous material supplemented by resilin. J. Anat. 227, 561-582. doi:10.1111/joa.12362
    OpenUrlCrossRef
  6. ↵
    1. Bontemps, A.,
    2. Vanneste, T.,
    3. Paquet, J.-B.,
    4. Dietsch, T.,
    5. Grondel, S. and
    6. Cattan, E.
    (2012). Design and performance of an insect-inspired nano air vehicle. Smart Mater. Struct. 22, 014008. doi:10.1088/0964-1726/22/1/014008
    OpenUrlCrossRef
  7. ↵
    1. Burkhard, D. U.,
    2. Ward, P. I. and
    3. Blanckenhorn, W. U.
    (2002). Using age grading by wing injuries to estimate size-dependent adult survivorship in the field: a case study of the yellow dung fly Scathophaga stercoraria. Ecol. Entomol. 27, 514-520. doi:10.1046/j.1365-2311.2002.00453.x
    OpenUrlCrossRef
  8. ↵
    1. Cartar, R. V.
    (1992). Morphological senescence and longevity: an experiment relating wing wear and life span in foraging wild bumble bees. J. Anim. Ecol. 61, 225-231. doi:10.2307/5525
    OpenUrlCrossRef
  9. ↵
    1. Combes, S. A. and
    2. Daniel, T. L.
    (2003a). Flexural stiffness in insect wings I. Scaling and the influence of wing venation. J. Exp. Biol. 206, 2979-2987. doi:10.1242/jeb.00523
    OpenUrlAbstract/FREE Full Text
  10. ↵
    1. Combes, S. A. and
    2. Daniel, T. L.
    (2003b). Flexural stiffness in insect wings II. Spatial distribution and dynamic wing bending. J. Exp. Biol. 206, 2989-2997. doi:10.1242/jeb.00524
    OpenUrlAbstract/FREE Full Text
  11. ↵
    1. Combes, S. A.,
    2. Crall, J. D. and
    3. Mukherjee, S.
    (2010). Dynamics of animal movement in an ecological context: dragonfly wing damage reduces flight performance and predation success. Biol. Lett. 6, 426-429. doi:10.1098/rsbl.2009.0915
    OpenUrlCrossRefPubMed
  12. ↵
    1. Daly, H. V.,
    2. Doyen, J. T. and
    3. Ehrlich, P. R.
    (1978). Introduction to Insect Biology and Diversity. New York: McGraw-Hill.
  13. ↵
    1. Davis, R.
    (1968). Wing defects in a population of pallid bats. Am. Midl. Nat. 79, 388-395. doi:10.2307/2423184
    OpenUrlCrossRef
  14. ↵
    1. Davis, R. and
    2. Doster, S. E.
    (1972). Wing repair in pallid bats. J. Mammal. 53, 377-378. doi:10.2307/1379180
    OpenUrlCrossRefWeb of Science
  15. ↵
    1. D'Andrea, M. and
    2. Carfi, S.
    (1988). Spines on the wing veins in Odonata. 1. Zygoptera. Odonatologica 17, 313-335.
    OpenUrl
  16. ↵
    1. D'Andrea, M. and
    2. Carfi, S.
    (1989). Spines on the wing veins in Odonata 2. Anisozygoptera and Anisoptera. Odonatologica 18, 147-178.
    OpenUrl
  17. ↵
    1. Dirks, J. H. and
    2. Taylor, D.
    (2012). Veins improve fracture toughness of insect wings. PLoS ONE 7, e43411. doi:10.1371/journal.pone.0043411
    OpenUrlCrossRefPubMed
  18. ↵
    1. Donoughe, S.,
    2. Crall, J. D.,
    3. Merz, R. A. and
    4. Combes, S. A.
    (2011). Resilin in dragonfly and damselfly wings and its implications for wing flexibility. J. Morphol. 272, 1409-1421. doi:10.1002/jmor.10992
    OpenUrlCrossRefPubMedWeb of Science
  19. ↵
    1. Dukas, R. and
    2. Dukas, L.
    (2011). Coping with nonrepairable body damage: effects of wing damage on foraging performance in bees. Anim. Behav. 81, 635-638. doi:10.1016/j.anbehav.2010.12.011
    OpenUrlCrossRefWeb of Science
  20. ↵
    1. Ellington, C. P.,
    2. Van Den Berg, C.,
    3. Willmott, A. P. and
    4. Thomas, A. L.
    (1996). Leading-edge vortices in insect flight. Nature 384, 626. doi:10.1038/384626a0
    OpenUrlCrossRefWeb of Science
  21. ↵
    1. Ennos, A. R.
    (1995). Mechanical behaviour in torsion of insect wings, blades of grass and other cambered structures. Proc. R. Soc. Lond. B Biol. Sci. 259, 15-18. doi:10.1098/rspb.1995.0003
    OpenUrlCrossRef
  22. ↵
    1. Ennos, A. R.
    (1988). The importance of torsion in the design of insect wings. J. Exp. Biol. 140, 137-160.
    OpenUrlAbstract/FREE Full Text
  23. ↵
    1. Faure, P. A.,
    2. Re, D. E. and
    3. Clare, E. L.
    (2009). Wound healing in the flight membranes of big brown bats. J. Mammal. 90, 1148-1156. doi:10.1644/08-MAMM-A-332.1
    OpenUrlCrossRef
  24. ↵
    1. Fauziyah, S.,
    2. Alam, C.,
    3. Soesilohadi, R. C. H.,
    4. Retnoaji, B. and
    5. Alam, P.
    (2014). Morphological and mechanical characterisation of the hindwing nodus from the Libellulidae family of dragonfly (Indonesia). Arthropod. Struct. Dev. 43, 415-422. doi:10.1016/j.asd.2014.06.004
    OpenUrlCrossRef
  25. ↵
    1. Fernández, M. J.,
    2. Springthorpe, D. and
    3. Hedrick, T. L.
    (2012). Neuromuscular and biomechanical compensation for wing asymmetry in insect hovering flight. J. Exp. Biol. 215, 3631-3638. doi:10.1242/jeb.073627
    OpenUrlAbstract/FREE Full Text
  26. ↵
    1. Floreano, D. and
    2. Wood, R. J.
    (2015). Science, technology and the future of small autonomous drones. Nature 521, 460. doi:10.1038/nature14542
    OpenUrlCrossRefPubMed
  27. ↵
    1. Foster, D. J. and
    2. Cartar, R. V.
    (2011). What causes wing wear in foraging bumble bees? J. Exp. Biol. 214, 1896-1901. doi:10.1242/jeb.051730
    OpenUrlAbstract/FREE Full Text
  28. ↵
    1. Francis, C. M. and
    2. Wood, D. S.
    (1989). Effects of age and wear on wing length of wood-warblers. J. Field Ornithol. 60, 495-503.
    OpenUrl
  29. ↵
    1. Ginn, H. B. and
    2. Melville, D. S.
    (1983). Moult in Birds. Tring: British Trust for Ornithology.
  30. ↵
    1. Gorb, S. N.
    (1999). Serial elastic elements in the damselfly wing: mobile vein joints contain resilin. Naturwissenschaften 86, 552-555. doi:10.1007/s001140050674
    OpenUrlCrossRefPubMedWeb of Science
  31. ↵
    1. Gorb, S. N.,
    2. Tynkkynen, K. and
    3. Kotiaho, J. S.
    (2009). Crystalline wax coverage of the imaginal cuticle in Calopteryx splendens (Odonata: Calopterygidae). Int. J. Odonatol. 12, 205-221. doi:10.1080/13887890.2009.9748340
    OpenUrlCrossRef
  32. ↵
    1. Grebennikov, V. V.
    (2008). How small you can go: Factors limiting body miniaturization in winged insects with a review of the pantropical genus Discheramocephalus and description of six new species of the smallest beetles (Pterygota: Coleoptera: Ptiliidae). Eur. J. Entomol. 105, 313-328. doi:10.14411/eje.2008.039
    OpenUrlCrossRef
  33. ↵
    1. Hargrove, J. W.
    (1975). The flight performance of tsetse flies. J. Insect Physiol. 21, 1385-1395. doi:10.1016/0022-1910(75)90264-4
    OpenUrlCrossRefPubMedWeb of Science
  34. ↵
    1. Hedenström, A.
    (2003). Flying with holey wings. J. Avian Biol. 34, 324-327. doi:10.1111/j.0908-8857.2003.03324.x
    OpenUrlCrossRef
  35. ↵
    1. Hedenström, A. and
    2. Sunada, S.
    (1999). On the aerodynamics of moult gaps in birds. J. Exp. Biol. 202, 67-76.
    OpenUrlAbstract/FREE Full Text
  36. ↵
    1. Hedenström, A.,
    2. Ellington, C. P. and
    3. Wolf, T. J.
    (2001). Wing wear, aerodynamics and flight energetics in bumblebees (Bombus terrestris): an experimental study. Funct. Ecol. 15, 417-422. doi:10.1046/j.0269-8463.2001.00531.x
    OpenUrlCrossRef
  37. ↵
    1. Haemig, P. D.
    (1997). Effects of birds on the intensity of ant rain: a terrestrial form of invertebrate drift. Anim. Behav. 54, 89-97. doi:10.1006/anbe.1996.0428
    OpenUrlCrossRefPubMedWeb of Science
  38. ↵
    1. Higginson, A. D. and
    2. Gilbert, F.
    (2004). Paying for nectar with wingbeats: a new model of honeybee foraging. Proc. Royal Soc. Lond. B. Biol. Sci. 271, 2595-2603. doi:10.1098/rspb.2004.2866
    OpenUrlCrossRefPubMedWeb of Science
  39. ↵
    1. Hu, D.
    (2020). How To Walk on Water and Climb up Walls. Princeton: Princeton University Press.
  40. ↵
    1. Jantzen, B. and
    2. Eisner, T.
    (2008). Hindwings are unnecessary for flight but essential for execution of normal evasive flight in Lepidoptera. Proc. Natl Acad. Sci. USA 105, 16636-16640. doi:10.1073/pnas.0807223105
    OpenUrlAbstract/FREE Full Text
  41. ↵
    1. Jehl, J. R.
    (1990). Aspects of the molt migration. In Bird Migration (ed. E. Gwinner), pp. 10-113. Heidelberg: Springer.
  42. ↵
    1. Johnson, S. A. and
    2. Cartar, R. V.
    (2014). Wing wear, but not asymmetry in wear, affects load-lifting capability in bumble bees Bombus impatiens. Can. J. Zool. 92, 179-184. doi:10.1139/cjz-2013-0229
    OpenUrlCrossRef
  43. ↵
    1. Johnston, P. R. and
    2. Rolff, J.
    (2015). Host and symbiont jointly control gut microbiota during complete metamorphosis. PLoS Pathog. 11, e1005246. doi:10.1371/journal.ppat.1005246
    OpenUrlCrossRefPubMed
  44. ↵
    1. Jongerius, S. R. and
    2. Lentink, D.
    (2010). Structural analysis of a dragonfly wing. Exp. Mech. 50, 1323-1334. doi:10.1007/s11340-010-9411-x
    OpenUrlCrossRef
  45. ↵
    1. Kassner, Z.,
    2. Dafni, E. and
    3. Ribak, G.
    (2016). Kinematic compensation for wing loss in flying damselflies. J. Insect Physiol. 85, 1-9. doi:10.1016/j.jinsphys.2015.11.009
    OpenUrlCrossRef
  46. ↵
    1. Kennedy, C. H.
    (1927). The exoskeleton as a factor in limiting and directing the evolution of insects. J. Morphol. 44, 267-312. doi:10.1002/jmor.1050440204
    OpenUrlCrossRef
  47. ↵
    1. Kesel, A. B.,
    2. Philippi, U. and
    3. Nachtigall, W.
    (1998). Biomechanical aspects of the insect wing: an analysis using the finite element method. Comput. Biol. Med. 28, 423-437. doi:10.1016/S0010-4825(98)00018-3
    OpenUrlCrossRefPubMed
  48. ↵
    1. Kingsolver, J. G.
    (1999). Experimental analyses of wing size, flight, and survival in the western white butterfly. Evolution 53, 1479-1490. doi:10.1111/j.1558-5646.1999.tb05412.x
    OpenUrlCrossRefWeb of Science
  49. ↵
    1. Labonte, D.,
    2. Lenz, A. K. and
    3. Oyen, M. L.
    (2017). On the relationship between indentation hardness and modulus, and the damage resistance of biological materials. Acta Biomater. 57, 373-383. doi:10.1016/j.actbio.2017.05.034
    OpenUrlCrossRef
  50. ↵
    1. Lai-Fook, J.
    (1968). The fine structure of wound repair in an insect (Rhodnius prolixus). J. Morphol. 124, 37-77. doi:10.1002/jmor.1051240104
    OpenUrlCrossRefPubMedWeb of Science
  51. ↵
    1. Ma, K. Y.,
    2. Chirarattananon, P.,
    3. Fuller, S. B. and
    4. Wood, R. J.
    (2013). Controlled flight of a biologically inspired, insect-scale robot. Science 340, 603-607. doi:10.1126/science.1231806
    OpenUrlAbstract/FREE Full Text
    1. Mamat-Noorhidayah, K. Y.,
    2. Numata, K. and
    3. Norma-Rashid, Y.
    (2018). Morphological and mechanical properties of flexible resilin joints on damselfly wings (Rhinocypha spp.). PLoS One 13, e0193147. doi:10.1371/journal.pone.0193147
    OpenUrlCrossRef
  52. ↵
    1. May, R. M.
    (1988). How many species are there on earth? Science 241, 1441-1449. doi:10.1126/science.241.4872.1441
    OpenUrlAbstract/FREE Full Text
  53. ↵
    1. Meyers, M. A.,
    2. Chen, P. Y.,
    3. Lin, A. Y. M. and
    4. Seki, Y.
    (2008). Biological materials: structure and mechanical properties. Prog. Mater. Sci. 53, 1-206. doi:10.1016/j.pmatsci.2007.05.002
    OpenUrlCrossRefWeb of Science
  54. ↵
    1. Misof, B.,
    2. Liu, S.,
    3. Meusemann, K.,
    4. Peters, R. S.,
    5. Donath, A.,
    6. Mayer, C.,
    7. Frandsen, P. B.,
    8. Ware, J.,
    9. Flouri, T.,
    10. Beutel, R. G. et al.
    (2014). Phylogenomics resolves the timing and pattern of insect evolution. Science, 346, 763-767. doi:10.1126/science.1257570
    OpenUrlAbstract/FREE Full Text
  55. ↵
    1. Mora, C.,
    2. Tittensor, D. P.,
    3. Adl, S.,
    4. Simpson, A. G.
    5. Worm, B.
    (2011). How many species are there on Earth and in the ocean? PLoS Biol. 9, e1001127. doi:10.1371/journal.pbio.1001127
    OpenUrlCrossRefPubMed
  56. ↵
    1. Mountcastle, A. M. and
    2. Combes, S. A.
    (2013). Wing flexibility enhances load-lifting capacity in bumblebees. Proc. R. Soc. B 280, 20130531. doi:10.1098/rspb.2013.0531
    OpenUrlCrossRefPubMed
  57. ↵
    1. Mountcastle, A. M. and
    2. Combes, S. A.
    (2014). Biomechanical strategies for mitigating collision damage in insect wings: structural design versus embedded elastic materials. J. Exp. Biol. 217, 1108-1115. doi:10.1242/jeb.092916
    OpenUrlAbstract/FREE Full Text
  58. ↵
    1. Mountcastle, A. M.,
    2. Alexander, T. M.,
    3. Switzer, C. M. and
    4. Combes, S. A.
    (2016). Wing wear reduces bumblebee flight performance in a dynamic obstacle course. Biol. Lett. 12, 20160294. doi:10.1098/rsbl.2016.0294
    OpenUrlCrossRefPubMed
  59. ↵
    1. Mountcastle, A. M.,
    2. Helbling, E. F. and
    3. Wood, R. J.
    (2019). An insect-inspired collapsible wing hinge dampens collision-induced body rotation rates in a microrobot. J. R. Soc. Interface 16, 20180618. doi:10.1098/rsif.2018.0618
    OpenUrlCrossRef
  60. ↵
    1. Muijres, F. T.,
    2. Iwasaki, N. A.,
    3. Elzinga, M. J.,
    4. Melis, J. M. and
    5. Dickinson, M. H.
    (2017). Flies compensate for unilateral wing damage through modular adjustments of wing and body kinematics. Interface Focus 7, 20160103. doi:10.1098/rsfs.2016.0103
    OpenUrlCrossRef
  61. ↵
    1. Nakata, T. and
    2. Liu, H.
    (2011). Aerodynamic performance of a hovering hawkmoth with flexible wings: a computational approach. Proc. R. Soc. B 279, 722-731. doi:10.1098/rspb.2011.1023
    OpenUrlCrossRefPubMed
  62. ↵
    1. Newman, D. J.
    (1982). The Functional Wing Morphology of some Odonata. Exeter: University of Exeter.
    1. Newman, D. J. S. and
    2. Wootton, R. J.
    (1986). An approach to the mechanics of pleating in dragonfly wings. J. Exp. Biol. 125, 361-372.
    OpenUrlAbstract/FREE Full Text
  63. ↵
    1. Newman, B. G.,
    2. Savage, S. G. and
    3. Schouella, D.
    (1977). Model tests on a wing section of an aeschna dragonfly. In Scale Effects in Animal Locomotion (ed. T. J. Pedley), pp. 475-489. New York: Academic Press.
  64. ↵
    1. Parle, E.,
    2. Dirks, J. H. and
    3. Taylor, D.
    (2016a). Damage, repair and regeneration in insect cuticle: The story so far, and possibilities for the future. Arthropod. Struct. Dev. 46, 49-55. doi:10.1016/j.asd.2016.11.008
    OpenUrlCrossRef
  65. ↵
    1. Parle, E.,
    2. Dirks, J. H. and
    3. Taylor, D.
    (2016b). Bridging the gap: wound healing in insects restores mechanical strength by targeted cuticle deposition. J. R. Soc. Interface 13, 20150984. doi:10.1098/rsif.2015.0984
    OpenUrlCrossRefPubMed
  66. ↵
    1. Pradhan, S.
    (1969). Insect Pests of Crops. Delhi: National Book Trust.
  67. ↵
    1. Ragland, S. S. and
    2. Sohal, R. S.
    (1973). Mating behavior, physical activity and aging in the housefly, Musca domestica. Exp. Gerontol. 8, 135-145. doi:10.1016/0531-5565(73)90003-X
    OpenUrlCrossRefPubMedWeb of Science
  68. ↵
    1. Rajabi, H. and
    2. Gorb, S. N.
    (2020). How do dragonfly wings work? A brief guide to functional roles of wing structural components. Int. J. Odonatol. 23, 23-30. doi:10.1080/13887890.2019.1677515
    OpenUrlCrossRef
  69. ↵
    1. Rajabi, H.,
    2. Moghadami, M. and
    3. Darvizeh, A.
    (2011). Investigation of microstructure, natural frequencies and vibration modes of dragonfly wing. J. Bionic Eng. 8, 165-173. doi:10.1016/S1672-6529(11)60014-0
    OpenUrlCrossRef
  70. ↵
    1. Rajabi, H.,
    2. Ghoroubi, N.,
    3. Darvizeh, A.,
    4. Dirks, J.-H.,
    5. Appel, E. and
    6. Gorb, S. N.
    (2015a). A comparative study of the effects of vein-joints on the mechanical behaviour of insect wings: I. Single joints. Bioinspir. Biomim. 10, 056003. doi:10.1088/1748-3190/10/5/056003
    OpenUrlCrossRef
  71. ↵
    1. Rajabi, H.,
    2. Darvizeh, A.,
    3. Shafiei, A.,
    4. Taylor, D. and
    5. Dirks, J.-H.
    (2015b). Numerical investigation of insect wing fracture behaviour. J. Biomech. 48, 89-94. doi:10.1016/j.jbiomech.2014.10.037
    OpenUrlCrossRef
  72. ↵
    1. Rajabi, H.,
    2. Ghoroubi, N.,
    3. Malaki, M.,
    4. Darvizeh, A. and
    5. Gorb, S. N.
    (2016a). Basal complex and basal venation of Odonata wings: structural diversity and potential role in the wing deformation. PLoS ONE 11, e0160610. doi:10.1371/journal.pone.0160610
    OpenUrlCrossRef
  73. ↵
    1. Rajabi, H.,
    2. Shafiei, A.,
    3. Darvizeh, A.,
    4. Dirks, J.-H.,
    5. Appel, E. and
    6. Gorb, S. N.
    (2016b). Effect of microstructure on the mechanical and damping behaviour of dragonfly wing veins. R. Soc. Open Sci. 3, 160006. doi:10.1098/rsos.160006
    OpenUrlCrossRef
  74. ↵
    1. Rajabi, H.,
    2. Rezasefat, M.,
    3. Darvizeh, A.,
    4. Dirks, J.-H.,
    5. Eshghi, S. H.,
    6. Shafiei, A.,
    7. Mostofi, T. M. and
    8. Gorb, S. N.
    (2016c). A comparative study of the effects of constructional elements on the mechanical behaviour of dragonfly wings. Appl. Phys. A 122, 19. doi:10.1007/s00339-015-9557-6
    OpenUrlCrossRef
  75. ↵
    1. Rajabi, H.,
    2. Ghoroubi, N.,
    3. Darvizeh, A.,
    4. Appel, E. and
    5. Gorb, S. N.
    (2016d). Effects of multiple vein microjoints on the mechanical behaviour of dragonfly wings: numerical modelling. R. Soc. Open Sci. 3, 150610. doi:10.1098/rsos.150610
    OpenUrlCrossRef
  76. ↵
    1. Rajabi, H.,
    2. Shafiei, A.,
    3. Darvizeh, A. and
    4. Gorb, S. N.
    (2016e). Resilin microjoints: a smart design strategy to avoid failure in dragonfly wings. Sci. Rep. 6, 39039. doi:10.1038/srep39039
    OpenUrlCrossRef
  77. ↵
    1. Rajabi, H.,
    2. Ghoroubi, N.,
    3. Stamm, K.,
    4. Appel, E. and
    5. Gorb, S. N.
    (2017a). Dragonfly wing nodus: a one-way hinge contributing to the asymmetric wing deformation. Acta Biomater. 60, 330-338. doi:10.1016/j.actbio.2017.07.034
    OpenUrlCrossRef
  78. ↵
    1. Rajabi, H.,
    2. Schroeter, V.,
    3. Eshghi, S. and
    4. Gorb, S. N.
    (2017b). The probability of wing damage in the dragonfly Sympetrum vulgatum (Anisoptera: Libellulidae): a field study. Biol. Open 6, 1290-1293. doi:10.1242/bio.027078
    OpenUrlAbstract/FREE Full Text
  79. ↵
    1. Rajabi, H.,
    2. Bazargan, P.,
    3. Pourbabaei, A.,
    4. Eshghi, S.,
    5. Darvizeh, A.,
    6. Gorb, S. N.,
    7. Taylor, D. and
    8. Dirks, J.-H.
    (2017c). Wing cross veins: an efficient biomechanical strategy to mitigate fatigue failure of insect cuticle. Biomech. Model. Mechanobiol. 16, 1947-1955. doi:10.1007/s10237-017-0930-6
    OpenUrlCrossRef
  80. ↵
    1. Rajabi, H.,
    2. Stamm, K.,
    3. Appel, E. and
    4. Gorb, S. N.
    (2018). Micro-morphological adaptations of the wing nodus to flight behaviour in four dragonfly species from the family Libellulidae (Odonata: Anisoptera). Arthropod. Struct. Dev. 47, 442-448. doi:10.1016/j.asd.2018.01.003
    OpenUrlCrossRef
  81. ↵
    1. Ritcher, P. O.
    (1976). Insect abundance. Am. Biol. Teach. 38, 235-238. doi:10.2307/4445555
    OpenUrlFREE Full Text
  82. ↵
    1. Robbins, R. K.
    (1981). The “false head” hypothesis: predation and wing pattern variation of lycaenid butterflies. Am. Nat. 118, 770-775. doi:10.1086/283868
    OpenUrlCrossRefWeb of Science
  83. ↵
    1. Roberts, J. C. and
    2. Cartar, R. V.
    (2015). Shape of wing wear fails to affect load lifting in common eastern bumble bees (Bombus impatiens) with experimental wing wear. Can. J. Zool. 93, 531-537. doi:10.1139/cjz-2014-0317
    OpenUrlCrossRef
  84. ↵
    1. Rodd, F. H.,
    2. Plowright, R. C. and
    3. Owen, R. E.
    (1980). Mortality rates of adult bumble bee workers (Hymenoptera: Apidae). Can. J. Zool. 58, 1718-1721. doi:10.1139/z80-236
    OpenUrlCrossRefWeb of Science
  85. ↵
    1. Roman, A. and
    2. Szczesna, N.
    (2008). Assessment of the flying activity of the buff-tailed bumblebee (Bombus terrestris L.) on greenhouse-grown tomatoes. J. Apic. Sci. 52, 93-100.
    OpenUrl
  86. ↵
    1. Rudolf, J.,
    2. Wang, L. Y.,
    3. Gorb, S. N. and
    4. Rajabi, H.
    (2019). On the fracture resistance of dragonfly wings. J. Mech. Behav. Biomed. Mater. 99, 127-133. doi:10.1016/j.jmbbm.2019.07.009
    OpenUrlCrossRef
  87. ↵
    1. Rueppell, O.,
    2. Fondrk, M. K. and
    3. Page, R. E. Jr.
    (2005). Biodemographic analysis of male honey bee mortality. Aging Cell 4, 13-19. doi:10.1111/j.1474-9728.2004.00141.x
    OpenUrlCrossRefPubMedWeb of Science
  88. ↵
    1. Rüppell, G.
    (1989). Kinematic analysis of symmetrical flight manoeuvres of Odonata. J. Exp. Biol. 144, 13-42.
    OpenUrlAbstract/FREE Full Text
  89. ↵
    1. Rüppell, G. and
    2. Hilfert-Rüppell, D.
    (2013). Biting in dragonfly fights. Int. J. Odonatol. 16, 219-229. doi:10.1080/13887890.2013.804364
    OpenUrlCrossRef
  90. ↵
    1. Shapiro, A. M.
    (1974). Beak-mark frequency as an index of seasonal predation intensity on common butterflies. Am. Nat. 108, 229-232. doi:10.1086/282901
    OpenUrlCrossRefWeb of Science
  91. ↵
    1. Smith, C. W.,
    2. Herbert, R.,
    3. Wootton, R. J. and
    4. Evans, K. E.
    (2000). The hind wing of the desert locust (Schistocerca gregaria Forskal). II. Mechanical properties and functioning of the membrane. J. Exp. Biol. 203, 2933-2943.
    OpenUrlAbstract
  92. ↵
    1. Sorensen, J. T.
    (2009). Aphids. In Encyclopedia of Insects, pp. 27-31. Cambridge: Academic Press.
  93. ↵
    1. Srygley, R. B. and
    2. Thomas, A. L. R.
    (2002). Unconventional lift-generating mechanisms in free-flying butterflies. Nature 420, 660. doi:10.1038/nature01223
    OpenUrlCrossRefPubMedWeb of Science
  94. ↵
    1. Stevens, M.
    (2013). Sensory Ecology, Behaviour, and Evolution (ed. V. H. Resh, R. T. Cardé). Oxford: Oxford University Press.
  95. ↵
    1. Sunada, S.,
    2. Zeng, L. and
    3. Kawachi, K.
    (1998). The relationship between dragonfly wing structure and torsional deformation. J. Theor. Biol., 193, 39-45. doi:10.1006/jtbi.1998.0678
    OpenUrlCrossRefWeb of Science
  96. ↵
    1. Swaddle, J. P. and
    2. Witter, M. S.
    (1994). Food, feathers and fluctuating asymmetries. Proc. R. Soc. Lond. B Biol. Sci. 255, 147-152. doi:10.1098/rspb.1994.0021
    OpenUrlCrossRef
  97. ↵
    1. Swaddle, J. P.,
    2. Witter, M. S.,
    3. Cuthill, I. C.,
    4. Budden, A. and
    5. McCowen, P.
    (1996). Plumage condition affects flight performance in common starlings: implications for developmental homeostasis, abrasion and moult. J. Avian Biol. 27, 103-111. doi:10.2307/3677139
    OpenUrlCrossRef
  98. ↵
    1. Taylor, D.
    (2014). Fracture mechanics: inspirations from nature. Frattura ed Integrità Strutturale 8, 1-6. doi:10.3221/IGF-ESIS.30.01
    OpenUrlCrossRef
  99. ↵
    1. Taylor, D.,
    2. Hazenberg, J. G. and
    3. Lee, T. C.
    (2007). Living with cracks: damage and repair in human bone. Nat. Mater. 6, 263. doi:10.1038/nmat1866
    OpenUrlCrossRefPubMedWeb of Science
  100. ↵
    1. Tipton, V. J.
    (1976). Insects: a success story. Am. Biol. Teach. 38, 205-207. doi:10.2307/4445548
    OpenUrlFREE Full Text
  101. ↵
    1. Toth, A. L.,
    2. Bilof, K. B. J.,
    3. Henshaw, M. T.,
    4. Hunt, J. H. and
    5. Robinson, G. E.
    (2009). Lipid stores, ovary development, and brain gene expression in Polistes metricus females. Insectes Soc. 56, 77-84. doi:10.1007/s00040-008-1041-2
    OpenUrlCrossRefWeb of Science
  102. ↵
    1. Vance, J. T. and
    2. Roberts, S. P.
    (2014). The effects of artificial wing wear on the flight capacity of the honey bee Apis mellifera. J. Insect Physiol. 65, 27-36. doi:10.1016/j.jinsphys.2014.04.003
    OpenUrlCrossRefPubMed
  103. ↵
    1. Voigt, C. C.
    (2013). Bat flight with bad wings: is flight metabolism affected by damaged wings? J. Exp. Biol. 216, 1516-1521. doi:10.1242/jeb.079509
    OpenUrlAbstract/FREE Full Text
  104. ↵
    1. Wagner, D. L. and
    2. Liebherr, J. K.
    (1992). Flightlessness in insects. Trends Ecol. Evol. 7, 216-220. doi:10.1016/0169-5347(92)90047-F
    OpenUrlCrossRefPubMedWeb of Science
  105. ↵
    1. Warnecke, L.,
    2. Turner, J. M.,
    3. Bollinger, T. K.,
    4. Misra, V.,
    5. Cryan, P. M.,
    6. Blehert, D. S.,
    7. Wibbelt, G. and
    8. Willis, C. K.
    (2013). Pathophysiology of white-nose syndrome in bats: a mechanistic model linking wing damage to mortality. Biol. Lett. 9, 20130177. doi:10.1098/rsbl.2013.0177
    OpenUrlCrossRefPubMed
  106. ↵
    1. Wegst, U. G.,
    2. Bai, H.,
    3. Saiz, E.,
    4. Tomsia, A. P. and
    5. Ritchie, R. O.
    (2015). Bioinspired structural materials. Nat. Mater. 14, 23. doi:10.1038/nmat4089
    OpenUrlCrossRefPubMed
  107. ↵
    1. Wilson, E. O.
    (2002). Hotspots-Preserving pieces of fragile biosphere. National Geographic 1, 318.
    OpenUrl
  108. ↵
    1. Wootton, R. J.
    (1981). Support and deformability in insect wings. J. Zool. 193, 447-468. doi:10.1111/j.1469-7998.1981.tb01497.x
    OpenUrlCrossRefWeb of Science
  109. ↵
    1. Wootton, R. J.
    (1992). Functional morphology of insect wings. Annu. Rev. Entomol. 37, 113-140. doi:10.1146/annurev.en.37.010192.000553
    OpenUrlCrossRefWeb of Science
  110. ↵
    1. Wootton, R. J.
    (1993). Leading edge section and asymmetric twisting in the wings of flying butterflies (Insecta, Papilionoidea). J. Exp. Biol. 180, 105-117.
    OpenUrlFREE Full Text
  111. ↵
    1. Wootton, R. J.
    (1999). Invertebrate paraxial locomotory appendages: design, deformation and control. J. Exp. Biol. 202, 3333-3345.
    OpenUrlAbstract/FREE Full Text
  112. ↵
    1. Wootton, R. J. and
    2. Newman, D. J.
    (2008). Evolution, diversification, and mechanics of dragonfly wings. In Dragonflies & Damselflies. Model Organisms for Ecological and Evolutionary Research (ed. A. Córdoba-Aguilar), pp. 261-275. Oxford: Oxford University Press.
  113. ↵
    1. Wootton, R. J.,
    2. Evans, K. E.,
    3. Herbert, R. and
    4. Smith, C. W.
    (2000). The hind wing of the desert locust (Schistocerca gregaria Forskal). I. Functional morphology and mode of operation. J. Exp. Biol. 203, 2921-2931.
    OpenUrlAbstract
  114. ↵
    1. Wootton, R. J.,
    2. Herbert, R. C.,
    3. Young, P. G. and
    4. Evans, K. E.
    (2003). Approaches to the structural modelling of insect wings. Phil. Trans. R. Soc. B 358, 1577-1587. doi:10.1098/rstb.2003.1351
    OpenUrlCrossRefPubMedWeb of Science
  115. ↵
    1. Yamazaki, K.
    (2010). Parachuting behavior and predation by ants in the nettle caterpillar, Scopelodes contracta. J. Insect Sci. 10, 39. doi:10.1673/031.010.3901
    OpenUrlCrossRefPubMed
  116. ↵
    1. Yanoviak, S. P.,
    2. Dudley, R. and
    3. Kaspari, M.
    (2005). Directed aerial descent in canopy ants. Nature 433, 624. doi:10.1038/nature03254
    OpenUrlCrossRefPubMedWeb of Science
  117. ↵
    1. Young, J.,
    2. Walker, S. M.,
    3. Bomphrey, R. J.,
    4. Taylor, G. K. and
    5. Thomas, A. L.
    (2009). Details of insect wing design and deformation enhance aerodynamic function and flight efficiency. Science 325, 1549-1552. doi:10.1126/science.1175928
    OpenUrlAbstract/FREE Full Text
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Keywords

  • Collision
  • Wear
  • Tear
  • Area loss
  • Fracture
  • Flight
  • Cuticle

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Insect wing damage: causes, consequences and compensatory mechanisms
Hamed Rajabi, Jan-Henning Dirks, Stanislav N. Gorb
Journal of Experimental Biology 2020 223: jeb215194 doi: 10.1242/jeb.215194 Published 4 May 2020
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COMMENTARY
Insect wing damage: causes, consequences and compensatory mechanisms
Hamed Rajabi, Jan-Henning Dirks, Stanislav N. Gorb
Journal of Experimental Biology 2020 223: jeb215194 doi: 10.1242/jeb.215194 Published 4 May 2020

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  • Top
  • Article
    • ABSTRACT
    • Introduction
    • Influence of collisions on the structural integrity of insect wings
    • Effects of wing damage and kinematic compensation
    • Material and structural properties that prevent initiation and propagation of wing damage
    • Factors affecting the evolution of insect wings
    • Conclusions, implications and future directions
    • Acknowledgements
    • FOOTNOTES
    • References
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