Differences in the aerobic capacity of flight muscles between butterfly populations and species with dissimilar flight abilities

Abstract

Habitat loss and climate change are rapidly converting natural habitats and thereby increasing the significance of dispersal capacity for vulnerable species. Flight is necessary for dispersal in many insects, and differences in dispersal capacity may reflect dissimilarities in flight muscle aerobic capacity. In a large metapopulation of the Glanville fritillary butterfly in the Åland Islands in Finland, adults disperse frequently between small local populations. Individuals found in newly established populations have higher flight metabolic rates and field-measured dispersal distances than butterflies in old populations. To assess possible differences in flight muscle aerobic capacity among Glanville fritillary populations, enzyme activities and tissue concentrations of the mitochondrial protein Cytochrome-c Oxidase (CytOx) were measured and compared with four other species of Nymphalid butterflies. Flight muscle structure and mitochondrial density were also examined in the Glanville fritillary and a long-distance migrant, the red admiral. Glanville fritillaries from new populations had significantly higher aerobic capacities than individuals from old populations. Comparing the different species, strong-flying butterfly species had higher flight muscle CytOx content and enzymatic activity than short-distance fliers, and mitochondria were larger and more numerous in the flight muscle of the red admiral than the Glanville fritillary. These results suggest that superior dispersal capacity of butterflies in new populations of the Glanville fritillary is due in part to greater aerobic capacity, though this species has a low aerobic capacity in general when compared with known strong fliers. Low aerobic capacity may limit dispersal ability of the Glanville fritillary.

Figure 1. Reduced minus oxidized difference spectrum of a butterfly thorax preparation.

Optical spectra of the flight muscle homogenate were collected in the ferricyanide oxidized and the dithionite reduced states. The difference spectrum has clear peaks at 550, 560 and 605c, b and a, respectively. This method allows highly accurate determination of tissue concentrations of the respiratory protein CytOx (also known as cytochrome aa₃ or Complex IV).

Figure 2. CytOx activity (A) and concentration (B) in flight muscles of Glanville fritillaries originating from old and new local populations.

Results are shown for individuals from old (open symbols; n = 15 males, 13 females) and new populations (filled symbols; n = 19 males, 24 females), plotted against thorax wet mass. Mean CytOx activities and concentrations are shown as horizontal lines (solid lines, new populations; dashed lines, old populations). Statistics in text.

Figure 3. CytOx activity (A) and concentration (B) in flight muscles of five butterfly species with dissimilar flight behaviours.

Means (±SE) of CytOx activity (A) and concentration (B) for five species of butterfly, two short-distance fliers (open bars; Ringlet Aphantopus hyperantus n = 5; Glanville fritillary M. cinxia n = 71), and three strong fliers (shaded bars; Small Tortoiseshell Aglais urticae n = 5; High Brown fritillary Argynnis adippe n = 5; Red Admiral Vanessa atalanta, n = 15). Letters denote differences between species (Tukey's HSD). Statistics in text.

Figure 4. Mitochondrial structure and density in the flight muscles of two butterfly species with dissimilar flight behaviours.

(A) Microscopic images of flight muscle of the Glanville fritillary (a, c) and the Red Admiral (b, d). Mitochondria (m and arrows), sarcoplasmic reticulum (s) and myofibrils (my) are indicated. Bars are 500 nm in a and b, 1 µm in c and d. (B) Distribution of mitochondrial profiles from thin sections of the flight muscle.