1932

Abstract

Insects can experience functional hypoxia, a situation in which O supply is inadequate to meet oxygen demand. Assessing when functional hypoxia occurs is complex, because responses are graded, age and tissue dependent, and compensatory. Here, we compare information gained from metabolomics and transcriptional approaches and by manipulation of the partial pressure of oxygen. Functional hypoxia produces graded damage, including damaged macromolecules and inflammation. Insects respond by compensatory physiological and morphological changes in the tracheal system, metabolic reorganization, and suppression of activity, feeding, and growth. There is evidence for functional hypoxia in eggs, near the end of juvenile instars, and during molting. Functional hypoxia is more likely in species with lower O availability or transport capacities and when O need is great. Functional hypoxia occurs normally during insect development and is a factor in mediating life-history trade-offs.

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2018-01-07
2024-07-18
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Literature Cited

  1. Apodaca CK, Chapman LJ. 1.  2004. Larval damselflies in extreme environments: behavioral and physiological response to hypoxic stress. J. Insect. Physiol. 50:767–75 [Google Scholar]
  2. Atkinson D, Morley SA, Hughes RN. 2.  2006. From cells to colonies: At what levels of body organization does the ‘temperature-size rule’ apply?. Evol. Dev. 8:202–14 [Google Scholar]
  3. Azad P, Ryu J, Haddad GG. 3.  2011. Distinct role of Hsp70 in Drosophila hemocytes during severe hypoxia. Free Radic. Biol. Med. 51:530–38 [Google Scholar]
  4. Azad P, Zhou D, Russo E, Haddad GG. 4.  2009. Distinct mechanisms underlying tolerance to intermittent and constant hypoxia in Drosophila melanogaster. PLOS ONE 4:e5371 [Google Scholar]
  5. Azevedo RBR, French V, Partridge L. 5.  2002. Temperature modulates epidermal cell size in Drosophila melanogaster. J. Insect. Physiol. 48:231–37 [Google Scholar]
  6. Azevedo SV, Caranton OAM, de Oliveira TL, Hartfelder K. 6.  2011. Differential expression of hypoxia pathway genes in honey bee (Apis mellifera L.) caste development. J. Insect. Physiol. 57:38–45 [Google Scholar]
  7. Baird NA, Turnbull DW, Johnson EA. 7.  2006. Induction of the heat shock pathway during hypoxia requires regulation of heat shock factor by hypoxia-inducible factor-1. J. Biol. Chem. 281:38675–81 [Google Scholar]
  8. Boardman L, Sørensen JG, Koštál V, Šimek P, Terblanche JS. 8.  2016. Chilling slows anaerobic metabolism to improve anoxia tolerance of insects. Metabolomics 12:176 [Google Scholar]
  9. Bohm S, ter Haar S, Ludwig K, Mathijssen D. 9.  2016. Het verband tussen de ademhalingsstrategieën van macroinvertebraten en de zuurstofcondities in duinplassen Course Report Systeemecologie, Radboud Univ Nijmegen, Neth.: [Google Scholar]
  10. Bozinovic F, Calosi P, Spicer JI. 10.  2011. Physiological correlates of geographic range in animals. Annu. Rev. Ecol. Evol. Syst. 42:155–79 [Google Scholar]
  11. Brodersen KP, Pedersen O, Walker IR, Tranekjaer Jensen M. 11.  2008. Respiration of midges (Diptera; Chironomidae) in British Columbian lakes: oxy-regulation, temperature and their role as palaeo-indicators. Freshwater Biol 53:593–602 [Google Scholar]
  12. Burggren W, Souder BM, Ho DH. 12.  2017. Metabolic rate and hypoxia tolerance are affected by group interactions and sex in the fruit fly (Drosophila melanogaster): new data and a literature survey. Biol. Open 6:471–80 [Google Scholar]
  13. Burkett BN, Schneiderman HA. 13.  1967. Control of spiracles in silk moths by oxygen and carbon dioxide. Science 156:1604–6 [Google Scholar]
  14. Burmester T. 14.  2015. Evolution of respiratory proteins across the Pancrustacea. Integr. Comp. Biol. 55:792–801 [Google Scholar]
  15. Bustami HP, Harrison JF, Hustert R. 15.  2002. Evidence for oxygen and carbon dioxide receptors in insect CNS influencing ventilation. Comp. Biochem. Physiol. A: Mol. Integr. Physiol. 133:595–604 [Google Scholar]
  16. Callier V, Nijhout HF. 16.  2011. Control of body size by oxygen supply reveals size-dependent and size-independent mechanisms of molting and metamorphosis. PNAS 108:14664–69 [Google Scholar]
  17. Callier V, Nijhout HF. 17.  2012. Supply-side constraints are insufficient to explain the ontogenetic scaling of metabolic rate in the tobacco hornworm. Manduca sexta. PLOS ONE 7:e45455 [Google Scholar]
  18. Callier V, Nijhout HF. 18.  2013. Body size determination in insects: a review and synthesis of size- and brain-dependent and independent mechanisms. Biol. Rev. 88:944–54 [Google Scholar]
  19. Callier V, Nijhout HF. 19.  2014. Plasticity of insect body size in response to oxygen: integrating molecular and physiological mechanisms. Curr. Opin. Insect. Sci. 1:59–65 [Google Scholar]
  20. Callier V, Shingleton AW, Brent CS, Ghosh SM, Kim J, Harrison JF. 20.  2013. The role of reduced oxygen in the developmental physiology of growth and metamorphosis initiation in Drosophila melanogaster. J. Exp. Biol. 216:4334–40 [Google Scholar]
  21. Camp AA, Funk DH, Buchwalter DB. 21.  2014. A stressful shortness of breath: Molting disrupts breathing in the mayfly Cloeon dipterum. Freshwater Sci 33:695–99 [Google Scholar]
  22. Cavallaro MC, Hoback WW. 22.  2014. Hypoxia tolerance of larvae and pupae of the semi-terrestrial caddisfly (Trichoptera: Limnephilidae). Ann. Entomol. Soc. Am. 107:1081–85 [Google Scholar]
  23. Centanin L, Gorr TA, Wappner P. 23.  2010. Tracheal remodelling in response to hypoxia. J. Insect. Physiol. 56:447–54 [Google Scholar]
  24. Chamberlin ME, Gibellatio CM, Noecker RJ, Dankoski EJ. 24.  1997. Changes in midgut active ion transport and metabolism during larval-larval molting in the tobacco hornworm (Manduca sexta). J. Exp. Biol. 200:643–48 [Google Scholar]
  25. Chandel NS, McClintock DS, Feliciano CE, Wood TM, Melendez JA. 25.  et al. 2000. Reactive oxygen species generated at mitochondrial complex III stabilize hypoxia-inducible factor-1α during hypoxia: a mechanism of O2 sensing. J. Biol. Chem. 275:25130–38 [Google Scholar]
  26. Charette M, Darveau C-A, Perry SF, Rundle HD. 26.  2011. Evolutionary consequences of altered atmospheric oxygen in Drosophila melanogaster. PLOS ONE 6:e26876 [Google Scholar]
  27. Chen B, Ma R, Ma G, Guo X, Tong X. 27.  et al. 2015. Haemocyanin is essential for embryonic development and survival in the migratory locust. Insect. Mol. Biol. 24:517–27 [Google Scholar]
  28. Chinopoulos C. 28.  2013. Which way does the citric acid cycle turn during hypoxia? The critical role of the α-ketoglutarate dehydrogenase complex. J. Neurosci. Res. 91:1030–33 [Google Scholar]
  29. Clarke KU. 29.  1957. On the role of the tracheal system in the post-embryonic growth of Locusta migratoria L. Proc. R. Entomol. Soc. Lond. A 32:67–79 [Google Scholar]
  30. Colombani J, Bianchini L, Layalle S, Pondeville E, Dauphin-Villemant C. 30.  et al. 2005. Antagonistic actions of ecdysone and insulins determine final size in Drosophila. Science 310:667–70 [Google Scholar]
  31. Czarnoleski M, Cooper BS, Kierat J, Angilletta MJ. 31.  2013. Flies developed small bodies and small cells in warm and in thermally fluctuating environments. J. Exp. Biol. 216:2896–901 [Google Scholar]
  32. Dejours P. 32.  1975. Principles of Comparative Respiratory Physiology. Amsterdam, Neth.: North-Holland [Google Scholar]
  33. Dekanty A, Centanin L, Wappner P. 33.  2007. Role of the hypoxia–response pathway on cell size determination and growth control. Dev. Biol. 306:339 [Google Scholar]
  34. D'Ignazio L, Bandarra D, Rocha S. 34.  2015. NF-κB and HIF crosstalk in immune responses. FEBS J 283:413–34 [Google Scholar]
  35. Dillon ME, Frazier MR. 35.  2006. Drosophila melanogaster locomotion in cold thin air. J. Exp. Biol. 209:364–71 [Google Scholar]
  36. Dillon ME, Frazier MR, Dudley R. 36.  2006. Into thin air: physiology and evolution of alpine insects. Integr. Comp. Biol. 46:49–61 [Google Scholar]
  37. Ern R, Huong DTT, Phuong NT, Madsen PT, Wang T, Bayley M. 37.  2015. Some like it hot: thermal tolerance and oxygen supply capacity in two eurythermal crustaceans. Sci. Rep. 5:10743 [Google Scholar]
  38. Farzin M, Albert T, Pierce N, VandenBrooks JM, Dodge T, Harrison JF. 38.  2014. Acute and chronic effects of atmospheric oxygen on the feeding behavior of Drosophila melanogaster larvae. J. Insect. Physiol. 68:23–29 [Google Scholar]
  39. Feala JD, Coquin L, Zhou D, Haddad GG, Paternostro G, McCulloch AD. 39.  2009. Metabolism as means for hypoxia adaptation: metabolic profiling and flux balance analysis. BMC Syst. Biol. 3:91 [Google Scholar]
  40. Frazier MR, Woods HA, Harrison JF. 40.  2001. Interactive effects of rearing temperature and oxygen on the development of Drosophila melanogaster. Physiol. Biochem. Zool. 74:641–50 [Google Scholar]
  41. Genkai-Kato M, Nozaki K, Mitsuhashi H, Kohmatsu Y, Miyasaka H, Nakanishi M. 41.  2000. Push-up response of stonefly larvae in low-oxygen conditions. Ecol. Res. 15:175–79 [Google Scholar]
  42. Gleixner E, Abriss D, Adryan B, Kraemer M, Gerlach F. 42.  et al. 2008. Oxygen-induced changes in hemoglobin expression in Drosophila. FEBS J 275:5108–16 [Google Scholar]
  43. Gleixner E, Ripp F, Gorr TA, Schuh R, Wolf C. 43.  et al. 2016. Knockdown of Drosophila hemoglobin suggests a role in O2 homeostasis. Insect Biochem. Mol. Biol. 72:20–30 [Google Scholar]
  44. Grazioli V, Rossaro B, Parenti P, Giacchini R, Lencioni V. 44.  2016. Hypoxia and anoxia effects on alcohol dehydrogenase activity and hemoglobin content in Chironomus riparius Meigen, 1804.. J. Limnol. 75:347–54 [Google Scholar]
  45. Greenlee KJ, Harrison JF. 45.  1998. Acid-base and respiratory responses to hypoxia in the grasshopper Schistocerca americana. J. Exp. Biol. 201:2843–55 [Google Scholar]
  46. Greenlee KJ, Harrison JF. 46.  2004. Development of respiratory function in the American locust Schistocerca americana I. Across-instar effects. J. Exp. Biol. 207:497–508 [Google Scholar]
  47. Greenlee KJ, Harrison JF. 47.  2004. Development of respiratory function in the American locust Schistocerca americana II. Within-instar effects. J. Exp. Biol. 207:509–17 [Google Scholar]
  48. Greenlee KJ, Harrison JF. 48.  2005. Respiratory changes throughout ontogeny in the tobacco hornworm caterpillar. Manduca sexta. J. Exp. Biol. 208:1385–92 [Google Scholar]
  49. Greenlee KJ, Henry JR, Kirkton SD, Westneat MW, Fezzaa K. 49.  et al. 2009. Synchrotron imaging of the grasshopper tracheal system: morphological components of tracheal hypermetry and the effect of age and stage on abdominal air sac volumes and convection. Am. J. Physiol. Regul. Integr. Comp. Physiol. 297:1343–50 [Google Scholar]
  50. Greenlee KJ, Nebeker C, Harrison JF. 50.  2007. Body size-independent safety margins for gas exchange across grasshopper species. J. Exp. Biol. 210:1288–96 [Google Scholar]
  51. Hamburger K, Dall PC, Lindegaard C. 51.  1994. Energy metabolism of Chironomus anthracinus (Diptera: Chironomidae) from the profundal zone of Lake Esrom, Denmark, as a function of body size, temperature and oxygen concentration. Hydrobiologia 294:43–50 [Google Scholar]
  52. Hamburger K, Dall PC, Lindegaard CL, Nilson IB. 52.  2000. Survival and energy metabolism in an oxygen deficient environment. Field and laboratory studies on the bottom fauna from the profundal zone of Lake Esrom, Denmark. Hydrobiologia 432:173–88 [Google Scholar]
  53. Harrison JF. 53.  2015. Handling and use of oxygen by pancrustaceans: conserved patterns and the evolution of respiratory structures. Integr. Comp. Biol. 55:802–15 [Google Scholar]
  54. Harrison JF, Klok CJ, Waters JS. 54.  2014. Critical PO2 is size-independent in insects: implications for the metabolic theory of ecology. Curr. Opin. Insect. Sci. 4:54–59 [Google Scholar]
  55. Harrison JF, Lighton JRB. 55.  1998. Oxygen-sensitive flight metabolism in the dragonfly Erythemis simplicicollis. J. Exp. Biol. 201:1739–44 [Google Scholar]
  56. Harrison JF, Philips JE, Gleeson TT. 56.  1991. Activity physiology of the two-striped grasshopper, Melanoplus bivittatus: gas exchange, hemolymph acid-base status, lactate production and the effect of temperature. Physiol. Zool. 64:451–72 [Google Scholar]
  57. Harrison JF, Shingleton AW, Callier V. 57.  2015. Stunted by developing in hypoxia: linking comparative and model organism studies. Physiol. Biochem. Zool. 88:455–70 [Google Scholar]
  58. Harrison JF, Wasserthal LT, Chapman RF. 58.  2013. Gaseous exchange. In The Insects: Structure and Function SJ Simpson, AE Douglas 501–45 New York: Cambridge Univ. Press [Google Scholar]
  59. Heinrich EC, Farzin M, Klok CJ, Harrison JF. 59.  2011. The effect of developmental stage on the sensitivity of cell and body size to hypoxia in Drosophila melanogaster. J. Exp. Biol. 214:1419–27 [Google Scholar]
  60. Helm BR, Davidowitz G. 60.  2013. Mass and volume growth of an insect tracheal system within a single instar. J. Exp. Biol. 216:4703–11 [Google Scholar]
  61. Henry JR, Harrison JF. 61.  2004. Plastic and evolved responses of larval tracheae and mass to varying atmospheric oxygen content in Drosophila melanogaster. J. Exp. Biol. 207:3559–67 [Google Scholar]
  62. Henry JR, Harrison JF. 62.  2014. Body size effects on the oxygen-sensitivity of dragonfly flight. J. Exp. Biol. 217:3447–56 [Google Scholar]
  63. Hessen DO, Daufresne M, Leinaas HP. 63.  2013. Temperature-size relations from the cellular-genomic perspective. Biol. Rev. 88:476–89 [Google Scholar]
  64. Hetz SK, Bradley TJ. 64.  2005. Insects breathe discontinuously to avoid oxygen toxicity. Nature 433:516–19 [Google Scholar]
  65. Hoback WW. 65.  2012. Ecological and experimental exposure of insects to anoxia reveals surprising tolerance. Anoxia: Evidence for Eukaryotic Survival and Paleontological Strategies A Altenbach, JM Bernhard, J Seckback 169–88 New York: Springer [Google Scholar]
  66. Hoback WW, Podrabsky JE, Higley LG, Stanley DW, Hand SC. 66.  2000. Anoxia tolerance of con-familial tiger beetle larvae is associated with differences in energy flow and anaerobiosis. J. Comp. Physiol. B 170:307–14 [Google Scholar]
  67. Hoback WW, Stanley DW. 67.  2001. Insects in hypoxia. J. Insect. Physiol. 47:533–42 [Google Scholar]
  68. Hoefnagel KN, Verberk WCEP. 68.  2015. Is the temperature-size rule mediated by oxygen in aquatic ectotherms?. J. Therm. Biol. 54:56–65 [Google Scholar]
  69. Holter P, Spangenberg A. 69.  1997. Oxygen uptake in coprophilous beetles (Aphodius, Geotrupes, Sphaeridium) at low oxygen and high carbon dioxide concentrations. Physiol. Entomol. 22:339–43 [Google Scholar]
  70. Horne CR, Hirst AG, Atkinson D. 70.  2015. Temperature-size responses match latitudinal-size clines in arthropods, revealing critical differences between aquatic and terrestrial species. Ecol. Lett. 18:327–35 [Google Scholar]
  71. Hsia CCW, Schmitz A, Lambertz M, Perry SF, Maina JN. 71.  2013. Evolution of air breathing: oxygen homeostasis and the transitions from water to land and sky. Compr. Physiol. 3:849–915 [Google Scholar]
  72. Jacobsen D. 72.  2008. Low oxygen pressure as a driving factor for the altitudinal decline in taxon richness of stream macroinvertebrates. Oecologia 154:795–807 [Google Scholar]
  73. Jarecki J, Johnson E, Krasnow MA. 73.  1999. Oxygen regulation of airway branching in Drosophila is mediated by branchless FGF. Cell 99:211–20 [Google Scholar]
  74. Joos B, Lighton JRB, Harrison JF, Suarez RK, Roberts SP. 74.  1997. Effects of ambient oxygen tension on flight performance, metabolism, and water loss of the honeybee. Physiol. Zool. 70:167–74 [Google Scholar]
  75. Kaiser A, Klok CJ, Socha JJ, Lee W-K, Quinlan MC, Harrison JF. 75.  2007. Increase in tracheal investment with beetle size supports hypothesis of oxygen limitation on insect gigantism. PNAS 104:13198–203 [Google Scholar]
  76. Kim KS, Chou H, Funk DH, Jackson JK, Sweeney BW, Buchwalter DB. 76.  2017. Physiological responses to short term thermal stress in mayfly larvae (Neocloeon triangulifer) in relation to upper thermal limits. J. Exp. Biol. 220:2598–605 [Google Scholar]
  77. Kirkton S, Hennessey L, Duffy B, Bennett M, Lee W-K, Greenlee K. 77.  2012. Intermolt development reduces oxygen delivery capacity and jumping performance in the American locust (Schistocerca americana). J. Comp. Physiol. B 182:217–30 [Google Scholar]
  78. Kivelä SM, Friberg M, Wiklund C, Leimar O, Gotthard K. 78.  2016. Towards a mechanistic understanding of insect life history evolution: oxygen-dependent induction of moulting explains moulting sizes. Biol. J. Linn. Soc. 117:586–600 [Google Scholar]
  79. Klok CJ, Harrison JF. 79.  2013. The temperature size rule in arthropods: independent of macro-environmental variables but size dependent. Integr. Comp. Biol. 53:557–70 [Google Scholar]
  80. Klok CJ, Kaiser A, Lighton JRB, Harrison JF. 80.  2010. Critical oxygen partial pressures and maximal tracheal conductances for Drosophila melanogaster reared for multiple generations in hypoxia or hyperoxia. J. Insect. Physiol. 56:461–69 [Google Scholar]
  81. Klok CJ, Kaiser A, Socha JJ, Lee WK, Harrison JF. 81.  2016. Multigenerational effects of rearing atmospheric oxygen level on the tracheal dimensions and diffusing capacities of pupal and adult Drosophila melanogaster. Hypoxia RC Roach, PD Wagner, PH Hackett New York: Springer [Google Scholar]
  82. Klok CJ, Sinclair BJ, Chown SL. 82.  2004. Upper thermal tolerance and oxygen limitation in terrestrial arthropods. J. Exp. Biol. 207:2361–70 [Google Scholar]
  83. Komai Y. 83.  1998. Augmented respiration in a flying insect. J. Exp. Biol. 201:2359–66 [Google Scholar]
  84. Komai Y. 84.  2001. Direct measurement of oxygen partial pressure in a flying bumblebee. J. Exp. Biol. 204:2999–3007 [Google Scholar]
  85. Lavista-Llanos S, Centanin L, Irisarri M, Russo DM, Gleadle JM. 85.  et al. 2002. Control of the hypoxic response in Drosophila melanogaster by the basic helix-loop-helix PAS protein similar. Mol. Cell. Biol. 22:6842–53 [Google Scholar]
  86. Lease HM, Klok CJ, Kaiser A, Harrison JF. 86.  2012. Body size is not critical for critical in scarabaeid and tenebrionid beetles. J. Exp. Biol. 215:2524–33 [Google Scholar]
  87. Lease HM, Wolf BO, Harrison JF. 87.  2006. Intraspecific variation in tracheal volume in the American locust, Schistocerca americana, measured by a new inert gas method. J. Exp. Biol. 209:3476–83 [Google Scholar]
  88. Lencioni V, Bernabò P, Vanin S, Di Muro P, Beltramini M. 88.  2008. Respiration rate and oxy-regulatory capacity in cold stenothermal chironomids. J. Insect. Physiol. 54:1337–42 [Google Scholar]
  89. Li Y, Padmanabha D, Gentile LB, Dumur CI, Beckstead RB, Baker KD. 89.  2013. HIF- and non-HIF-regulated hypoxic responses require the estrogen-related receptor in Drosophila melanogaster. PLOS Genet 9:e1003230 [Google Scholar]
  90. Lighton JRB. 90.  2007. Hot hypoxic flies: Whole-organism interactions between hypoxic and thermal stressors in Drosophila melanogaster. J. Therm. Biol. 32:134–43 [Google Scholar]
  91. Lighton JRB. 91.  2017. Limitations and requirements for measuring metabolic rates: a mini review. Eur. J. Clin. Nutr. 71:301–05 [Google Scholar]
  92. Liu G, Roy J, Johnson EA. 92.  2006. Identification and function of hypoxia-response genes in Drosophila melanogaster. Physiol. Genom. 25:134–41 [Google Scholar]
  93. Lord JC. 93.  2009. Efficacy of Beauveria bassiana for control of Tribolium castaneum with reduced oxygen and increased carbon dioxide. J. Appl. Entomol. 133:101–7 [Google Scholar]
  94. Loudon C. 94.  1989. Tracheal hypertrophy in mealworms: design and plasticity in oxygen supply systems. J. Exp. Biol. 147:217–35 [Google Scholar]
  95. Ma E, Haddad GG. 95.  1999. Isolation and characterization of the hypoxia-inducible factor 1β in Drosophila melanogaster. Mol. Brain Res. 73:11–16 [Google Scholar]
  96. Madsen PB, Morabowen A, Andino P, Espinosa R, Cauvy-Fraunie SC. 96.  et al. 2015. Altitudinal distribution limits of aquatic macroinvertebrates: an experimental test in a tropical alpine stream. Ecol. Entomol. 40:629–38 [Google Scholar]
  97. Marden JH, Fescemyer HW, Schilder RJ, Doerfler WR, Vera JC, Wheat CW. 97.  2012. Genetic variation in HIF signaling underlies quantitative variation in physiological and life-history traits within lowland butterfly populations. Evolution 67:1105–15 [Google Scholar]
  98. Matthews PGD, Snelling EP, Seymour RS, White CR. 98.  2012. A test of the oxidative damage hypothesis for discontinuous gas exchange in the locust Locusta migratoria. Biol. Lett. 8:682–84 [Google Scholar]
  99. McElroy GS, Chandel NS. 99.  2017. Mitochondria control acute and chronic responses to hypoxia. Exp. Cell Res. 356:217–22 [Google Scholar]
  100. McMullen DC, Storey K. 100.  2008. Mitochondria of cold hardy insects: responses to cold and hypoxia assessed at enzymatic, mRNA and DNA levels. Insect Biochem. Mol. Biol. 38:367–73 [Google Scholar]
  101. Michaud MR, Benoit JB, Lopez-Martinez G, Elnitsky MA, Lee REJ, Denlinger DL. 101.  2008. Metabolomics reveals unique and shared metabolic changes in response to heat shock, freezing and desiccation in the Antarctic midge. Belgica antarctica. J. Insect. Physiol. 54:645–55 [Google Scholar]
  102. Michaud MR, Denlinger DL. 102.  2007. Shifts in the carbohydrate, polyol, and amino acid pools during rapid cold-hardening and diapause-associated cold-hardening in flesh flies (Sarcophaga crassipalpis): a metabolomic comparison. J. Comp. Physiol. B 177:753–63 [Google Scholar]
  103. Mölich AB, Förster TD, Lighton JRB. 103.  2012. Hyperthermic overdrive: oxygen delivery does not limit thermal tolerance in Drosophila melanogaster. J. Insect Sci. 12:109 [Google Scholar]
  104. Monaghan P, Metcalfe NB, Roxana T. 104.  2009. Oxidative stress as a mediator of life history trade-offs: mechanisms, measurements and interpretation. Ecol. Lett. 12:75–92 [Google Scholar]
  105. Morin P Jr., McMullen DC, Storey KB. 105.  2005. HIF-1α involvement in low temperature and anoxia survival by a freeze tolerant insect. Mol. Cell. Biochem 280:99–106 [Google Scholar]
  106. Morton DB, Stewart JA, Langlais KK, Clemens-Grisham RA, Vermehren A. 106.  2008. Synaptic transmission in neurons that express the Drosophila atypical soluble guanylyl cyclases, Gyc-89Da and Gyc-89Db, is necessary for the successful completion of larval and adult ecdysis. J. Exp. Biol. 211:1645–56 [Google Scholar]
  107. Mukherjee T, Kim WS, Mandal L, Banerjee U. 107.  2011. Interaction between Notch and Hif-α in development and survival of Drosophila blood cells. Science 332:1210–13 [Google Scholar]
  108. Neven LG, Lehrman N, Hansen LD. 108.  2014. Effects of temperature and modified atmospheres on diapausing 5th instar codling moth metabolism. J. Therm. Biol. 42:9–14 [Google Scholar]
  109. Owings AA, Yocum GD, Rinehart JP, Kemp WP, Greenlee KJ. 109.  2014. Changes in respiratory structure and function during post-diapause development in the alfalfa leafcutting bee. Megachile rotundata. J. Insect. Physiol. 66:20–27 [Google Scholar]
  110. Peck LS, Maddrell SHP. 110.  2005. Limitation of size by hypoxia in the fruit fly Drosophila melanogaster. J. Exp. Zool. A 303A:968–75 [Google Scholar]
  111. Philipson GN, Moorhouse BHS. 111.  1974. Observations on ventilatory and net-spinning activities of larvae of the genus Hydropsyche Pictet (Trichoptera, Hydropsychidae) under experimental conditions. Freshwater Biol 4:525–33 [Google Scholar]
  112. Pörtner H-O. 112.  2010. Oxygen- and capacity-limitation of thermal tolerance: a matrix for integrating climate-related stressor effects in marine ecosystems. J. Exp. Biol. 213:881–93 [Google Scholar]
  113. Pörtner H-O, Giomi F. 113.  2013. Nothing in experimental biology makes sense except in the light of ecology and evolution—correspondence on. J. Exp. Biol 216:2771–2782 J. Exp. Biol. 216:4494–95 [Google Scholar]
  114. Rascón B, Harrison JF. 114.  2004. Atmospheric oxygen effects on metabolic rate and behavior of tethered flying locusts. Integr. Comp. Biol. 44:627 [Google Scholar]
  115. Rascón B, Harrison JF. 115.  2005. Oxygen partial pressure effects on metabolic rate and behavior of tethered flying locusts. J. Insect. Physiol. 51:1193–99 [Google Scholar]
  116. Rascón B, Harrison JF. 116.  2010. Lifespan and oxidative stress show a nonlinear response to atmospheric oxygen level in Drosophila. J. Exp. Biol. 213:3441–48 [Google Scholar]
  117. Reiling JH, Hafen E. 117.  2004. The hypoxia-induced paralogs Scylla and Charybdis inhibit growth by down-regulating S6K activity up stream of TSC in Drosophila. Genes Dev 18:2879–92 [Google Scholar]
  118. Reynolds JA, Hand SC. 118.  2009. Decoupling development and energy flow during embryonic diapause in the cricket. Allonemobius socius. J. Exp. Biol. 212:2065–74 [Google Scholar]
  119. Rhee SG, Woo HA, Kil IS, Bae SH. 119.  2012. Peroxiredoxin functions as a peroxidase and a regulator and sensor of local peroxides. J. Biol. Chem. 287:4403–10 [Google Scholar]
  120. Shelomi M. 120.  2012. Where are we now? Bergman's rule senso lato in insects. Am. Nat. 180:511–19 [Google Scholar]
  121. Shichita T, Hasegawa E, Kimura A, Morita R, Sakaguchi R. 121.  et al. 2012. Peroxiredoxin family proteins are key initiators of post-ischemic inflammation in the brain. Nat. Med. 18:911–17 [Google Scholar]
  122. Simpson PD, Eipper BA, Katz MJ, Gandara L, Wappner P. 122.  et al. 2015. Striking oxygen sensitivity of the peptidylglycine α-amidating monooxygenase (PAM) in neuroendocrine cells. J. Biol. Chem. 290:24891–901 [Google Scholar]
  123. Stevens MM, Jackson S, Bester SA, Terblanche JS, Chown SL. 123.  2010. Oxygen limitation and thermal tolerance in two terrestrial arthropod species. J. Exp. Biol. 213:2209–18 [Google Scholar]
  124. Tennessen JM, Baker KD, Lam G, Evans J, Thummel CS. 124.  2011. The Drosophila estrogen-related receptor directs a metabolic switch that supports developmental growth. Cell Metab 13:139–48 [Google Scholar]
  125. Tennessen JM, Bertagnolli NM, Evans J, Sieber MH, Cox J, Thummel CS. 125.  2014. Coordinated metabolic transitions during Drosophila embryogenesis and the onset of aerobic glycolysis. G3 4839–50 [Google Scholar]
  126. Välimäki P, Kivelä SM, Raitanen J, Pakanen V-M, Vatka E. 126.  et al. 2015. Larval melanism in a geometrid moth: promoted neither by a thermal nor seasonal adaptation but desiccating environments. J. Anim. Ecol. 84:817–28 [Google Scholar]
  127. van der Geest HG. 127.  2007. Behavioural responses of caddisfly larvae (Hydropsyche angustipennis) to hypoxia. Contrib. Zool. 76:255–60 [Google Scholar]
  128. Van der Have TM. 128.  2002. A proximate model for thermal tolerance in ectotherms. Oikos 98:141–55 [Google Scholar]
  129. Van Voorhies WA. 129.  2009. Metabolic function in Drosophila melanogaster in response to hypoxia and pure oxygen. J. Exp. Biol. 212:3132–41 [Google Scholar]
  130. VandenBrooks JM, Munoz EE, Weed MD, Ford CF, Harrison MA, Harrison JF. 130.  2012. Impacts of paleo-oxygen levels on the size, development, reproduction, and tracheal systems of Blatella germanica. Evol. Biol. 39:83–93 [Google Scholar]
  131. Verberk WCEP, Atkinson D. 131.  2013. Why polar gigantism and Palaeozoic gigantism are not equivalent: effects of oxygen and temperature on the body size of ectotherms. Funct. Ecol. 27:1275–85 [Google Scholar]
  132. Verberk WCEP, Bilton DT. 132.  2011. Can oxygen set thermal limits in an insect and drive gigantism?. PLOS ONE 6:e22610 [Google Scholar]
  133. Verberk WCEP, Bilton DT. 133.  2013. Respiratory control in aquatic insects dictates their vulnerability to global warming. Biol. Lett. 9:20130473 [Google Scholar]
  134. Verberk WCEP, Bilton DT. 134.  2015. Oxygen-limited thermal tolerance is seen in a plastron-breathing insect and can be induced in a bimodal gas exchanger. J. Exp. Biol. 218:2083–88 [Google Scholar]
  135. Verberk WCEP, Bilton DT, Calosi P, Spicer JI. 135.  2011. Oxygen supply in aquatic ectotherms: Partial pressure and solubility together explain biodiversity and size patterns. Ecology 92:1565–72 [Google Scholar]
  136. Verberk WCEP, Durance I, Vaughan IP, Ormerod SJ. 136.  2016. Field and laboratory studies reveal interacting effects of stream oxygenation and warming on aquatic ectotherms. Glob. Change Biol. 22:1769–78 [Google Scholar]
  137. Verberk WCEP, Overgaard J, Ern R, Bayley M, Wang T. 137.  et al. 2016. Does oxygen limit thermal tolerance in arthropods? A critical review of current evidence. Comp. Biochem. Physiol. A: Mol. Integr. Physiol. 192:64–78 [Google Scholar]
  138. Verberk WCEP, Sommer U, Davidson RL, Viant MR. 138.  2013. Anaerobic metabolism at thermal extremes: a metabolomic test of the oxygen limitation hypothesis in an aquatic insect. Integr. Comp. Biol. 53:609–19 [Google Scholar]
  139. Vermehren-Schmaedick A, Ainsley JA, Johnson WA, Davies S-A, Morton DB. 139.  2010. Behavioral responses to hypoxia in Drosophila larvae are mediated by atypical soluble guanylyl cyclases. Genetics 186:183–96 [Google Scholar]
  140. Walshe BM. 140.  1950. The function of haemoglobin in Chironomus plumosus under natural conditions. J. Exp. Biol. 27:73–95 [Google Scholar]
  141. Wegener G. 141.  1993. Hypoxia and posthypoxic recovery in insects: physiological and metabolic aspects. Surviving Hypoxia: Mechanisms of Control and Adaptation PW Hochachka, PL Lutz, T Sick, M Rosenthal, G van den Thillart 417–34 Boca Raton, FL: CRC Press [Google Scholar]
  142. Wegener G, Moratzky T. 142.  1995. Hypoxia and anoxia in insects: microcalorimetric studies on two species (Locusta migratoria and Manduca sexta) showing different degrees of anoxia tolerance. Thermochim. Acta 251:209–18 [Google Scholar]
  143. Wheat CW, Fescemyer HW, Kvist J, Tas EVA, Vera JC. 143.  et al. 2011. Functional genomics of life history variation in a butterfly metapopulation. Mol. Ecol. 20:1813–28 [Google Scholar]
  144. Wigglesworth VB. 144.  1983. The physiology of insect tracheoles. Adv. Insect Physiol. 17:85–149 [Google Scholar]
  145. Williams DD, Tavares AR, Bryant E. 145.  1987. Respiratory device or camouflage? A case for the caddisfly. Oikos 50:42–52 [Google Scholar]
  146. Wingrove JA, O'Farrell PH. 146.  1999. Nitric oxide contributes to behavioral, cellular, and developmental responses to low oxygen in Drosophila. Cell 98:105–14 [Google Scholar]
  147. Wong DM, Shen Z, Owyang KE, Martinez-Agosto JA. 147.  2014. Insulin- and warts-dependent regulation of tracheal plasticity modulates systemic larval growth during hypoxia in Drosophila melanogaster. PLOS ONE 9:e115297 [Google Scholar]
  148. Woods HA, Bonnecaze RT, Zrubek B. 148.  2005. Oxygen and water flux across eggshells of Manduca sexta. J. Exp. Biol. 208:1297–308 [Google Scholar]
  149. Woods HA, Hill RI. 149.  2004. Temperature-dependent oxygen limitation in insect eggs. J. Exp. Biol. 207:2267–76 [Google Scholar]
  150. Woods HA, Lane SJ. 150.  2016. Metabolic recovery from drowning by insect pupae. J. Exp. Biol. 219:3126–36 [Google Scholar]
  151. Yerra A, Challa S, Valluri SV, Mamillapalli A. 151.  2016. Spermidine alleviates oxidative stress in silk glands of Bombyx mori. J. Asia-Pac. Entomol. 19:1197–202 [Google Scholar]
  152. Zebe E. 152.  1991. In vivo studies on the function of hemoglobin in the larvae of Chironomus thummi (Insecta, Diptera). Comp. Biochem. Physiol. A: Physiol. 99:525–29 [Google Scholar]
  153. Zhang Z-Y, Chen B, Zhao D-J, Kang L. 153.  2013. Functional modulation of mitochondrial cytochrome c oxidase underlies adaptation to high-altitude hypoxia in a Tibetan migratory locust. Proc. R. Soc. B 280:20122758 [Google Scholar]
  154. Zhou D, Xue J, Lai JCK, Schork NJ, White KP, Haddad GG. 154.  2008. Mechanisms underlying hypoxia tolerance in Drosophila melanogaster: hairy as a metabolic switch. PLOS Genet 4:e1000221 [Google Scholar]
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