Respiratory changes throughout ontogeny in the tobacco hornworm caterpillar,Manduca sexta

Abstract

SUMMARY The respiratory system of growing caterpillars is challenged in two distinct ways as they develop from hatchlings to fifth instars preparing for pupation. First, across instars, body sizes and tracheal lengths increase substantially. Second, within each instar, animal mass can more than double while major tracheal respiratory system structures, such as spiracles and large tracheae, are fixed in size until molting. To test whether these growth processes result in a decrease in O2 delivery capacity relative to tissue oxygen needs, we exposed feeding Manduca sexta larvae of various ages to decreasing levels of atmospheric O2 and measured their metabolic rate and ability to feed. We found that near the beginning of all instars, M. sexta were able to maintain gas exchange and feed down to approximately 5 kPa O2, indicating that these insects are able to match tracheal O2 delivery to increased metabolic rates across instars. However, gas exchange and feeding of caterpillars nearing the molt were limited at much higher O2 levels (up to 15 kPa O2), suggesting that caterpillars have limited capacities to increase tracheal O2 delivery as O2 consumption rates increase within instars. It seems possible that the safety margin for O2 delivery may disappear completely in the last hours before ecdysis, providing an ultimate if not proximate explanation for the necessity of molting.

Body size effects on the oxygen-sensitivity of dragonfly flight

“…8). These results suggest that large and small flying dragonflies have similar safety margins for oxygen delivery, which is similar to what has been observed with resting (Greenlee and Harrison, 2004;Greenlee et al, 2007) and hopping grasshoppers (Kirkton et al, 2005), resting beetles (Lease et al, 2012) and feeding caterpillars (Greenlee and Harrison, 2005). The finding that oxygen sensitivity is independent of size during flight is particularly important because the oxygen demand of insects is highest during flight.…”

“…Direct tests of whether the physiological and behavioral functions of larger insects are more sensitive to declining oxygen levels have been negative for resting grasshoppers (Greenlee and Harrison, 2004;Greenlee et al, 2007), hopping grasshoppers (Kirkton et al, 2005), resting beetles (Lease et al, 2012) and feeding caterpillars (Greenlee and Harrison, 2005). However, these prior tests for an increase in oxygen sensitivity with body size can be criticized on the basis that they did not examine insects during high rates of aerobic metabolism when the oxygen delivery system is operating near its maximal capacity.…”

The role of reduced oxygen in the developmental physiology of growth and metamorphosis initiation inDrosophila melanogaster

“…It has been hypothesized that the rising oxygen need combined with partial inflexibility in tracheal morphology could lead to oxygen demand outstripping supply, causing cellular P O2 to decline with time within an instar and trigger molting (Peck and Maddrell, 2005). Consistent with this hypothesis is the observation that late-instar D. melanogaster, Schistocerca americana grasshoppers and M. sexta are more susceptible to hypoxia than early-instar animals (Callier and Nijhout, 2011;Greenlee and Harrison, 2005;Heinrich et al, 2011). Also consistent with this hypothesis is the observation that metabolic rates rise linearly with age before the critical weight in M. sexta, but plateau after the critical weight, consistent with oxygen limitation of metabolism later in the instar (Callier and Nijhout, 2011).…”

Effects of shape variations on the energy metabolism of the sand cricket Gryllus firmus: a geometric morphometric analysis

“…Indeed, one of the most prominent hypotheses explaining the large body sizes of insects in the Paleozoic era is related to the fact that atmospheric oxygen concentration was 35% at that time, supporting the idea that present insect size is limited by the present oxygen concentration (Kirkton, 2007). In fact, many researchers are interested in determining how and when size limitations affect insect respiration and metabolism in present-day insects (Hack, 1997;Davis et al, 1999;Chown and Nicolson, 2004;Hartung et al, 2004;Merrick and Smith, 2004;Greenlee and Harrison, 2005;Harrison et al, 2005;Nespolo et al, 2005;Kirkton, 2007;Nespolo et al, 2008). Given the constraints related to body size in animals with tracheae, it is reasonable to postulate that at larger body sizes, compensatory mechanisms, such as body deformations (Hartung et al, 2004), exist to improve the effi ciency of respiration (Kirkton, 2007).…”