Allometric Scaling of Tracheal Morphology among Bumblebee Sisters (Apidae:Bombus): Compensation for Oxygen Limitation at Large Body Sizes?

Abstract

The scaling of insect respiratory systems with body size has important implications for ecology and evolution of insects, ranging from allometry of aerobic performance to current and past environmental constraints on insect body size. Previous work examining scaling across beetle species and during ontogeny of grasshoppers suggests strong tracheal hypermetry, with larger insects investing relatively more volume in their tracheal systems. However, these approaches potentially confound body size differences with species or life stage differences in morphology or physiology. To circumvent these issues, we took advantage of large body size variation within bumblebee nests. Workers with 75% genetic similarity nevertheless varied in body size from under 50 mg to more than 250 mg, and queens exceeded 500 mg. We estimated respiratory volume, dimensions of pronotal spiracles, and body size of individual bumblebees (Bombus impatiens) from lab-reared nests. Among workers, tracheal system volume scaled hypermetrically with mass(2.6), whereas overall scaling of the cross-sectional area of the pronotal spiracular tracheae scaled isometrically with mass(0.67). Queen bumblebees had tracheal systems similar in size to those of workers 1/3 their body mass but had larger-than-expected cross-sectional area of spiracular tracheae. Given space constraints within the rigid exoskeleton, the strong hypermetry of the tracheal system among bumblebee workers may impose an upper limit to body size as the tracheal system occupied 25% of total body volume for the largest workers.

The Effect of Oxygen Limitation on a Xylophagous Insect’s Heat Tolerance Is Influenced by Life-Stage Through Variation in Aerobic Scope and Respiratory Anatomy

“…This approach assumes no variance in the theoretical slope value but employs the estimated slope and standard error of the empirical data (Zar, 1997). However, while scaling patterns of respiratory structures are expected to vary among tracheated arthropod species, they may also be highly variable across and within stages of the same species due to the discontinuous growth of the tracheal system and, in some cases, complex life histories (e.g., occurrence of diapause) (Helm and Davidowitz, 2013; Vogt and Dillon, 2013; Greenlee et al, 2014). Therefore, no specific allometry model or anatomical scaling hypothesis has been adequately developed yet regarding the scaling relationship of the tracheal volume in this study with body size to test, and we instead sought here to statistically compare the estimated scaling slopes (regression exponents) with other scaling values commonly reported in the literature across a wide range of species (Chown et al, 2007) and between the two main life-stages investigated.…”

Isometric Spiracular Scaling in Scarab Beetles: Implications for Diffusive and Advective Oxygen Transport

“…Comparing tenebrionid beetles inter-specifically, the leg tracheae scale hypermetrically, but the head tracheae scale isometrically (6). Within a bumblebee species, one spiracle scales isometrically (16). In the leg of growing locust ( Schistocerca americana ), the diffusing capacity of the large longitudinal tracheae of the leg scales hypometrically (17), whereas in a growing caterpillar ( Manduca sexta ), diameters of most tracheae scale isometrically (55).…”

“…In contrast, there is relatively limited information on the scaling of gas exchange structures in invertebrates, despite the fact that most animal species are invertebrates (5,14). The scaling of the insect respiratory system is of particular interest, as aspects of tracheal system structure have been reported to scale hypermetrically, in contrast to the isometric or hypometric scaling of respiratory structures in vertebrates, supporting the hypothesis that possession of a tracheal respiratory system limits insect body size (6,(15)(16)(17)(18).…”

Phat queens emerge fashionably late: body size and condition predict timing of spring emergence for queen bumble bees

“…The width between the tegulae (intertegular width, ITW, mm, also termed intertegular span, ITS; Cane, 1987) was measured from photographs by first setting the scale based on the object of known size and then measuring the length of a straight line drawn between the outside edges of the tegula using ImageJ (Rasband, 1997; Schneider et al, 2012). ITW is not affected by variation in feeding or hydration state, so is a reliable estimate of body size of bumble bees (Cane, 1987; Lozier et al, 2021; Vogt & Dillon, 2013). We estimated body condition of queens as the bee mass to ITW ratio (BeeMI).…”

“…To test these predictions, we measured mass and intertegular width (ITW, a measurement of exoskeletal size fixed at eclosion; Cane, 1987; Vogt and Dillon, 2013) of Bombus huntii queens throughout the spring emergence period for two years in Laramie, WY. Queens that weighed less emerged earlier as predicted.…”