Insect Metabolic Rates (original) (raw)

Abstract

1 Insect metabolic rates are highly variable and are affected by acute environmental and behavioral, developmental, and evolutionary factors. 2 The effects of temperature on insect metabolic rates depend on their behavior, life-history stage, morphology, and size. In many cases, inactive insect metabolic rates increase with temperature in a manner consistent with the assumptions of the metabolic theory of ecology (MTE), but exceptions include insects that are flying, endothermic, or behaviorally thermoregulating. In these cases metabolic rates may remain constant or decrease with increasing temperature. 3 Insect metabolic rates are not generally constrained by oxygen limitation. 4 The metabolic rates for behaviorally active insects may be elevated up to 30 times greater than their standard resting metabolic rates, an aerobic scope greater than the comparable range found among similarly sized vertebrates. 5 Nutritional state can have dramatic influences on insect metabolic rates, ranging from extreme diapause in response to starvation to nearly 10-fold increases in metabolic rate following feeding. 6 Metabolic rate correlates with insect body size both intra- and interspecifically. The interspecific slope is ¾, as predicted by MTE. Individual insects as well as eusocial insect colonies share common hypometric scaling exponents, but there is extensive variation in the metabolic elevation (i.e., scaling intercept or normalization constant) of these allometric relationships. While some of this variation may be related to methodology and behavioral variation, it is likely that these patterns may reflect previously unrecognized evolutionary differences in physiology and life history. 7 Future extensions of MTE should include physiological, behavioral, and evolutionary mechanisms. Future developments of MTE have great potential to investigate a number of areas in which further research is in highly needed including the evolution of insect endothermy, body size, eusociality, and metabolic symmorphosis.

Figures (7)

Figure 16.1 Insect tracheal systems provide the primary pathway for transporting oxygen from the environment to all of the metabolically active tissues within the body. (A) Synchrotron x-ray phase contrast image (Socha et al. 2007) of the head and thorax of the beetle, Pterostichus stygicus; scale bar: 1 mm. (B) Magnified view of the thorax from the region enclosed by the dotted lines in (A); scale bar: 1 mm (Socha et al. 2007). (C) Confocal microscopy image of the autofluorescent tracheae and tracheoles within the thoracic longitudinal flight muscle of a Drosophila melanogaster male; scale bar: 200 um. (D) Transmission electron microscopy image of a single taenidia-reinforced tracheole (t) positioned near mitochondria (m) within the flight muscle of Drosophila; scale bar: 1 um. Data for (C) and (D) were collected by the authors at the Bioimaging Facility in the School of Life Sciences at Arizona State University.

Figure 16.1 Insect tracheal systems provide the primary pathway for transporting oxygen from the environment to all of the metabolically active tissues within the body. (A) Synchrotron x-ray phase contrast image (Socha et al. 2007) of the head and thorax of the beetle, Pterostichus stygicus; scale bar: 1 mm. (B) Magnified view of the thorax from the region enclosed by the dotted lines in (A); scale bar: 1 mm (Socha et al. 2007). (C) Confocal microscopy image of the autofluorescent tracheae and tracheoles within the thoracic longitudinal flight muscle of a Drosophila melanogaster male; scale bar: 200 um. (D) Transmission electron microscopy image of a single taenidia-reinforced tracheole (t) positioned near mitochondria (m) within the flight muscle of Drosophila; scale bar: 1 um. Data for (C) and (D) were collected by the authors at the Bioimaging Facility in the School of Life Sciences at Arizona State University.

Figure 16.2 Insect metabolic rates are sensitive to temperature and dependent on behavioral and environmental factors. In (A), the mass-specific metabolic rates for 31 insect species from eight taxonomic orders and also ranging across eight orders of magnitude in body size are plotted as a function of air temperature. There is a common trend of insect metabolic rates increasing with temperature in the majority of sampled studies but there are also a number of exceptions. In particular, highly metabolically active, endothermic insects (e.g., endothermic flying insects, cold-exposed honeybee swarms) tend to show little effect of air temperature on metabolic rate, or even an inverse relationship. The coefficients of the linear regressions describing the rate-temperature relationships are provided with asterisks (*) indicating whether the slope or intercept of the fitted data are significantly (p < 0.05) different from the coefficients of the common regression parameters shared by the majority of inactive insects. Note that the intercept estimates and their standard error are in log-transformed units. (B) Frequency distribution of activation energies of insects. Activation energies were obtained as the slopes of OLS regressions of the natural logarithm of mass-specific metabolic rate as a function of inverse absolute temperature for the 35 analyzed datasets. References for the data analyzed in (A) and (B) include: ant colonies (Lighton 1989), flying insects (Casey and Ellington 1989), hovering bees (Roberts et al. 1998; Harrison and Fewell 2002), honeybee colonies (Heinrich 1980), inactive insects (Casey 1977; Herreid et al. 1981; Chappell 1983, 1984; Morgan et al. 1985; Casey and Knapp 1987; Schultz et al. 1992; Vogt and Appel 1999; Fielden et al. 2004; Klok and Chown 2005; Terblanche and Chown 2007), pre-flight warm-up (Casey and Hegel-Little 1987), scarab beetles (Davis et al. 2000), and whiteflies (Salvucci and Crafts-Brandner 2000).

Figure 16.2 Insect metabolic rates are sensitive to temperature and dependent on behavioral and environmental factors. In (A), the mass-specific metabolic rates for 31 insect species from eight taxonomic orders and also ranging across eight orders of magnitude in body size are plotted as a function of air temperature. There is a common trend of insect metabolic rates increasing with temperature in the majority of sampled studies but there are also a number of exceptions. In particular, highly metabolically active, endothermic insects (e.g., endothermic flying insects, cold-exposed honeybee swarms) tend to show little effect of air temperature on metabolic rate, or even an inverse relationship. The coefficients of the linear regressions describing the rate-temperature relationships are provided with asterisks (*) indicating whether the slope or intercept of the fitted data are significantly (p < 0.05) different from the coefficients of the common regression parameters shared by the majority of inactive insects. Note that the intercept estimates and their standard error are in log-transformed units. (B) Frequency distribution of activation energies of insects. Activation energies were obtained as the slopes of OLS regressions of the natural logarithm of mass-specific metabolic rate as a function of inverse absolute temperature for the 35 analyzed datasets. References for the data analyzed in (A) and (B) include: ant colonies (Lighton 1989), flying insects (Casey and Ellington 1989), hovering bees (Roberts et al. 1998; Harrison and Fewell 2002), honeybee colonies (Heinrich 1980), inactive insects (Casey 1977; Herreid et al. 1981; Chappell 1983, 1984; Morgan et al. 1985; Casey and Knapp 1987; Schultz et al. 1992; Vogt and Appel 1999; Fielden et al. 2004; Klok and Chown 2005; Terblanche and Chown 2007), pre-flight warm-up (Casey and Hegel-Little 1987), scarab beetles (Davis et al. 2000), and whiteflies (Salvucci and Crafts-Brandner 2000).

Figure 16.3 To quantify the safety margin for oxygen delivery, organism function can be measured over a range of oxygen partial pressures; the partial pressure (pO2) at which the activity measure significantly decreases is referred to as that organism’s critical oxygen partial pressure. The critical pO, for the metabolic rate of adult D. melanogaster is 3 kPa or at about 85% less oxygen than normal, with a safety margin of 18kPa O; (Van Voorhies 2009). in which VO, indicates an organism’s oxygen con- sumption rate, G the conductance of the respiratory system, and APO, the partial pressure gradient for oxygen from atmosphere to mitochondria. G is a measure of the capacity of the respiratory system to transport oxygen, and in this simplified case represents the combination of both diffusive and convective con- ductance (Buck 1962). If ambient oxygen level is slowly lowered, and APO, drops, animals will typically increase the conductance of their respiratory system (in the case of insects, by opening spiracles and increas- ing ventilation) to maintain a constant VO,. Over this range, the organism is within its safety margin for oxygen transport and is not supply limited. The organ- ism’s critical pO, for that particular function is defined as the pO, when oxygen becomes limiting and below which VO, decreases (Fig. 16.3). We know from work

Figure 16.3 To quantify the safety margin for oxygen delivery, organism function can be measured over a range of oxygen partial pressures; the partial pressure (pO2) at which the activity measure significantly decreases is referred to as that organism’s critical oxygen partial pressure. The critical pO, for the metabolic rate of adult D. melanogaster is 3 kPa or at about 85% less oxygen than normal, with a safety margin of 18kPa O; (Van Voorhies 2009). in which VO, indicates an organism’s oxygen con- sumption rate, G the conductance of the respiratory system, and APO, the partial pressure gradient for oxygen from atmosphere to mitochondria. G is a measure of the capacity of the respiratory system to transport oxygen, and in this simplified case represents the combination of both diffusive and convective con- ductance (Buck 1962). If ambient oxygen level is slowly lowered, and APO, drops, animals will typically increase the conductance of their respiratory system (in the case of insects, by opening spiracles and increas- ing ventilation) to maintain a constant VO,. Over this range, the organism is within its safety margin for oxygen transport and is not supply limited. The organ- ism’s critical pO, for that particular function is defined as the pO, when oxygen becomes limiting and below which VO, decreases (Fig. 16.3). We know from work

Figure 16.4 Insects often exhibit an impressively broad safety margin for maintaining measures of activity (e.g., O2 consumption, CO, emission, performance) in spite of reduced partial pressures of oxygen in their environment. This figure plots the range of critical pO, in the literature for a diverse range of insects and their behaviors. Critical pO, tends to be higher in active insects. In cases where hyperoxic values are reported, this indicates that the measure of activity (i.e. dragonfly CO, emission and grasshopper jumping performance) increased in hyperoxia relative to normoxia. Normal pO, is 21 kPa, as indicated by the dotted line. The letter superscript associated with each row indicates the reference for that dataset: a (Harrison et al. 2006b), b (Zhou et al. 2000), c (Chappell and Rogowitz 2000), d (Klok et al. 2010), e (Greenlee and Harrison 2005), f (Greenlee and Harrison 2004a), g (Kirkton et al. 2005), h (Joos et al. 1997; Rascon and Harrison 2005), and i (Harrison and Lighton 1998). While oxygen supply seems to meet demand as insects increase in size, this may occur because larger insects exhibit an increased investment in respiratory structure. Larger tenebrionid beetle species have a greater fraction of their body devoted to the tracheal system, and extrapolations of these trends suggest that this pattern could explain oxygen limitations on insect size (Kaiser et al. 2007). Similar hypermetric patterns Most inactive insects exhibit very low critical pO, values (Fig. 16.4), clearly indicating that resting meta- bolic rate is not oxygen-limited. However, critical pO, values do tend to be higher when metabolic rate is elevated, as during flight (Fig. 16.4). When compari-

Figure 16.4 Insects often exhibit an impressively broad safety margin for maintaining measures of activity (e.g., O2 consumption, CO, emission, performance) in spite of reduced partial pressures of oxygen in their environment. This figure plots the range of critical pO, in the literature for a diverse range of insects and their behaviors. Critical pO, tends to be higher in active insects. In cases where hyperoxic values are reported, this indicates that the measure of activity (i.e. dragonfly CO, emission and grasshopper jumping performance) increased in hyperoxia relative to normoxia. Normal pO, is 21 kPa, as indicated by the dotted line. The letter superscript associated with each row indicates the reference for that dataset: a (Harrison et al. 2006b), b (Zhou et al. 2000), c (Chappell and Rogowitz 2000), d (Klok et al. 2010), e (Greenlee and Harrison 2005), f (Greenlee and Harrison 2004a), g (Kirkton et al. 2005), h (Joos et al. 1997; Rascon and Harrison 2005), and i (Harrison and Lighton 1998). While oxygen supply seems to meet demand as insects increase in size, this may occur because larger insects exhibit an increased investment in respiratory structure. Larger tenebrionid beetle species have a greater fraction of their body devoted to the tracheal system, and extrapolations of these trends suggest that this pattern could explain oxygen limitations on insect size (Kaiser et al. 2007). Similar hypermetric patterns Most inactive insects exhibit very low critical pO, values (Fig. 16.4), clearly indicating that resting meta- bolic rate is not oxygen-limited. However, critical pO, values do tend to be higher when metabolic rate is elevated, as during flight (Fig. 16.4). When compari-

Figure 16.5 The allometry of body composition provides insight into the unusual intraspecific hypometric scaling of metabolic rate with body size in the carpenter bee, Xylocopa varipuncta. This figure, adapted from Roberts et al (2004), shows in (A) that body mass-specific metabolic rates decrease very strongly with body mass (so whole-organism rates scale with M~°? for maximal performance in hypodense air and M®”” for normal hovering). This pattern occurs because the relative content of thorax muscle mass (the major site of oxygen consumption during flight) decreases with body size (B).

Figure 16.5 The allometry of body composition provides insight into the unusual intraspecific hypometric scaling of metabolic rate with body size in the carpenter bee, Xylocopa varipuncta. This figure, adapted from Roberts et al (2004), shows in (A) that body mass-specific metabolic rates decrease very strongly with body mass (so whole-organism rates scale with M~°? for maximal performance in hypodense air and M®”” for normal hovering). This pattern occurs because the relative content of thorax muscle mass (the major site of oxygen consumption during flight) decreases with body size (B).

Figure 16.6 Allometry of colony metabolic rate in three colonial species compared with individual metabolic rate in seven solitary species. Social insect colonies, like individual insects, exhibit metabolic rates that scale hypometrically with mass. Thi figure combines intraspecific data for individual ants (Chown et al. 2007), two functioning whole ant colony species (Shik 2010; Waters et al. 2010), and thermoregulating honeybee clusters (Southwick et al. 1990). The OLS regression results for each group are displayed above (slopes are given with standard errors) and the overall model, which fits a separate slope and intercept for each species, has an r? = 0.99. The average homogenous slope was 0.62 and the only species that show significantly higher than average scaling slopes are Eciton hamatum (slope: 0.83, p < 0.003) and P. dentata (slope: 0.78, p< 0.002).

Figure 16.6 Allometry of colony metabolic rate in three colonial species compared with individual metabolic rate in seven solitary species. Social insect colonies, like individual insects, exhibit metabolic rates that scale hypometrically with mass. Thi figure combines intraspecific data for individual ants (Chown et al. 2007), two functioning whole ant colony species (Shik 2010; Waters et al. 2010), and thermoregulating honeybee clusters (Southwick et al. 1990). The OLS regression results for each group are displayed above (slopes are given with standard errors) and the overall model, which fits a separate slope and intercept for each species, has an r? = 0.99. The average homogenous slope was 0.62 and the only species that show significantly higher than average scaling slopes are Eciton hamatum (slope: 0.83, p < 0.003) and P. dentata (slope: 0.78, p< 0.002).

Figure 16.7 The hypometric scaling of inactive insect metabolic rates (Chown 2007) is generally consistent with the pattern observed for mammals (Savage et al. 2004b); both taxa exhibit similar 3/4-power scaling slopes but insects have lower intercepts or normalization constants. In (A) the metabolic rates for 391 insect species have been adjusted using the Arrhenius equation to 37°C, a standard mammalian body temperature (see Brown and Sibly, Chapter 2). Independent of mass, inactive insects have metabolic rates about two times lower than inactive mammals with the same body temperature (figure inset displays the intercept values from the OLS regression on log-log data). (B) The interspecific data on insect metabolic rates at 25°C (Chown 2007) can be analyzed by taxonomic order. A linear model that fits unique slopes and intercepts for each order was not a significantly better model than one that preserved a common slope (0.72 + 0.2 SE) but allowed for variation in intercepts by order. The maximum intercept (Diptera, 3.5 mW) was more than 18 times greater than the minimal intercept (Isoptera, 0.19 mW). Part of this variation may be due to behavioral variation among “inactive” insects, and methodological variation among researchers, but the data suggest substantial order-level variation in inactive metabolic rates among insects.

Figure 16.7 The hypometric scaling of inactive insect metabolic rates (Chown 2007) is generally consistent with the pattern observed for mammals (Savage et al. 2004b); both taxa exhibit similar 3/4-power scaling slopes but insects have lower intercepts or normalization constants. In (A) the metabolic rates for 391 insect species have been adjusted using the Arrhenius equation to 37°C, a standard mammalian body temperature (see Brown and Sibly, Chapter 2). Independent of mass, inactive insects have metabolic rates about two times lower than inactive mammals with the same body temperature (figure inset displays the intercept values from the OLS regression on log-log data). (B) The interspecific data on insect metabolic rates at 25°C (Chown 2007) can be analyzed by taxonomic order. A linear model that fits unique slopes and intercepts for each order was not a significantly better model than one that preserved a common slope (0.72 + 0.2 SE) but allowed for variation in intercepts by order. The maximum intercept (Diptera, 3.5 mW) was more than 18 times greater than the minimal intercept (Isoptera, 0.19 mW). Part of this variation may be due to behavioral variation among “inactive” insects, and methodological variation among researchers, but the data suggest substantial order-level variation in inactive metabolic rates among insects.

Key takeaways

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  1. Insect metabolic rates vary significantly due to environmental, behavioral, and evolutionary factors.
  2. Active insects can have metabolic rates up to 30 times their standard resting rates.
  3. Temperature effects on metabolism are inconsistent depending on insect behavior and life stages.
  4. Metabolic rates correlate with body size, showing a ¾ interspecific slope, as predicted by metabolic theory.
  5. Future research should integrate physiological and evolutionary mechanisms into metabolic theory of ecology extensions.

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