Edward P. Snelling

Accelerometry estimates field metabolic rate in giant Australian cuttlefish Sepia apama during breeding

1. Estimating the metabolic rate of animals in nature is central to understanding the physiological, behavioural and evolutionary ecology of animals. Doubly labelled water and heart-rate methods are the most commonly used approaches, but both have limitations that preclude their application to some systems. 2. Accelerometry has emerged as a powerful tool for estimating energy expenditure in a range of animals, but is yet to be used to estimate field metabolic rate in aquatic taxa. We combined two-dimensional accelerometry and swim-tunnel respirometry to estimate patterns of energy expenditure in giant Australian cuttlefish Sepia apama during breeding. 3. Both oxygen consumption rate (Vo2) and swimming speed showed strong positive associations with body acceleration, with coefficients of determination comparable to those using similar accelerometers on terrestrial vertebrates. Despite increased activity during the day, field metabolic rate rarely approached Vo2, and night-time Vo2 was similar to that at rest. 4. These results are consistent with the life-history strategy of this species, which has a poor capacity to exercise anaerobically, and a mating strategy that is visually based. With the logistical difficulties associated with observation in aquatic environments, accelerometry is likely to prove a valuable tool for estimating energy expenditure in aquatic animals.

Symmorphosis and the insect respiratory system: allometric variation

SUMMARY Taylor and Weibels theory of symmorphosis predicts that structures of the respiratory system are matched to maximum functional requirements with minimal excess capacity. We tested this hypothesis in the respiratory system of the migratory locust, Locusta migratoria, by comparing the aerobic capacity of the jumping muscles with the morphology of the oxygen cascade in the hopping legs using an intraspecific allometric analysis of different body mass (Mb) at selected juvenile life stages. The maximum oxygen consumption rate of the hopping muscle during jumping exercise scales as Mb1.02±0.02, which parallels the scaling of mitochondrial volume in the hopping muscle, Mb1.02±0.08, and the total surface area of inner mitochondrial membrane, Mb0.99±0.10. Likewise, at the oxygen supply end of the insect respiratory system, there is congruence between the aerobic capacity of the hopping muscle and the total volume of tracheoles in the hopping muscle, Mb0.99±0.16, the total inner surface area of the tracheoles, Mb0.99±0.16, and the anatomical radial diffusing capacity of the tracheoles, Mb0.99±0.18. Therefore, the principles of symmorphosis are upheld at each step of the oxygen cascade in the respiratory system of the migratory locust.

A test of the oxidative damage hypothesis for discontinuous gas exchange in the locust Locusta migratoria

The discontinuous gas exchange cycle (DGC) is a breathing pattern displayed by many insects, characterized by periodic breath-holding and intermittently low tracheal O2 levels. It has been hypothesized that the adaptive value of DGCs is to reduce oxidative damage, with low tracheal O2 partial pressures (PO2 ∼2–5 kPa) occurring to reduce the production of oxygen free radicals. If this is so, insects displaying DGCs should continue to actively defend a low tracheal PO2 even when breathing higher than atmospheric levels of oxygen (hyperoxia). This behaviour has been observed in moth pupae exposed to ambient PO2 up to 50 kPa. To test this observation in adult insects, we implanted fibre-optic oxygen optodes within the tracheal systems of adult migratory locusts Locusta migratoria exposed to normoxia, hypoxia and hyperoxia. In normoxic and hypoxic atmospheres, the minimum tracheal PO2 that occurred during DGCs varied between 3.4 and 1.2 kPa. In hyperoxia up to 40.5 kPa, the minimum tracheal PO2 achieved during a DGC exceeded 30 kPa, increasing with ambient levels. These results are consistent with a respiratory control mechanism that functions to satisfy O2 requirements by maintaining PO2 above a critical level, not defend against high levels of O2.

Scaling of resting and maximum hopping metabolic rate throughout the life cycle of the locust Locusta migratoria

SUMMARY The hemimetabolous migratory locust Locusta migratoria progresses through five instars to the adult, increasing in size from 0.02 to 0.95 g, a 45-fold change. Hopping locomotion occurs at all life stages and is supported by aerobic metabolism and provision of oxygen through the tracheal system. This allometric study investigates the effect of body mass (Mb) on oxygen consumption rate (, μmol h–1) to establish resting metabolic rate (), maximum metabolic rate during hopping () and maximum metabolic rate of the hopping muscles () in first instar, third instar, fifth instar and adult locusts. Oxygen consumption rates increased throughout development according to the allometric equations , , and, if adults are excluded, and . Increasing body mass by 20–45% with attached weights did not increase mass-specific significantly at any life stage, although mean mass-specific hopping was slightly higher (ca. 8%) when juvenile data were pooled. The allometric exponents for all measures of metabolic rate are much greater than 0.75, and therefore do not support West, Brown and Enquists optimised fractal network model, which predicts that metabolism scales with a ¾-power exponent owing to limitations in the rate at which resources can be transported within the body.

Symmorphosis and the insect respiratory system: a comparison between flight and hopping muscle

SUMMARY Weibel and Taylors theory of symmorphosis predicts that the structural components of the respiratory system are quantitatively adjusted to satisfy, but not exceed, an animals maximum requirement for oxygen. We tested this in the respiratory system of the adult migratory locust Locusta migratoria by comparing the aerobic capacity of hopping and flight muscle with the morphology of the oxygen cascade. Maximum oxygen uptake by flight muscle during tethered flight is 967±76 μmol h−1 g−1 (body mass specific, ±95% confidence interval CI), whereas the hopping muscles consume a maximum of 158±8 μmol h−1 g−1 during jumping. The 6.1-fold difference in aerobic capacity between the two muscles is matched by a 6.4-fold difference in tracheole lumen volume, which is 3.5×108±1.2×108 μm3 g−1 in flight muscle and 5.5×107±1.8×107 μm3 g−1 in the hopping muscles, a 6.4-fold difference in tracheole inner cuticle surface area, which is 3.2×109±1.1×109 μm2 g−1 in flight muscle and 5.0×108±1.7×108 μm2 g−1 in the hopping muscles, and a 6.8-fold difference in tracheole radial diffusing capacity, which is 113±47 μmol kPa−1 h−1 g−1 in flight muscle and 16.7±6.5 μmol kPa−1 h−1 g−1 in the hopping muscles. However, there is little congruence between the 6.1-fold difference in aerobic capacity and the 19.8-fold difference in mitochondrial volume, which is 3.2×1010±3.9×109 μm3 g−1 in flight muscle and only 1.6×109±1.4×108 μm3 g−1 in the hopping muscles. Therefore, symmorphosis is upheld in the design of the tracheal system, but not in relation to the amount of mitochondria, which might be due to other factors operating at the molecular level.

Moulting of insect tracheae captured by light and electron-microscopy in the metathoracic femur of a third instar locust Locusta migratoria

The insect tracheal system is an air-filled branching network of internal tubing that functions to exchange respiratory gases between the tissues and the environment. The light and electron-micrographs presented in this study show tracheae in the process of moulting, captured from the metathoracic hopping femur of a juvenile third instar locust (Locusta migratoria). The images provide evidence for the detachment of the cuticular intima from the tracheal epithelial cells, the presence of moulting fluid between the new and old cuticle layers, and the withdrawal of the shed cuticular lining through larger upstream regions of the tracheal system during moulting. The micrographs also reveal that the cuticular intima of the fine terminal branches of the tracheal system is cast at ecdysis. Therefore, the hypothesis that tracheoles retain their cuticle lining at each moult may not apply to all insect species or developmental stages.

Burrowing energetics of the Giant Burrowing Cockroach Macropanesthia rhinoceros: an allometric study.

Burrowing is an important life strategy for many insects, yet the energetic cost of constructing burrows has never been studied in insects of different sizes. Open flow respirometry was used to determine the allometric scaling of standard metabolic rate (MRS) and burrowing metabolic rate (MRB) in the heaviest extant cockroach species, the Giant Burrowing Cockroach Macropanesthia rhinoceros, at different stages of development. At 10 °C, MRS (mW) scales with body mass (M; g) according to the allometric power equation, MRS=0.158M(0.74), at 20 °C the equation is MRS=0.470M(0.53), and at 30 °C the equation is MRS=1.22M(0.49) (overall Q10=2.23). MRS is much lower in M. rhinoceros compared to other insect species, which is consistent with several aspects of their life history, including flightlessness, extreme longevity (>5 years), burrowing, parental behaviour, and an energy-poor diet (dry eucalypt leaf litter). Energy expenditure during burrowing at 25 °C scales according to MRB=16.9M(0.44), and is approximately 17 times higher than resting rates measured at the same temperature, although the metabolic cost over a lifetime is probably low, because the animal does not burrow to find food. The net cost of transport by burrowing (Jm(-1)) scales according to NCOT=120M(0.49), and reflects the energetically demanding task of burrowing compared to other forms of locomotion. The net cost of excavating the soil (J cm(-3)) is statistically independent of body size.

Scaling of left ventricle cardiomyocyte ultrastructure across development in the kangaroo Macropus fuliginosus

ABSTRACT The heart and left ventricle of the marsupial western grey kangaroo Macropus fuliginosus exhibit biphasic allometric growth, whereby a negative shift in the trajectory of cardiac growth occurs at pouch exit. In this study, we used transmission electron microscopy to examine the scaling of left ventricle cardiomyocyte ultrastructure across development in the western grey kangaroo over a 190-fold body mass range (0.355−67.5 kg). The volume-density (%) of myofibrils, mitochondria, sarcoplasmic reticuli and T-tubules increase significantly during in-pouch growth, such that the absolute volume (ml) of these organelles scales with body mass (Mb; kg) with steep hyperallometry: 1.41Mb1.38, 0.64Mb1.29, 0.066Mb1.45 and 0.035Mb1.87, respectively. Maturation of the left ventricle ultrastructure coincides with pouch vacation, as organelle volume-densities scale independent of body mass across post-pouch development, such that absolute organelle volumes scale in parallel and with relatively shallow hypoallometry: 4.65Mb0.79, 1.75Mb0.77, 0.21Mb0.79 and 0.35Mb0.79, respectively. The steep hyperallometry of organelle volumes and volume-densities across in-pouch growth is consistent with the improved contractile performance of isolated cardiac muscle during fetal development in placental mammals, and is probably critical in augmenting cardiac output to levels necessary for endothermy and independent locomotion in the young kangaroo as it prepares for pouch exit. The shallow hypoallometry of organelle volumes during post-pouch growth suggests a decrease in relative cardiac requirements as body mass increases in free-roaming kangaroos, which is possibly because the energy required for hopping is independent of speed, and the capacity for energy storage during hopping could increase as the kangaroo grows. Summary: Scaling of cardiomyocyte ultrastructure across development of the kangaroo is associated with cellular transformation and improved contractile performance during in-pouch growth followed by a decrease in cardiac development and perfusion requirements during post-pouch growth.

Biphasic Allometry of Cardiac Growth in the Developing Kangaroo Macropus fuliginosus

Interspecific studies of adult mammals show that heart mass (Mh, g) increases in direct proportion to body mass (Mb, kg), such that Mh ∝ Mb1.00. However, intraspecific studies on heart mass in mammals at different stages of development reveal considerable variation between species, Mh ∝ Mb0.70–1.00. Part of this variation may arise as a result of the narrow body size range of growing placental mammals, from birth to adulthood. Marsupial mammals are born relatively small and offer an opportunity to examine the ontogeny of heart mass over a much broader body size range. Data from 29 western grey kangaroos Macropus fuliginosus spanning 800-fold in body mass (0.084–67.5 kg) reveal the exponent for heart mass decreases significantly when the joey leaves the pouch (ca. 5–6 kg body mass). In the pouch, the heart mass of joeys scales with hyperallometry, Mh(in-pouch) = 6.39Mb1.10 ± 0.05, whereas in free-roaming juveniles and adults, heart mass scales with hypoallometry, Mh(postpouch) = 14.2Mb0.77 ± 0.08. Measurements of heart height, width, and depth support this finding. The relatively steep heart growth allometry during in-pouch development is consistent with the increase in relative cardiac demands as joeys develop endothermy and the capacity for hopping locomotion. Once out of the pouch, the exponent decreases sharply, possibly because the energy required for hopping is independent of speed, and the efficiency of energy storage during hopping increases as the kangaroo grows. The right∶left ventricular mass ratios (0.30–0.35) do not change over the body mass range and are similar to those of other mammals, reflecting the principle of Laplace for the heart.

Maximum metabolic rate, relative lift, wingbeat frequency and stroke amplitude during tethered flight in the adult locust Locusta migratoria

SUMMARY Flying insects achieve the highest mass-specific aerobic metabolic rates of all animals. However, few studies attempt to maximise the metabolic cost of flight and so many estimates could be sub-maximal, especially where insects have been tethered. To address this issue, oxygen consumption was measured during tethered flight in adult locusts Locusta migratoria, some of which had a weight attached to each wing (totalling 30–45% of body mass). Mass-specific metabolic rate increased from 28±2 μmol O2 g−1 h−1 at rest to 896±101 μmol O2g−1 h−1 during flight in weighted locusts, and to 1032±69 μmol O2 g−1 h−1 in unweighted locusts. Maximum metabolic rate of locusts during tethered flight (ṀmO2; μmol O2 h−1) increased with body mass (Mb; g) according to the allometric equation ṀmO2=994Mb0.75±0.19, whereas published metabolic rates of moths and orchid bees during hovering free flight (ṀhO2) are approximately 2.8-fold higher, ṀhO2=2767Mb0.72±0.08. The modest flight metabolic rate of locusts is unlikely to be an artefact of individuals failing to exert themselves, because mean maximum lift was not significantly different from that required to support body mass (95±8%), mean wingbeat frequency was 23.7±0.6 Hz, and mean stroke amplitude was 105±5 deg in the forewing and 96±5 deg in the hindwing – all of which are close to free-flight values. Instead, the low cost of flight could reflect the relatively small size and relatively modest anatomical power density of the locust flight motor, which is a likely evolutionary trade-off between flight muscle maintenance costs and aerial performance.