Butterfly flight activity affects reproductive performance and longevity relative to landscape structure

Abstract

Due to an overlap in the resources used by the flight muscles with the resources used during egg production, it has been hypothesised that an increased dispersal in fragmented landscapes may result in a physiological trade-off between flight and reproduction. In a common garden experiment, we investigated the effects of increased flight on the reproductive output of female speckled wood butterflies (Pararge aegeria, L.) from closed continuous woodland populations versus open highly fragmented agricultural landscapes in central France. Our flight treatment significantly affected resource allocation to egg size, but had no effect on mean daily fecundity. This treatment effect was similar for females from the two landscapes of origin, and suggests that energetic costs associated with increased flight result in a decrease in resource allocation to egg provisioning. There was a landscape-specific effect of flight on longevity: flight reduced longevity by 21% in woodland females, but had no affect on agricultural females. This result suggests that woodland landscape females further compensate for excessive flight by redirecting resources away from somatic maintenance, resulting in reduced life spans. Our results strongly indicate that increased flight caused by changes in landscape structure may impact on key life history traits such as reproductive success and longevity.

A long life in the fast lane: positive association between peak metabolic rate and lifespan in a butterfly

“…In contrast, exercise has been reported to have increased lifespan in mice (Chigurupati et al, 2008). In a butterfly, experimental flight treatments shortened lifespan in some populations but the effect was absent in populations that were adapted to frequent flight due to landscape structure (Gibbs and Van Dyck, 2010). In another butterfly, experiment flight treatments alone did not affect lifespan, unless coupled with starvation at the larval stage.…”

“…While houseflies and fruit flies can show a simple relationship between flight and longevity (Sohal and Buchan, 1981;Magwere et al, 2006), experimental work has shown that the effect of forced flight on butterfly longevity is far from uniform. Depending on the population of origin (Gibbs and Van Dyck, 2010) or the conditions experienced during development (Saastamoinen et al, 2010), butterflies may be seemingly immune to negative effects of flight on lifespan. It is also worth pointing out that we examined in our experiments existing individual variation in metabolic rate.…”

“…The study of ageing may benefit from more attention on how resources are allocated among different processes (Boggs, 2009). This is particularly relevant while trying to understand how lifespan is affected by stressful conditions when resources are scarce (Gibbs and Van Dyck, 2010;Saastamoinen et al, 2010).…”

Thermal biology of flight in a butterfly: genotype, flight metabolism, and environmental conditions

“…Butterflies are especially dependent on flight for most activities during adult life, including foraging, escaping predation, locating mates, searching for host plants, and dispersal (Kingsolver 1983; Saastamoinen and Hanski 2008; Niitepõld et al. 2009; Gibbs 2010). However, insect flight is energetically very costly, and thoracic muscles of flying insects exhibit the highest rates of metabolism known for any locomotor tissue (Dudley 2000; Suarez 2000), exceeding metabolism at rest by up to two orders of magnitude (Kammer and Heinrich 1978).…”

Selecting for invasive tendencies: the evolution of morphological, physiological, and movement behaviour traits associated with dispersal

“…Two general ideas that have empirical support are that: 1) dispersal trades off with reproduction directly; and 2) dispersal does not trade off with reproduction (coloniser strategy). Dispersal trade-offs occur when dispersers have a low reproductive value because of either the energetic cost of dispersal itself, or the delay of reproduction due to the time cost of dispersal (Ziegler 1976;Hughes et al 2003;Gibbs & Van Dyck 2010;Rousset 2012). In residents, the absence of dispersal costs should increase resources that are available for reproductive investment; therefore, residents have a higher reproductive value (Riddle & Dawson 1983;Gu et al 2006;Pärn et al 2009).…”