Do respiratory limitations affect metabolism of insect larvae before moulting: an empirical test at the individual level

Abstract

Recent data suggest that oxygen limitation may induce moulting in larval insects. This oxygen-dependent induction of moulting (ODIM) hypothesis stems from the fact that the tracheal respiratory system of insects grows primarily at moults, whereas tissue mass increases massively between moults. This may result in a mismatch between oxygen supply and demand at the end of each larval instar because oxygen demand of growing tissues exceeds the relatively fixed supply capacity of the respiratory system. The ODIM hypothesis predicts that, within larval instars, respiration and metabolic rates of an individual larva first increase with increasing body mass but eventually level off once the supply capacity of the tracheal system starts to constrain metabolism. Here, we provide the first individuallevel test of this key prediction of the ODIM hypothesis. We use a novel methodology where we repeatedly measure respiration and metabolic rates throughout the penultimate-and final-instar larvae in the butterfly Pieris napi. In the penultimate instar, respiration and metabolic rates gradually decelerated along with growth, supporting the ODIM hypothesis. However, respiration and metabolic rates increased linearly during growth in the final instar, contradicting the prediction. Moreover, our data suggest considerable variation among individuals in the association between respiration rate and mass in the final instar. Overall, the results provide partial support for the ODIM hypothesis and suggest that oxygen limitation may emerge gradually within a larval instar. The results also suggest that there may be different moult induction mechanisms in larva-to-larva moults compared with the final metamorphic moult.

The consequences of daily cyclic hypoxia on a European grass shrimp: From short‐term responses to long‐term effects

“…see Abehsera et al., ; Tom et al., ). The increased expression of cuticular contigs after 7‐day exposure suggested that cyclic hypoxia might exert an effect on the moult cycle of P. varians , similarly to that reported for insect larvae reared in hypoxia (Kivelä et al., ). This conclusion was supported by the upregulation of PMP, CaAP and DD5 genes, markers highly expressed during postmoult phase in crustaceans (Ikeya et al., ; Inoue, ; Roer et al., ).…”

“…In arthropods, the respiratory system grows primarily at moults because it is covered by the rigid exoskeleton (Lundquist, Kittilson, Ahsan, & Greenlee, 2017), whereas tissue mass increases between moults (and so does oxygen demand) (Kivelä, Lehmann, & Gotthard, 2016). In hypoxic conditions, a mismatch between oxygen supply and oxygen demand can develop (Massabuau & Abele, 2012).…”

How to become larger: ontogenetic basis of among‐population size differences in a moth

“…In particular, it appears that larger size cannot be attained by a major modification of growth patterns within one single instar, such a difference has to be accumulated in the course of several instars. Recent studies have suggested that oxygen limitation may constitute the proximate basis of the constraint on within‐instar mass increment (Greenlee & Harrison, ; Callier & Nijhout, ; Kivelä et al., ,b).…”

Developmental plasticity in metabolism but not in energy reserve accumulation in a seasonally polyphenic butterfly

“…The number of faecal pellets produced during the measurement was recorded to take into account potential variation in the digestive cycle and CO 2 released from the faeces. We did not measure movement of larvae during measurements as a previous study using a similar setup showed that larvae move little in the tubes and, in that study, the movement effect was either statistically insignificant or very small (Kivelä et al, 2016b).…”

“…In P. napi , diapause pupae contain more storage lipids than pupae that develop directly into adult six days after pupation, lipidomes and metabolomes differing between the developmental pathways in the same phase of pupal development as well (Lehmann et al, 2016, 2018). It remains unknown if these differences appear already in the larval stage during which lipid reserves are accumulated in P. napi (Kivelä et al, 2016b) and many other insects (Tauber et al, 1986; Hahn and Denlinger, 2007, 2011). Interestingly, however, metabolic rate and metabolome are similar in diapausing and directly developing P. napi pupae right after pupation (Lehmann et al, 2016, 2018).…”