Abstract
A growing number of studies have examined insect survival times during exposure to severe hypoxia and anoxia. Ecologically, terrestrial insects can be exposed to these conditions during immersion from terrestrial flooding, from encasement in ice during winter periods, and as a result of specialization to feed in decomposing material, or as internal parasites of vertebrates. Severe hypoxia has also been tested against a multitude of stored product and museum pests as an alternative to chemical treatment. Finally, severe hypoxia has been induced experimentally to examine physiological responses of a few model species. Together, these experiments have revealed a surprising tolerance of insects to severe hypoxia ranging from hours to weeks. In some cases, ecological studies have revealed apparent adaptation to flooding frequency and duration, while in other cases, the patterns of survival do not appear to correspond with likely abiotic challenges. This chapter seeks to summarize the body of experimental work on insects in hypoxia and to serve as a frame of reference for future experiments aimed at elucidating the adaptive significance of anoxia tolerance by members of the most diverse, ecologically important, and physiologically varied animals on the planet.
This is a preview of subscription content, log in via an institution.
Buying options
Tax calculation will be finalised at checkout
Purchases are for personal use only
Learn about institutional subscriptionsReferences
Anderson JF, Ultsch GR (1987) Respiratory gas concentration in the microhabitats of some Florida arthropods. Comp Biochem and Phys 88:585–588
Bailey SW, Banks FJ (1980) A review of the recent studies of the effect of controlled atmosphere on stored-product pests. In: Shejbal J (ed) Controlled atmosphere storage of grains. Elsevier Scientific Publishing Co, Amsterdam
Banks HJ, Annis PC (1977) Suggested procedures for controlled atmosphere storage of dry grain CSIRO. Aust Div Entomol Tech Pap 13
Baumgartl H, Kritzler K, Zimelka W, Zinkler D (1994) Local Po2 measurements in the environment of submerged soil microarthropods. Acta Oecologia 15:781–789
Block W, Sømme L (1983) Low temperature adaptations in beetles from the sub-Antarctic island of South Georgia. Polar Biol 2:109–114
Bradley TJ (2000) The discontinuous gas exchange cycle in insects may serve to reduce oxygen supply to the tissues. Am Zool 40:952
Brust ML, Hoback WW (2009) Hypoxia tolerance in adult and larval Cicindela tiger beetles varies by life history but not habitat association. Ann Entomol Soc Am 102:462–466
Brust ML, Hoback WW, Skinner KM, Knisley CB (2005) Differential immersion survival by populations of Cicindela hirticollis Say (Coleoptera: Cicindelidae). Ann Entomol Soc Am 98:973–979
Brust ML, Hoback WW, Wright RJ (2007) Immersion tolerance in rangeland grasshoppers (Orthoptera: Acrididae). J Orthop Res 16:135–138
Centanin L, Gorr TA, Wappner P (2010) Tracheal remodeling in response to hypoxia. J Insect Physiol 56:447–454
Chapman RF (1982) The insects structure and function. Harvard University Press, Cambridge
Chefurka W (1965) Some comparative aspects of the metabolism of carbohydrates in insects. Annu Rev Entomol 10:345–382
Chen Q, Haddad GG (2004) Role of trehalose phosphate synthase and trehalose during hypoxia: from flies to mammals. J Exp Biol 207:3125–3129
Chown SL, Holter P (2000) Discontinuous gas exchange cycles in Aphodius fossor (Scarabaeidae): a test of hypotheses concerning the origins and mechanisms. J Exp Biol 203:397–403
Chown SL, Nicholson SW (2004) Insect physiological ecology. Oxford University Press, New York
Chown SL, Gibbs AG, Hetz SK, Klok CJ, Lighton JRB, Marias E (2006) Discontinuous gas exchange in insects: a clarification of hypotheses and approaches. Physiol Biochem Zool 79:333–343
Conradi-Larsen E-M, Sømme L (1973) Anaerobiosis in the overwintering beetle Pelophila borealis. Nature 245:388–390
Contreras HL, Bradley TJ (2009) Metabolic rate controls respiratory pattern in insects. J Exp Biol 212:424–428
Dawson-Scully K, Bukvic D, Chakborty-Chatterjee M, Ferreira R, Milton SL, Sokolowski MB (2010) Controlling anoxic tolerance in adult Drosophila via the cGMP-PKG pathway. J Exp Biol 213:2410–2416
Delate KM, Armstrong JW, Jones VP (1994) Postharvest control treatments for Hypothenemus obscures (F.) (Coleoptera: Scolytidae) in Macadamia nuts. J Econ Entomol 87:120–126
der Geest V (2007) Behavioral responses of caddisfly larvae (Hydropsyche angustipennis) to hypoxia. Contrib Zool 76:255–260
Donahaye E (1990) Laboratory selection of resistance by the red flour beetle, Tribolium castaneum (Herbst), to an atmosphere of low oxygen concentration. Phytoparasitica 18:189–202
Foster WA, Treherne JE (1976) The effects of tidal submergence on an intertidal aphid, Pemphigus trehernei Foster. J Anim Ecol 45:291–301
Gallon C, Hare L, Tessier A (2008) Surviving in anoxic surroundings: how burrowing aquatic insects create an oxic microenvironment. J N Am Benthol Soc 27:570–580
Gaufin AR (1973) Water quality requirements of aquatic insects. EPA 660/3-73-004. United States Environmental Protection Agency, Corvallis, 86 pp
Gilberg M (1989) Inert atmosphere fumigation of museum objects. Stud Conserv 34:30–34
Gilberg M (1991) The effects of low oxygen atmospheres on museum pests. Stud Conserv 36:93–98
Greenlee KJ, Harrison JF (1998) Acid-base and respiratory responses to hypoxia in the grasshopper Shistocerca americana. J Exp Biol 210:2843–2855
Grieshaber MK, Hardewig I, Kreutzer U, Portner H-O (1994) Physiological and metabolic responses to hypoxia in invertebrates. Rev Physiol Biochem Pharmacol 125:43–147
Hamilton J (1885) Hibernation of the Coleoptera. Can Entomol 17:35–38
Harrison J, Frazier MR, Henry JR, Kaiser A, Klok CJ, Rascón B (2006) Responses of terrestrial insects to hypoxia or hyperoxia. Respir Physiol Neurobiol 154:4–17
Held DW, Potter DA, Gates BS, Anderson RG (2001) Modified atmosphere treatments as a potential disinfestations technique for arthropod pests in greenhouses. J Econ Entomol 94:430–438
Heslop JP, Price GM, Ray JW (1963) Anaerobic metabolism in the housefly, Musca domestica L. Biochem J 87:35–38
Hetz SK, Bradley TJ (2005) Insects breathe discontinuously to avoid oxygen toxicity. Nature 433:516–519
Hoback WW, Stanley DW (2001) Insects in hypoxia. J Insect Physiol 47:533–542
Hoback WW, Higley LG, Stanley DW, Barnhart MC (1998) Survival of immersion and anoxia by larval tiger beetles, Cicindela togata. Am Midl Nat 140:27–33
Hoback WW, Podrabsky JE, Higley LG, Stanley DW, Hand SC (2000) Anoxia tolerance of con-familial tiger beetle larvae is associated with differences in energy flow and anaerobiosis. J Comp Physiol B 170:307–314
Hoback WW, Clark TL, Meinke LJ, Higley LG, Scalzitti JM (2002) Immersion survival differs among three Diabrotica species. Entomol Exp Appl 105:29–34
Hochachka PW, Nener JC, Hoar J, Saurez RK (1993) Disconnecting metabolism from adenylate control during extreme oxygen limitation. Can J Zool 71:1267–1270
Hodkinson ID, Bird JB (2004) Anoxia tolerance in high arctic terrestrial microarthropods. Ecol Entomol 29:506–509
Holter P (1991) Concentrations of oxygen, carbon dioxide and methane in the air within dung pats. Pedobiolgica 35:381–386
Holter P, Spangenberg A (1997) Oxygen uptake in coprophilous beetles (Aphodius, Geotrupes, Sphaeridium) at low oxygen and high carbon dioxide concentrations. Physiol Entomol 22:339–343
Jayas DS, Jeyamkondan S (2002) Modified atmosphere storage of grains meats fruits and vegetables. Biosyst Eng 82:235–251
Joanisse DR, Storey KB (1998) Oxidative stress and antioxidants in stress recovery of cold-hardy insects. Insect Biochem Mol Biol 28:23–30
Knipling GD, Sullivan WN, Fulton RA (1961) The survival of several species of insects in a nitrogen atmosphere. J Econ Ent 54:1054–1055
Kölsch G (2001) Anoxia tolerance and anaerobic metabolism in two tropical weevil species (Coleoptera, Curculionidae). J Comp Physiol B 171:595–602
Kölsch G, Jakobi K, Wegener G, Braune HJ (2002) Energy metabolism and metabolic rate of the alder leaf beetle Agelastica alni (L.) (Coleoptera, Chrysomelidae) under aerobic and anaerobic conditions: a micorcalorimetric study. J Insect Physiol 48:143–151
Krafsur ES, Graham CL (1970) Spiracular responses of Aedes mosquitoes to carbon dioxide and oxygen. Ann Entomol Soc Am 63:691–696
Krishnan SN, Sun YA, Mohsenin A, Wyman RJ, Haddad GG (1997) Behavioral and electrophysiological responses of Drosophila melanogaster to prolonged periods of anoxia. J Insect Physiol 43:203–210
Leinaas HP, Sømme L (1984) Adaptations in Xenylla maritima and Anurophorus laricis (Collembola) to lichen habitats on alpine rocks. Oikos 43:197–206
Levenbook L (1950) The effect of carbon dioxide and certain respiratory inhibitors on the respiration of larvae of the horse bot fly (Gastrophilus intestinalis De Geer). J Exp Biol 28:181–202
Lighton JRB (1996) Discontinuous gas exchange in insects. Annu Rev Entomol 41:309–324
Lighton JRB (2007) Respiratory biology: why insects evolved discontinuous gas exchange. Curr Biol 17:645–647
Ma E, Xu T, Haddad GG (1999) Gene regulation by O2 deprivation: an anoxia-regulated novel gene in Drosophila melanogaster. Brain Res Mol Brain Res 63:217–224
Mani MS (1968) Ecology and biogeography of high altitude insects. W.S. Junk N.V. Publishers, Belinfante, 527 pp
Marais E, Klok CJ, Terblanch JS, Chown SL (2005) Insect gas exchange patterns: a phylogenetic perspective. J Exp Biol 14:470–472
Mathews PG, White CR (2011) Discontinuous gas exchange in insects: is it all in their heads? Am Nat 177:130–134
Meidell EM (1983) Diapause, aerobic and anaerobic metabolism in alpine adult Melasoma collaris (Coleoptera). Oikos 41:239–244
Meyer SGE (1977) Concentrations of some glycolytic and other intermediates in larvae of Callitroga macellaria (F.) (Diptera, Calliphoridae) during anaerobiosis. Comp Biochem Physiol B 58:49–55
Miller MF, Labandeira CC (2002) Slow crawl across the salinity divide: delayed colonization of freshwater ecosystems by invertebrates. GSA Today 12:4–10
Nagell B (1977) Survival of Cloeon dipterum (Ephemeroptera) larvae under anoxic conditions in winter. Oikos 29:161–165
Nagell B, Fagerstrom T (1978) Adaptations and resistance to anoxia in Cloeon dipterum (Ephemeroptera) and Nemoura cinera (Plecoptera). Oikos 30:95–99
Nagell B, Landahl C-C (1978) Resistance to anoxia of Chironomus plumosus and Chironomus anthracinus (Diptera) larvae. Holarct Ecol 1:333–336
Nielsen MG (1997) Nesting biology of the mangrove mud-nesting ant Polyrhachis sokolova Forel (Hymenoptera, Formicidae) in northern Australia. Insectes Sociaux 44:15–21
Nielsen MG, Christian KA (2007) The mangrove ant, Camponotus andersoni, switches to anaerobic respiration in response to elevated CO2 levels. J Insect Physiol 53:505–508
Paim U, Beckel WE (1964) Effects of environmental gases on the motility and survival of larvae and pupae of Orthosoma brunnem (Forster) (Col. Cerambycidae). Can J Zool 42:59–69
Quinlan MC, Gibbs AG (2006) Discontinuous gas exchange in terrestrial insects. Respir Physiol Neurobiol 154:18–29
Redecker B, Zebe E (1988) Anaerobic metabolism in aquatic insect larvae: studies on Chironomus thummi and Culex pipiens. J Comp Physiol B 158:307–315
Rosenberg DM, Resh VH (eds) (1993) Freshwater biomonitoring and benthic macroinvertebrates. Chapman & Hall, New York, 488 pp
Rust M, Kennedy J (1993) The feasibility of using modified atmospheres to control insect pests in museums. Internal report, The Getty Conservation Institute Scientific Program, Marina del Rey
Schmidt-Nielson K (1990) Animal physiology: adaptation and environment, 4th edn. Cambridge University Press, New York, 602 pp
Soderstrom EL, Brandl DG, Mackey B (1990) Responses of codling moth (Lepidoptera: Tortricidae) life stages to high carbon dioxide or low oxygen atmospheres. J Econ Entomol 83:472–475
Sømme L (1974) Anaerobiosis in some alpine Coleoptera. Norsk Entomol Tidskr 21:155–158
Sømme L (1979) Overwintering ecology of alpine Collembola and oribatid mites from the Austrian Alps. Ecol Entomol 4:175–180
Sømme L, Block W (1982) Cold hardiness of Collembola at Signy Island, maritime Antarctic. Oikos 38:168–176
Sømme L, Conradi-Larsen E-M (1977) Anaerobiosis in overwintering collembolans and oribatid mites from windswept mountain ridges. Oikos 29:127–132
Storey KB, Storey JM (1992) Biochemical adaptations for winter survival in insects. In: Steponkus PL (ed) Advances in low-temperature biology, vol 1. JAI Press, London, pp 101–140
Teixeria LAF, Averill AL (2006) Evaluation of flooding for cultural control of Sparganothis sulfureana (Lepidoptera: Torticidae) in cranberry bogs. Environ Entomol 35:670–675
Valentin N (1993) Comparative analysis of insect control by nitrogen, argon, and carbon dioxide in museum, archive, and herbarium collections. Int Biodeterior Biodegrad 32:263–278
Valentin N, Preusser FD (1990) Insect control by inert gases in museums, museum archives, and museum collections. Restaurator 11:22–33
Wang F, Tessier A, Hare L (2001) Oxygen measurements in the burrows of freshwater insects. Freshwater Biol 46:317–327
Ward P, Labandeira C, Laurin M, Berner RA (2006) Confirmation of Romer’s Gap as a low oxygen interval constraining the timing of initial arthropod and vertebrate terrestrialization. Proc Natl Acad Sci U S A 103:16818–16822
Wegener G (1993) Hypoxia and post hypoxic recovery in insects: physiological and metabolic aspects. In: Hochachaka PW, Lutz PL, Rosenthal M, Sick T, van den Thillart G (eds) Surviving hypoxia – mechanisms of control and adaptation. CRC Press, Boca Raton, pp 417–432
Westneat MW, Belz O, Blob RW, Fezzaa K, Cooper WJ, Lee W-K (2003) Tracheal respiration in insects visualized with synchrotron x-ray imaging. Science 299:558–560
White CR, Blackburn TM, Terblanche JS, Marias E, Gibernau M, Chown SL (2007) Evolutionary responses of discontinuous gas exchange in insects. Proc Natl Acad Sci U S A 104:8357–8361
Williams AA, Rose MR, Bradley TJ (1997) CO2 release patters in Drosophila melanogaster: the effect of selection for desiccation resistance. J Exp Biol 200:615–624
Wingrove JA, O’Farrell PH (1999) Nitric oxide contributes to behavioral, cellular, and developmental responses to low oxygen in Drosophila. Cell 98:105–114
Wyatt TD (1986) How a subsocial intertidal beetle, Bledius spectabilis, prevents flooding and anoxia in its burrow. Behav Ecol Sociobiol 19:323–331
Zerm M, Adis J (2003) Exceptional anoxia resistance in larval tiger beetle, Phaeoxantha klugii (Coleoptera: Cicindelidae). Physiol Entomol 28:150–153
Zerm M, Walenciak O, Val AL, Adis J (2004a) Evidence for anaerobic metabolism in the larval tiger beetle, Phaeoxantha klugii (Col. Cicindelidae) from a central Amazonian floodplain (Brazil). Physiol Entomol 29:483–488
Zerm M, Zinkler D, Adis J (2004b) Oxygen uptake and local PO2 profiles of submerged larvae of Phaexantha klugii (Coleoptera: Cicindelidae), as well as their metabolic rate in air. Physiol Biochem Zool 77:378–389
Zinkler D, Russbeck R (1986) Ecolophysiological adaptations of collembolan to low oxygen concentrations. In: Dallai R (ed) International Seminar on Apterygota. University of Siena, Siena, pp 123–127
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2012 Springer Science+Business Media B.V.
About this chapter
Cite this chapter
Hoback, W.W. (2012). Ecological and Experimental Exposure of Insects to Anoxia Reveals Surprising Tolerance. In: Altenbach, A., Bernhard, J., Seckbach, J. (eds) Anoxia. Cellular Origin, Life in Extreme Habitats and Astrobiology, vol 21. Springer, Dordrecht. https://doi.org/10.1007/978-94-007-1896-8_10
Download citation
DOI: https://doi.org/10.1007/978-94-007-1896-8_10
Published:
Publisher Name: Springer, Dordrecht
Print ISBN: 978-94-007-1895-1
Online ISBN: 978-94-007-1896-8
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)