Discontinuous gas exchange in Orthoptera – mechanisms and hypotheses

Groenewald, Berlize (2014-12)

Thesis (PhDAgric)--Stellenbosch University, 2014.

Thesis

ENGLISH ABSTRACT: Respiratory and ventilatory dynamics in insects are of fundamental importance to understanding evolved variation in gas exchange patterns, such as the discontinuous gas exchange cycle (DGC). However, the evolutionary origin and maintenance of the DGC in tracheate arthropods are poorly understood and highly controversial. Possible reasons for the occurrence of the DGC include water savings (hygric hypothesis) or the prevention of oxygen toxicity (oxidative damage hypothesis). Research presented in this dissertation aimed to examine the variation or modulation of the discontinuous gas exchange pattern, the environmental factors that potentially drive this relationship, and the competing hypotheses by: 1) examining the relative importance of convection vs diffusion during the DGC; 2) testing the oxidative damage and hygric hypotheses; 3) investigating ventilatory movements over the entire DGC; 4) examining intratracheal pressure patterns; and 5) investigating prioritisation of abiotic factors in the gas exchange control cascade. To accomplish these aims two model species of Orthoptera (Acrididae) which show discontinuous gas exchange cycles (DGCs) were chosen: the desert locust, Schistocerca gregaria, and a grasshopper commonly associated with wetlands, Paracinema tricolor. Firstly, I found that in S. gregaria, there was no clear intratracheal pressure pattern that accompanies the DGC. This shows that the gas exchange dynamics of Orthoptera differ substantially from those of Lepidoptera, in which a distinctive intratracheal pressure pattern accompanies the DGC, highlighting that the Lepidoptera cannot serve as a general model for all insects showing the DGC. Secondly, I found that in P. tricolor, a hierarchy of abiotic factors influence the DGC, rather than only a single hypothesis or factor explaining the occurrence of the DGC. For S. gregaria, gas exchange is most efficient at slightly hypoxic to normoxic conditions. At these conditions, diffusive gas exchange dominates, meaning that no body movements are necessary to aid gas exchange, making this mode of gas exchange less energetically costly than active convection. In conclusion, these results confirm that the maintenance of the DGC is affected by multiple abiotic factors. The findings of this dissertation have significant implications for understanding the mechanistic basis and energetic cost of gas exchange in insects.

AFRIKAANSE OPSOMMING: Asemhalings en ventilasie dinamika in insekte is van fundamentele belang om die ontwikkelde variasie in asemhalingspatrone, soos bv. die diskontinue gaswisseling siklus (DGS), te verstaan. Tog word die evolusionêre oorsprong en instandhouding van die DGS in geleedpotiges wat ‘n trageale asemhalingsisteem besit tans nog nie goed verstaan nie. Moontlike redes vir die voorkoms van die DGS sluit in waterbesparing (waterbesparings hipotese) of die voorkoming van suurstof toksisiteit (oksidatiewe skade hipotese). Navorsing wat in hierdie dissertasie voorgelê word het gemik om die variase en modulasie van die DGS the ondersoek, die omgewingsfaktore wat potensieel hierdie verhouding kan aandryf, asook die kompeterende hipoteses deur: 1) die relatiewe belangrikheid van konveksie teenoor diffusie tydens die DGS te ondersoek; 2) die oksidatiewe skade en waterbesparings hipoteses te ondersoek; 3) ventilasie bewegings tydens die hele DGS te ondersoek; 4) druk patrone in die tragea te ondersoek; en 5) die prioritisering van abiotiese faktore in die gaswisseling hiërargie te ondersoek. Om hierdie doelwitte te bereik is twee model spesies van Orthoptera (Acrididae) wat die DGS toon gekies: die woestyn sprinkaan, Schistocerca gregaria, en ‘n sprinkaan wat algemeen in vleilande voorkom, Paracinema tricolor. Eerstens het ek gevind dat daar geen duidelike patroon in die druk van die tragea van S. gregaria voorkom wat gepaardgaan met die DGS nie. Dit dui daarop dat die gaswisselings dinamika van Orthoptera aansienlik verskil van die van Lepidoptera. In Lepidoptera is daar ‘n duidelike patroon in die druk van die tragea sigbaar wat gepaardgaan met die DGS, wat beklemtoon dat die Lepidoptera nie gebruik kan word as ‘n algemene model vir alle insekte wat die DGS gebruik nie. Tweedens het ek gevind dat eerder as wat slegs ‘n enkele faktor of hipotese die voorkoms van die DGS bepaal, daar ‘n hiërargie van abiotiese faktore is wat die DGS in P. tricolor beïnvloed. Vir S. gregaria is gaswisseling die doeltreffendste by effens hipoksiese tot normoksiese suurstof kondisies. By hierdie kondisies vind gaswisseling hoofsaaklik deur middel van diffusie plaas, wat beteken dat geen liggaams bewegings nodig is om gaswisseling aan te vul nie. Dit maak hierdie vorm van gaswisseling goedkoper (in terme van energie kostes) as aktiewe konveksie. Ten slotte bevestig hierdie resultate dat die voorkoms en modulasie van die DGS beïnvloed word deur verskeie abiotiese faktore. Die bevindings van hierdie dissertasie hou ook belangrike implikasies in vir die begrip van die meganistiese basis en kostes (in terme van energie) van gaswisseling in insekte.

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