Hypoxic tolerance in air-breathing invertebrates

Terrestrial invertebrates experience hypoxia in many habitats and under a variety of physiological conditions. Some groups (at least insects) are much more capable of recovery from anoxia than most vertebrates, but there is still a tremendous unexplained variation in hypoxia/anoxia tolerance among terrestrial invertebrates. Crustaceans and arachnids may be less often confronted with hypoxic environments than insects and myriapods and also seem to be less hypoxia/anoxia tolerant. Tracheated groups, especially those that are able to ventilate their tracheal system like many insects, cope with lower critical PO2 than nontracheated groups. Modulation of oxygen carrier proteins is normally not important in hypoxia resistance. Recent application of genetic and cellular tools are revealing that many of the same pathways documented for mammals (e.g. HIF, nitric oxide) function to regulate morphological and biochemical responses to hypoxia/anoxia in insects.

[1]  C. Bridges The haemocyanin of the tarantula Lasiodora erythrocythara—the influence of CO2, organic cofactors and temperature on oxygen affinity , 1988 .

[2]  Neuromuscular coordination and proprioceptive control of rhythmical abdominal ventilation in intactLocusta migratoria migratorioides , 1975, Journal of comparative physiology.

[3]  P. Miller The Regulation of Breathing in Insects , 1966 .

[4]  S. Morris,et al.  Respiratory, Acid-Base, and Metabolic Responses of the Christmas Island Blue Crab, Cardisoma hirtipes (Dana), during Simulated Environmental Conditions , 1997, Physiological Zoology.

[5]  C. Gans,et al.  Implications of the late Palaeozoic oxygen pulse for physiology and evolution , 1995, Nature.

[6]  S. Morris The ecophysiology of air-breathing in crabs with special reference to Gecarcoidea natalis. , 2002, Comparative biochemistry and physiology. Part B, Biochemistry & molecular biology.

[7]  J. Harrison,et al.  Interactive Effects of Rearing Temperature and Oxygen on the Development of Drosophila melanogaster , 2001, Physiological and Biochemical Zoology.

[8]  J. Buck,et al.  CYCLIC CO2 RELEASE IN DIAPAUSING AGAPEMA PUPAE , 1955 .

[9]  P. Holter,et al.  Oxygen uptake in coprophilous beetles (Aphodius, Geotrupes, Sphaeridium) at low oxygen and high carbon dioxide concentrations , 1997 .

[10]  G. Kölsch,et al.  Energy metabolism and metabolic rate of the alder leaf beetle Agelastica alni (L.) (Coleoptera, Chrysomelidae) under aerobic and anaerobic conditions: a microcalorimetric study. , 2002, Journal of insect physiology.

[11]  J. Lighton,et al.  Discontinuous Gas Exchange in the Pseudoscorpion Garypus californicus Is Regulated by Hypoxia, Not Hypercapnia , 2002, Physiological and Biochemical Zoology.

[12]  Quinlan,et al.  Acid-base status and spiracular control during discontinuous ventilation in grasshoppers , 1995, The Journal of experimental biology.

[13]  J. Markl,et al.  Identification, Structure, and Properties of Hemocyanins from Diplopod Myriapoda* , 1999, The Journal of Biological Chemistry.

[14]  P. Davies,et al.  Respiration in the Land Crab, Gecarcinus Lateralis , 1981 .

[15]  T. Weis-Fogh,et al.  Respiration and tracheal ventilation in locusts and otger flying insects. , 1967, The Journal of experimental biology.

[16]  G. Haddad,et al.  Understanding the molecular responses to hypoxia using Drosophila as a genetic model , 2003, Respiratory Physiology & Neurobiology.

[17]  C. Heip,et al.  Size and shape of ocean margin nematodes: morphological diversity and depth-related patterns , 2002 .

[18]  S. Morris,et al.  Locomotion, Respiratory Physiology, and Energetics of Amphibious and Terrestrial Crabs* , 2000, Physiological and Biochemical Zoology.

[19]  R. Wyman,et al.  Behavioral and Electrophysiologic Responses of Drosophila melanogaster to Prolonged Periods of Anoxia. , 1997, Journal of insect physiology.

[20]  J. Harrison,et al.  Development of respiratory function in the American locust Schistocerca americana I. Across-instar effects , 2004, Journal of Experimental Biology.

[21]  H. Pörtner,et al.  Physiological and metabolic responses to hypoxia in invertebrates. , 1994, Reviews of physiology, biochemistry and pharmacology.

[22]  B. Linzen,et al.  Respiration in the tarantulaEurypelma californicum: evidence for diffusion lungs , 1987, Journal of Comparative Physiology B.

[23]  L. Levenbook The effect of carbon dioxide and certain respiratory inhibitors on the respiration of larvae of the horse bot fly (Gastrophilus intestinalis de Geer). , 1951, The Journal of experimental biology.

[24]  V. Wigglesworth The Physiology of Insect Tracheoles , 1983 .

[25]  G. Fraenkel,et al.  The Oxygen Consumption of Flies During Flight , 1940 .

[26]  Lázaro Centanin,et al.  Control of the Hypoxic Response in Drosophila melanogaster by the Basic Helix-Loop-Helix PAS Protein Similar , 2002, Molecular and Cellular Biology.

[27]  G. Gäde Anaerobic Energy Metabolism , 1984 .

[28]  John F Anderson,et al.  Respiratory Gas Exchange in Spiders , 1982, Physiological Zoology.

[29]  K. Behar,et al.  Role of Trehalose Phosphate Synthase in Anoxia Tolerance and Development in Drosophila melanogaster * , 2002, The Journal of Biological Chemistry.

[30]  Leon G. Higley,et al.  Anoxia tolerance of con-familial tiger beetle larvae is associated with differences in energy flow and anaerobiosis , 2000, Journal of Comparative Physiology B.

[31]  J. Wägele,et al.  Morphology and evolution of respiratory structures in the pleopod exopodites of terrestrial Isopoda (Crustacea, Isopoda, Oniscidea) , 2001 .

[32]  H. Schneiderman,et al.  Roles of oxygen and carbon dioxide in the control of spiracular function in Cecropia pupae. , 1974, The Biological bulletin.

[33]  Lloyd S. Peck,et al.  Polar gigantism dictated by oxygen availability , 1999, Nature.

[34]  C. Penteado,et al.  Respiratory Responses in a Brazilian Millipede, Pseudonannolene tricolor, to Declining Oxygen Pressures , 1991, Physiological Zoology.

[35]  J. Lighton Notes from Underground: Towards Ultimate Hypotheses of Cyclic, Discontinuous Gas-Exchange in Tracheate Arthropods' , 1998 .

[36]  Eric Johnson,et al.  Oxygen Regulation of Airway Branching in Drosophila Is Mediated by Branchless FGF , 1999, Cell.

[37]  J. Lighton,et al.  Effects of Ambient Oxygen Tension on Flight Performance, Metabolism, and Water Loss of the Honeybee , 1997, Physiological Zoology.

[38]  Lighton,et al.  Ant breathing: testing regulation and mechanism hypotheses with hypoxia , 1995, The Journal of experimental biology.

[39]  K. Thaler The Diversity of High Altitude Arachnids (Araneae, Opiliones, Pseudoscorpiones) in the Alps , 2003 .

[40]  J. Adis,et al.  Exceptional anoxia resistance in larval tiger beetle, Phaeoxantha klugii (Coleoptera: Cicindelidae) , 2003 .

[41]  A. Ar,et al.  Effects of chronic hypoxia, normoxia and hyperoxia on larval development in the beetle Tenebrio molitor , 1996 .

[42]  D. Zinkler,et al.  Local PO2 measurements in the environment of submerged soil microarthropods , 1994 .

[43]  R. Shonat,et al.  Critical [Formula: see text] of skeletal muscle in vivo. , 1999, American journal of physiology. Heart and circulatory physiology.

[44]  P. O’Farrell,et al.  Nitric Oxide Contributes to Behavioral, Cellular, and Developmental Responses to Low Oxygen in Drosophila , 1999, Cell.

[45]  R. Dudley,et al.  The evolutionary physiology of animal flight: paleobiological and present perspectives. , 2000, Annual review of physiology.

[46]  R. Hustert,et al.  Evidence for oxygen and carbon dioxide receptors in insect CNS influencing ventilation. , 2002, Comparative biochemistry and physiology. Part A, Molecular & integrative physiology.

[47]  E. Conradi-Larsen,et al.  Anaerobiosis in the Overwintering Beetle Pelophila borealis , 1973, Nature.

[48]  M. Barnhart,et al.  Depression of Aerobic Metabolism and Intracellular pH by Hypercapnia in Land Snails, Otala Lactea , 1988 .

[49]  R. Henry,et al.  Respiratory, cardiovascular, and hemolymph acid‐base changes in the amphibious crab, Cardisoma guanhumi, during immersion and emersion , 2001 .

[50]  S. Morris Respiratory gas exchange and transport in crustaceans: ecological determinants , 1991 .

[51]  Harrison,et al.  Haemolymph acid-base status, tracheal gas levels and the control of post-exercise ventilation rate in grasshoppers , 1996, The Journal of experimental biology.

[52]  C. Loudon Development of Tenebrio molitor in low oxygen levels , 1988 .

[53]  B. Mcmahon Functions and Functioning of Crustacean Hemocyanin , 1985 .

[54]  J. Lighton Discontinuous gas exchange in insects. , 1996, Annual review of entomology.

[55]  J. Lighton,et al.  Oxygen-sensitive flight metabolism in the dragonfly erythemis simplicicollis , 1998, The Journal of experimental biology.

[56]  G. L. Robinson,et al.  Regulation of external respiration by the book-lung spiracles of the spiders, Araneus diadematus Clerck and A. marmoreus Clerck , 1969 .

[57]  Harrison,et al.  Acid-base and respiratory responses to hypoxia in the grasshopper Schistocerca americana. , 1998, The Journal of experimental biology.

[58]  E. G. Mendes,et al.  The influence of size, temperature and oxygen tension upon the respiratory metabolism of the terrestrial amphipod Talitrus (Talitroides) pacificus Hurley, 1955 , 1987 .

[59]  S. Chown,et al.  Discontinuous gas-exchange in centipedes and its convergent evolution in tracheated arthropods. , 2002, The Journal of experimental biology.

[60]  S. Morris Organic Ions as Modulators of Respiratory Pigment Function during Stress , 1990, Physiological Zoology.

[61]  D. Stanley,et al.  Insects in hypoxia. , 2001, Journal of insect physiology.

[62]  N B Terwilliger,et al.  Functional adaptations of oxygen-transport proteins. , 1998, The Journal of experimental biology.

[63]  C. Wood,et al.  Oxygen and carbon dioxide exchange during exercise in the land crab (Cardisoma carnifex) , 1981 .

[64]  S. Morris,et al.  The Respiratory Gas Transport, Acid-Base State, Ion and Metabolite Status of the Christmas Island Blue Crab, Cardisoma hirtipes (Dana) Assessed in Situ with Respect to Immersion , 1996, Physiological Zoology.

[65]  J. Lighton,et al.  Gas exchange in wind spiders (Arachnida, Solphugidae): Independent evolution of convergent control strategies in solphugids and insects , 1996 .

[66]  R. Levy,et al.  Discontinuous respiration in insects. II. The direct measurement and significance of changes in tracheal gas composition during the respiratory cycle of silkworm pupae. , 1966, Journal of insect physiology.

[67]  C. F. Herreid Hypoxia in invertebrates , 1980 .

[68]  Harrison,et al.  Control of resting ventilation rate in grasshoppers , 1996, The Journal of experimental biology.

[69]  J. Buck,et al.  Respiration of Phormia regina in relation to temperature and oxygen , 1961 .

[70]  S. Perry,et al.  Bimodal breathing in jumping spiders: morphometric partitioning of the lungs and tracheae in Salticus scenicus (Arachnida, Araneae, Salticidae). , 2001, The Journal of experimental biology.

[71]  C. Loudon TRACHEAL HYPERTROPHY IN MEALWORMS: DESIGN AND PLASTICITY IN OXYGEN SUPPLY SYSTEMS , 1989 .

[72]  A. Pinder,et al.  The Burrow Microhabitat of the Land Crab Cardisoma guanhumi: Respiratory/Ionic Conditions and Physiological Responses of Crabs to Hypercapnia , 1993, Physiological Zoology.

[73]  C. Penteado Respiratory responses of the tropical millipede Plusioporus setiger (Broelemann, 1902) (Spirostreptida: Spirostreptidae) to normoxic and hypoxic conditions , 1987 .

[74]  A. Wessel Westheide. W., Rieger, R. (Hrsg.) (1996): Spezielle Zoologie. Erster Teil: Einzeller und Wirbellose Tiere. Gustav Fischer Verlag, Stuttgart, Jena, New York. 909 S., 1167 Abb. und 5 Tab., geb. DM 148,– , 1997 .

[75]  L. Peck,et al.  Reduced oxygen at high altitude limits maximum size , 2003, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[76]  K. Prestwich Anaerobic Metabolism in Spiders , 1983, Physiological Zoology.

[77]  J. Woodring,et al.  Anatomical and physiological studies of water balance in the millipedes Pachydesmus crassicutis (polydesmida) and Orthoporus texicolens (spirobolida) , 1973 .

[78]  C. F. Herreid,et al.  Cardiac and respiratory response to hypoxia in the land crab, Cardisoma guanhumi (Latreille) , 1979 .

[79]  C. McClain,et al.  The relationship between dissolved oxygen concentration and maximum size in deep-sea turrid gastropods: an application of quantile regression , 2001 .

[80]  J. N. Cameron,et al.  Aerial gas exchange in the coconut crab, Birgus latro with some notes on Gecarcoidea lalandii. , 1973, Respiration physiology.

[81]  S. Morris,et al.  Properties of Respiratory Pigments in Bimodal Breathing Animals: Air and Water Breathing by Fish and Crustaceans , 1994 .

[82]  W. Burggren,et al.  Respiration and Adaptation to the Terrestrial Habitat in the Land Hermit Crab Coenobita Clypeatus , 1979 .

[83]  C. Mangum Major Events in the Evolution of the Oxygen Carriers , 1998 .

[84]  L. Sømme ADAPTATIONS OF TERRESTRIAL ARTHROPODS TO THE ALPINE ENVIRONMENT , 1989 .

[85]  T. Burmester,et al.  Complete subunit sequences, structure and evolution of the 6 x 6-mer hemocyanin from the common house centipede, Scutigera coleoptrata. , 2003, European journal of biochemistry.