Wing wear affects wing use and choice of floral density in foraging bumble bees

The effects of flight behavior on physiology and senescence may be profound in insects because of the extremely high metabolic costs of flight. Flight capacity in insects decreases with age; in contrast, limiting flight behavior extends lifespan and slows the age-related loss of antioxidant capacity and accumulation of oxidative damage in flight muscles. In this study, we tested the effects of age and lifetime flight behavior on flight capacity by measuring wingbeat frequency, the ability to fly in a hypo-dense gas mixture, and metabolic rate in Drosophila melanogaster. Specifically, 5-day-old adult flies were separated into three life-long treatments: (1) those not allowed to fly (no flight), (2) those allowed -but not forced -to fly (voluntary flight) and (3) those mechanically stimulated to fly (induced flight). Flight capacity senesced earliest in flies from the no-flight treatment, followed by the induced-flight group and then the voluntary flight group. Wingbeat frequency senesced with age in all treatment groups, but was most apparent in the voluntary-and induced-flight groups. Metabolic rate during agitated flight senesced earliest and most rapidly in the induced flight group, and was low and uniform throughout age in the no-flight group. Early senescence in the induced-flight group was likely due to the acceleration of deleterious aging phenomena such as the rapid accumulation of damage at the cellular level, while the early loss of flight capacity and low metabolic rates in the no-flight group demonstrate that disuse effects can also significantly alter senescence patterns of whole-insect performance.

Section: Research Articlementioning

confidence: 99%

The effects of age and lifetime flight behavior on flight capacity inDrosophila melanogaster

Frankino

Elekonich

Roberts

2014

“…Nevertheless, animals with damaged, asymmetric wings are able to maintain flight stability and perform complex manoeuvres (Haas and Cartar, 2008). Here we investigate the biomechanical and neuromuscular means by which flying animals compensate for asymmetrically damaged wings and maintain flight stability, building on prior investigation of the causes and effects of wing damage (Foster and Cartar, 2011a;Foster and Cartar, 2011b;Hedenström et al, 2001;Higginson and Barnard, 2004;Rodd et al, 1980).…”

Section: Introductionmentioning

confidence: 99%

Neuromuscular and biomechanical compensation for wing asymmetry in insect hovering flight

Fernández

Springthorpe

Hedrick

2012

SUMMARYWing damage is common in flying insects and has been studied using a variety of approaches to assess its biomechanical and fitness consequences. Results of these studies range from strong to nil effect among the variety of species, fitness measurements and damage modes studied, suggesting that not all damage modes are equal and that insects may be well adapted to compensate for some types of damage. Here, we examine the biomechanical and neuromuscular means by which flying insects compensate for asymmetric wing damage, which is expected to produce asymmetric flight forces and torques and thus destabilize the animal in addition to reducing its total wing size. We measured the kinematic and neuromuscular responses of hawkmoths (Manduca sexta) hovering in free flight with asymmetrically damaged wings via high-speed videography and extracellular neuromuscular activity recordings. The animals responded to asymmetric wing damage with asymmetric changes to wing stroke amplitude sufficient to restore symmetry in lift production. These asymmetries in stroke amplitude were significantly correlated with bilateral asymmetries in the timing of activation of the dorsal ventral muscle among and within trials. Correspondingly, the magnitude of wing asymmetry was significantly, although non-linearly, correlated with the magnitude of the neuromuscular response among individuals. The strongly non-linear nature of the relationship suggests that active neural compensation for asymmetric wing damage may only be necessary above a threshold (>12% asymmetry in wing second moment of area in this case) below which passive mechanisms may be adequate to maintain flight stability. Supplementary material available online at

“…While foraging on these plant species, bees have the option of walking along the inflorescences of an individual plant rather than flying. In contrast, bees foraging on more dispersed inflorescences, such as those of sticky purple geranium (Geranium viscosissimum), tall larkspur (Delphinium glaucum) or fireweed (Chamerion angustifolium), must use costly flight to reach the next flower on an inflorescence or another inflorescence (Foster and Cartar, 2011). Bumble bees also may forage on plant species that influence how often they must initiate flights within a given period.…”

Section: Introductionmentioning

confidence: 99%

“…Many studies have used wing wear to estimate relative insect age (Mueller and Wolf-Mueller, 1993;Kemp, 2000;Burkhard et al, 2002;Richards, 2003;Inoue and Endo, 2006;Peixoto and Benson, 2008). Wing wear has consequences, which include increased wingbeat frequency (Hargrove, 1975;Kingsolver, 1999;Hedenstrom et al, 2001), changed flight speed (Fischer and Kutsch, 2002), changed flight performance (Haas and Cartar, 2008;Jantzen and Eisner, 2008;Combes et al, 2010), changed foraging behaviour (Higginson and Barnard, 2004;Foster and Cartar, 2011) and increased risk of mortality (Cartar, 1992).…”

mentioning

confidence: 99%

What causes wing wear in foraging bumble bees?

Foster

Cartar

2011

Self Cite

Organisms undergo wear and tear of their bodies as they age, as illustrated by tooth erosion, hearing loss, appendage loss and ovipositor wear (reviewed by Finch, 1990;Lalonde and Mangel, 1994). An example common to many flying insects is wing wear. Insects have no mechanism to repair damage to their wings; therefore, as an insect ages and continues to use its wings, the amount of wing wear is cumulative and progressive (Alcock, 1996;Eltz et al., 1999;Hayes and Wall, 1999;Burkhard et al., 2002;Higginson and Barnard, 2004;Lopez-Uribe et al., 2008). Many studies have used wing wear to estimate relative insect age (Mueller and Wolf-Mueller, 1993;Kemp, 2000;Burkhard et al., 2002;Richards, 2003;Inoue and Endo, 2006;Peixoto and Benson, 2008). Wing wear has consequences, which include increased wingbeat frequency (Hargrove, 1975;Kingsolver, 1999;Hedenstrom et al., 2001), changed flight speed (Fischer and Kutsch, 2002), changed flight performance (Haas and Cartar, 2008;Jantzen and Eisner, 2008;Combes et al., 2010), changed foraging behaviour (Higginson and Barnard, 2004;Foster and Cartar, 2011) and increased risk of mortality (Cartar, 1992).Many eusocial insects, particularly bees and wasps, rely on their wings to defend their nest from predators (Breed et al., 1990;Kastberger et al., 2009), maintain colony temperature and assure proper larval development (Heinrich, 1979a;O'Donnell and Foster, 2001), and acquire food for themselves and their colony (Heinrich, 1979a). Providing protection, care and food for the colony's young are the ways in which a non-reproductive forager increases its inclusive fitness. Therefore, wing wear may have important consequences for both individual and colony fitness.Risk of mortality in worker bumble bees (Bombus spp.) increases with age (Brian, 1952;Garofalo, 1978;Rodd et al., 1980;Goldblatt and Fell, 1987;Smeets and Duchateau, 2003), as it does in honey bees (Apis mellifera) (Dukas, 2008). Wing wear has been speculated to lead to an increased risk of mortality in honey bee drones (Rueppell et al., 2005) and tsetse flies (Glossina morsitans) (Allsopp, 1985). Bumble bees that either were wing-clipped or had high naturally occurring amounts of wear died earlier than did those with more pristine wings (Cartar, 1992). An increase in mortality risk with wing wear could result from a number of factors, all of which are supported only by speculation: decreased manoeuvrability, making it more difficult for a bee to escape from predators or severe weather conditions (Rodd et al., 1980), increased energy expenditure (Cartar, 1992) (but see Hedenstrom et al., 2001) and/or increased wingbeat frequency, which matters if the number of wingbeats is limited over a lifespan (Higginson and Gilbert, 2004). Regardless of how wing wear is linked with lifespan, the causes of wing wear have yet to be formally investigated in any insect.Wing wear is associated with male intra-sexual competition (Alcock, 1996), mating attempts (Ragland and Sohal, 1973), failed predator attacks (Robbins, 1981) and foraging activity...