Are altitudinal limits of equatorial stream insects reflected in their respiratory performance

Summary 1. We measured respiration of the larvae of aquatic insects from streams in the Ecuadorian Andes in relation to oxygen saturation at 5, 8, 11, 14 and 17 °C. Polycentropus (Polycentropodidae), Lachlania (Oligoneuriidae), Anchytarsus (Ptilodactylidae) and Anacroneuria (Perlidae) represented genera absent from the highest altitudes, reaching 2720, 2930, 3120, 3450 m a.s.l., respectively, while Claudioperla (Gripopterygidae) and Anomalocosmoecus (Limnephilidae) occurred only above 2900 m a.s.l. Our purpose was to determine whether natural altitudinal limits were reflected in physiological critical points on respiration versus oxygen curves and by the effect of temperature on the ability to oxy-regulate. 2. For all six genera, respiration was affected by oxygen saturation and temperature. Respiration (mg O2 g−1 AFDM h−1) at 70% oxygen saturation (Michaelis–Menten fitted) varied from 2.6 to 7.6 between genera at 17 °C, and from 1.3 to 2.5 at 5 °C. Q10 values for this temperature interval ranged 1.5–2.9 (mean 2.3). The two “high-altitude” genera had higher respiration rates at low temperature and oxygen saturation, and their respiration rate saturated at lower temperatures, than three of the four “low-altitude” genera. 3. The oxy-regulatory capacity (critical points and initial decrease in respiration versus oxygen regressions) varied among genera and was affected by temperature. Lachlania, Claudioperla and Anomalocosmoecus had a higher ability to oxy-regulate at low than at high temperatures, Anacroneuria was not clearly affected by temperature, while Polycentropus and Anchytarsus had a greater oxy-regulatory capacity at high than at low temperature. These results indicate that the ability to oxy-regulate is related to the temperature (altitude) at which species naturally occur. 4. Upper altitudinal limits of the six genera were not reflected in their respiratory performance, because all genera had critical minima of temperature and oxygen saturation much lower than those occurring at the limits of their natural distribution. So, the altitudinal limit could not be attributed to absolute short-term physiological tolerance of low temperature and oxygen concentration. 5. Multiple regressions (based on respiration experiments and previously obtained relationships between water temperature, oxygen saturation and altitude) were used to predict how respiration rates should vary with altitude. At the upper limit of the four “low-altitude” genera, respiration rates were 50–68% of those predicted at the centre of the range. With an arbitrary increase of 400 m above the actual limit, the effect of temperature would be a 13% decrease, and that of oxygen a 2% decrease, in respiration rate of Polycentropus, Lachlania and Anacroneuria, while respiration in Anchytarsus would be reduced by 5% by both factors. 6. It seems that, while the immediate decrease in respiration with increased altitude is caused mainly by a decrease in temperature, the long-term survival of a species at given altitudes might be more affected by oxygen saturation. Further quantitative and long-term studies on survival and recruitment in populations and communities are needed to determine the importance of temperature and oxygen for altitudinal limits of aquatic insects.

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

[2]  K. Bérg,et al.  The respiration of some animals from the Profundal Zone of a lake , 2004, Hydrobiologia.

[3]  D. Jacobsen,et al.  Respiration Rate of Stream Insects Measured in situ Along a Large Altitude Range , 2005, Hydrobiologia.

[4]  D. Jacobsen,et al.  Are macroinvertebrates in high altitude streams affected by oxygen deficiency , 2003 .

[5]  C. Lindegaard,et al.  Chironomids (Diptera) and oxy‐regulatory capacity: An experimental approach to paleolimnological interpretation , 2004 .

[6]  D. Jacobsen Altitudinal changes in diversity of macroinvertebrates from small streams in the Ecuadorian Andes , 2003 .

[7]  S. Golubkov,et al.  Dependence of the respiration rate upon oxygen concentration in water for some rheophilous mayfly larvae (Ephemeroptera) , 1989 .

[8]  F. Hayashi Respiratory responses of aquatic insects to low oxygen concentration. , 1989 .

[9]  R. Dudley,et al.  Into thin air: Physiology and evolution of alpine insects. , 2006, Integrative and comparative biology.

[10]  D. Jacobsen Contrasting patterns in local and zonal family richness of stream invertebrates along an Andean altitudinal gradient , 2004 .

[11]  S. Halloy Altitudinal Limits of Life in Subtropical Mountains: What Do We Know? , 1989 .

[12]  A. Nebeker Effect of Low Oxygen Concentration on Survival and Emergence of Aquatic Insects , 1972 .

[13]  N. Walz,et al.  Chaoborus flavicans (Diptera) is an oxy-regulator , 2002 .

[14]  B. Nagell,et al.  Critical oxygen demand in Plecoptera and Ephemeroptera nymphs as determined by two methods , 1981 .

[15]  W. V. Winkle,et al.  Responses of Aquatic Invertebrates to Declining Oxygen Conditions , 1973 .

[16]  J. Stanford,et al.  Thermal Responses in the Evolutionary Ecology of Aquatic Insects , 1982 .

[17]  A. Hildrew,et al.  FACTORS FACILITATING THE COEXISTENCE OF HYDROPSYCHID CADDIS LARVAE (TRICHOPTERA) IN THE SAME RIVER SYSTEM , 1979 .

[18]  Kevin J. Gaston,et al.  Exploring links between physiology and ecology at macro‐scales: the role of respiratory metabolism in insects , 1999 .

[19]  G. Philipson,et al.  Respiratory behaviour of larvae of four species of the Family Polycentropodidae (Trichoptera) , 1976 .

[20]  W. Hilsenhoff Rapid Field Assessment of Organic Pollution with a Family-Level Biotic Index , 1988, Journal of the North American Benthological Society.

[21]  D. Jacobsen The effect of organic pollution on the macroinvertebrate fauna of Ecuadorian highland streams , 1998 .

[22]  L. Benedetto Observations on the Oxygen Needs of Some Species of European Plecoptera , 1970 .

[23]  D. Williams,et al.  Respiratory device or camouflage? ― A case for the caddisfly , 1987 .

[24]  R. Klenke,et al.  Aquatic insect larvae as indicators of limiting minimal contents of dissolved oxygen ‐ part II , 1981 .

[25]  M. Bournaud,et al.  Stream continuum and metabolic rate in the larvae of five species of Hydropsyche (Trichoptera) , 1992 .

[26]  C. Rahbek The role of spatial scale and the perception of large‐scale species‐richness patterns , 2004 .

[27]  T. Reynoldson,et al.  Effects of chronic hypoxia and reduced temperature on survival and growth of burrowing mayflies, (Hexagenia limbata) (Ephemeroptera: Ephemeridae) , 1996 .

[28]  Ole Pedersen,et al.  Respiration of midges (Diptera; Chironomidae) in British Columbian lakes: oxy‐regulation, temperature and their role as palaeo‐indicators , 2008 .

[29]  S. L. Kocharina,et al.  Dependence of the respiration rate of aquatic insects upon the oxygen concentration in running and still water , 1992 .

[30]  R. Pearson,et al.  Effect of low dissolved oxygen on survival, emergence, and drift of tropical stream macroinvertebrates , 2004, Journal of the North American Benthological Society.

[31]  D. Jacobsen Low oxygen pressure as a driving factor for the altitudinal decline in taxon richness of stream macroinvertebrates , 2007, Oecologia.

[32]  J. Hart,et al.  The relation of temperature to oxygen consumption in the goldfish. , 1946, The Anatomical record.

[33]  A. Clarke,et al.  Seasonal acclimatization and latitudinal compensation in metabolism: do they exist? , 1993 .

[34]  B. Nagell The oxygen consumption of mayfly (Ephemeroptera) and stonefly (Plecoptera) larvae at different oxygen concentration , 1973, Hydrobiologia.

[35]  B. W. Sweeney,et al.  Geographic Analysis of Thermal Equilibria: A Conceptual Model for Evaluating the Effect of Natural and Modified Thermal Regimes on Aquatic Insect Communities , 1980, The American Naturalist.

[36]  C. Navas Herpetological diversity along Andean elevational gradients: links with physiological ecology and evolutionary physiology. , 2002, Comparative biochemistry and physiology. Part A, Molecular & integrative physiology.