Influence of Body Size and Environmental Temperature on Carbon ...

PHYSIOLOGICAL ECOLOGY

Influence of Body Size and Environmental Temperature on Carbon Dioxide Production by Forest Centipedes from Southwestern North America LINDSEY A. PENNINGTON

AND

TIMOTHY D. MEEHAN1

Department of Sciences and Conservation Studies, College of Santa Fe, 1600 Saint Michaels Drive, Santa Fe, NM 87505

Environ. Entomol. 36(4): 673Ð680 (2007)

ABSTRACT We conducted a laboratory study to evaluate the mass and temperature dependence of carbon dioxide production by three dominant centipede speciesÑArctogeophilus umbraticus McNeill, Gonibius glyptocephalus Chamberlin, and Oabius sp.Ñfrom a montane forest in southwestern North America. We found that CO2 production (Q, ␮l/h) of resting, nonfasted individuals was related to body mass (M, mg live) and environmental temperature (T, K) as Q ⫽ e18.32M0.82e⫺0.49/kT, where e is the base of the natural logarithm and k is BoltzmannÕs constant (8.62 ⫻ 10⫺5 eV/K). Our results indicated that the mass and temperature dependence of centipede metabolism is comparable with that of other arthropods. They also supported previous claims that centipede metabolic rate, for a given mass and temperature, is relatively low compared with other arthropods. Suggestions are given for using resulting metabolic rate equations in conjunction with data on abundance, body size, and environmental temperature to assess energy ßux by centipede populations. KEY WORDS body mass, Chilopoda, environmental temperature, metabolic rate, New Mexico

Whole organism metabolic rate is the rate at which an individual transforms matter and energy for maintenance, growth, and reproduction. Metabolic rate reßects the pace of an organismÕs life and is linked to life history characteristics such as development time (Peters 1983, Gillooly et al. 2002) and reproductive rate (Banse and Mosher 1980, Savage et al. 2004a) and to ecological patterns and processes such as population density (Damuth 1981, Allen et al. 2002, Meehan 2006a) and energy ßux (Nielsen 1961, Enquist et al. 2003, Allen et al. 2005). The metabolic rate of an individual organism is not static but varies considerably depending on several factors that reßect its physiological state. These factors include age, reproductive status, activity level, and nutritional status. Given this variation, an assortment of metabolic rate types has been devised for measuring and comparing metabolic rates across organisms. For ectothermic animals, standard metabolic rate (SMR) is generally considered the minimum metabolic rate necessary for physiological maintenance. It is deÞned as the lowest observed metabolic rate at a standard temperature for an animal that is rested, awake, physically inactive, and has fasted for a speciÞed period (IUPS 2001). Opposite SMR is maximum metabolic rate, which is the highest observed metabolic rate recorded during a speciÞed period of work compatible 1 Corresponding author: Department of Entomology, University of Wisconsin, Madison, WI 53706 (e-mail: [email protected]. edu).

with sustained aerobic metabolism. Between these two metabolic endpoints exists resting metabolic rate (RMR), the rate of energy consumption by an animal that is resting but not fasted (IUPS 2001). RMR is typically near SMR, but is not a true measure of minimal maintenance metabolism because it incorporates energy consumption associated with minimal activity and digestion (speciÞc dynamic effect). Metabolic rates also vary considerably across animals. For ectothermic organisms, the two factors that account for the largest share of that variation are body mass and environmental temperature. The relationship between metabolic rate, R, and body mass, M, is typically represented by the power function R ⬀ Mb (Huxley 1932, Kleiber 1932, Hemmingsen 1960, Peters 1983, Gillooly et al. 2001, Glazier 2005). The mechanistic determinants and the exact value of the scaling exponent b are currently debated (Dodds et al. 2001, Banavar et al. 2002, Darveau et al. 2002, Makarieva et al. 2005, West and Brown 2005). However, the power function form is widely accepted, and empirical estimates of b typically fall between 0.50 and 1.00 and tend toward 0.75 (Peters 1983, Withers 1992, Savage et al. 2004b, Glazier 2005). The relationship between metabolic rate and environmental temperature, T, has been represented in several ways. The most common way of describing the temperature dependence of ectotherm metabolic rate is with a Q10 factor (vanÕt Hoff 1896), which describes the factorial increase in a rate with a 10⬚C increase in temperature. Although Q10 is intuitively satisfying, it

0046-225X/07/0673Ð0680$04.00/0 䉷 2007 Entomological Society of America

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does not Þt well within a multivariate analysis of metabolic rates. One simple mathematical form for temperature dependence that is commonly used in a multivariate context is R ⬀ ecT (Robinson et al. 1983, Clarke 2004), where T is in ⬚C and c is a rate constant equal to 0.1 ⫻ ln(Q10). Another widely used form is the Arrhenius or Boltzmann equation R ⬀ e⫺␮/kT (Crozier 1924, Clarke and Johnston 1999, Gillooly et al. 2001). The Arrhenius and Boltzmann equations were developed to describe the effects of absolute temperature on simple chemical reactions. In that context, ␮ represents the activation energy of the reaction and k represents either the universal gas constant or BoltzmannÕs constant. These equations also work well as statistical descriptions of temperature dependence for complex biological processes, such as metabolism (Withers 1992, Clarke 2004, 2006). In this context, ␮ denotes the “critical thermal increment” or “apparent activation energy” of the whole biological process (Withers 1992). When k is substituted with BoltzmannÕs constant (0.0000862 eV/K), empirical estimates for the critical thermal increment for various taxa have ranged from 0.25 to 0.79 eV (Gillooly et al. 2001, Vasseur and McCann 2005, Meehan 2006b). The mass and temperature dependence of metabolic rate has been studied for a great variety of animal species. For terrestrial invertebrates, in particular, mass and temperature dependence has been studied for insects (Persson and Lohm 1977, Petersen 1981, Lighton and Fielden 1995, Addo-Bediako et al. 2002, Niven and Scharlemann 2005, Meehan 2006b), arachnids (Berthet 1964, Anderson 1970, Wood and Lawton 1973, Luxton 1975, Greenstone and Bennett 1980, Lighton and Fielden 1995, Meehan 2006b), isopods (Phillipson and Watson 1965, Al-Dabbagh and Marina 1986), millipedes (Frears et al. 1996), and oligochaetes (Nielsen 1961, Gromadska 1962, Byzova 1965, Phillipson and Bolton 1976, Meehan 2006b). Compared with other terrestrial invertebrates, however, there has been relatively little published on the mass and temperature dependence of centipede metabolism (Crawford et al. 1975, Riddle 1975, Albert 1983b, Poser 1988, Klok et al. 2002). Here we report on a laboratory study of the mass and temperature dependence of RMR for three dominant species of litter- and soil-dwelling centipedes living in a montane forest in southwestern North America. Centipedes are thought to be important predators in detrital food webs (Coleman et al. 2004), and they are the most abundant macroinvertebrate predators in our study system (Meehan et al. 2006). The main objective of our study was to produce models for predicting metabolic rates that could eventually be used to quantify the role of centipedes in the local soil food web in energetic terms (Bornebusch 1930, Phillipson 1971, Albert 1983a). Materials and Methods The centipedes included in this study were collected from an aspen (Populus tremuloides Michx.)

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and conifer [Pseudotsuga menziesii (Mirb.) Franco, Pinus ponderosa Douglas ex Lawson and C. Lawson] forest at ⬇3,020 m elevation in the Sangre de Cristo Mountains of northern New Mexico. The collection area was centered at ⬇35.7735⬚ N, 105.8149⬚ W latitude and longitude (WGS84 and NAD83 coordinate system). The mean annual temperature at the collection site is ⬇0⬚C, and total annual precipitation is ⬇700 mm (Gosz 1980, Yin 1999). Adult centipedes were collected haphazardly during May through October 2005 from under leaf litter and decaying logs. Immediately after capture, centipedes were taken to the laboratory and stored in large plastic containers with their native soil and plant debris, so that they had access to familiar prey until metabolic rate measurements were made (Albert 1983b). Centipedes were left in plastic containers in the laboratory at 20⬚C for 5Ð10 d before metabolic rate measurements were made. Centipedes were from three dominant taxa: Arctogeophilus umbraticus McNeill (Geophilidae), Gonibius glyptocephalus Chamberlin (Lithobiidae), and Oabius sp. (Lithobiidae). Voucher specimens of animals included in this study were archived with the Arthropod Division of the Museum of Southwestern Biology at the University of New Mexico, Albuquerque, NM. The RMR of an animal can be represented in terms of heat production, oxygen consumption, or carbon dioxide production rate. These rates are related by simple constants and can be converted back and forth using known or assumed respiratory quotients and oxyenergetic coefÞcients (Petrusewicz and Macfadyen 1970, Prus 1975). We used constant-pressure respirometers to measure RMR in terms of carbon dioxide production. Constant-pressure respirometers have been a standard tool for measuring arthropod metabolic rate for many years (Petrusewicz and Macfadyen 1970, Klekowski 1975), and the particular style of respirometers that we used have been implemented in several previous studies (Lee and Baust 1982a, b, Bennett and Lee 1989, Lee 1995). Each respirometer was comprised of a plastic 3-ml syringe with a 75-␮l pipette glued onto the needle hub (Fig. 1a). For each experimental trial, a single centipede was weighed to 0.1 mg and placed into a respirometer, and the plunger was inserted into the respirometer so that there was ⬇3 ml of air space remaining (Fig. 1a). A wet piece of tissue paper was also placed in each respirometer to maintain high relative humidity throughout an experimental trial. Loaded respirometers were placed in a glass-sided water bath with the tip of the pipettes ⬇3 mm above the water surface (Fig. 1a). Centipedes were allowed to sit in submerged respirometers for ⬇1 h before measurements began, so that they would recover from handling stress and settle into a resting state. The activity of animals was monitored during RMR measurements. If individuals were consistently active, their metabolic rate measurements were not included in subsequent analyses. After the 1-h adjustment period, a drop of 2 M KOH solution, tinted with food coloring, was placed into the pipette of each respirometer using a hypodermic nee-

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fect of temperature changes on the position of the KOH in the pipette. The position of KOH in the pipette was converted to respirometer volume using the length to volume ratio of the pipette. Respirometer volume was regressed against the time the photo was taken to calculate the CO2 production rate for the animal in each respirometer (Fig. 1b). R2 values for regressions of volume against time ranged from 0.73 to 0.99, although most were between 0.90 and 1.00 (Fig. 1b). CO2 production was measured in this way at 9, 19, and 29⬚C and between 1300 and 2200 hours. All resulting CO2 production rates were adjusted to standard temperature and pressure. Following the discussion above, the relationship between carbon dioxide production, Q (␮l/h), body mass (mg live), and environmental temperature (K) can be described by the following equation (Gillooly et al. 2001): Q ⫽ qMbe⫺␮/kT.

[1a]

Here, q is a normalizing constant (␮l/h⫺1/mg⫺b), ␮ is the critical thermal increment of RMR, and k is BoltzmannÕs constant. Taking the natural logarithm of both sides of equation 1a gives a linear form that can be Þtted to natural log-transformed data using general linear modeling techniques (Ramsey and Shafer 1996). The linear form used in this analysis was: ln(Q)⫽b0⫹b1(ln[M]) ⫺ b2(1/kT).

[1b]

In this equation, b0 corresponds with the natural logarithm of q in equation 1a, b1 corresponds with b, and b2 corresponds with ␮. To determine if there was statistically signiÞcant variation in mass and temperature dependence across the three species, we began the analysis with the interaction model: Fig. 1. Respirometry methods used in this study. (a) Photograph of 10 respirometers containing centipedes, 2 control respirometers, water bath, reference ruler, and thermometer. Note the arrows pointing to the drop of KOH solution (above) and a centipede resting on wet tissue paper (below) in the inset. (b) Data on decrease in volume (␮l) over time (h) for four representative respirometers. CO2 production per animal was the slope of the least squares regression line.

dle. As centipedes respired, CO2 was absorbed by the KOH, which caused compensatory movement of KOH down the pipette (Fig. 1a). The progression of the KOH down the pipette was photographed using a digital camera (Canon PowerShot A400, Lake Success, NY) interfaced with a desktop computer using PSRemote software (Breeze Systems, Surrey, UK). The PSRemote software was programmed to take photographs of respirometers every 15Ð30 min for 3Ð 6 h, depending on the sizes of the centipedes in the respirometers. Scion Image analysis software (Scion Corp., Frederick, MD) was used to measure the position of the KOH on each photograph. A control respirometer (thermobarometer), without a centipede but with moist tissue paper, was used during each experimental trial to correct for the confounding ef-

ln(Q) ⫽ b0⫹b1(ln[M]) ⫺ b2(1/kT) ⫹ b3(S) ⫹ b4(ln[M] ⫻ S) ⫹ b5([1/kT] ⫻ S)

[2]

Here, S represents species, ln[M] ⫻ S represents an interaction between species and mass, and [1/kT] ⫻ S represents an interaction between species and environmental temperature. In this context, a statistically signiÞcant coefÞcient for S (b3) would indicate that there was a difference in model intercepts across species. Statistically signiÞcant coefÞcients for the interaction terms (b4 and b5) would indicate that the mass exponents and critical thermal increments were signiÞcantly different across species. We used F-tests based on type III sums of squares to determine the statistical signiÞcance of model coefÞcients (Ramsey and Shafer 1996). Results and Discussion The live masses of the 50 centipedes included in this study varied from 1.60 to 76.10 mg, whereas experimental temperatures ranged from 9 to 29⬚C, and CO2 production rates ranged from 0.44 to 27.91 ␮l/h. In general, CO2 production rates increased with body mass and environmental temperature (Fig. 2).

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and temperature dependence of metabolic rate could be modeled with a single equation for all three species. The Þnal model (F2,47 ⫽ 190.49, P ⬍ 0.001, R2 ⫽ 0.89; Fig. 2) for CO2 production by all three centipede species was: ln(Q) ⫽ 18.32 ⫹ 0.82共ln[M]) ⫺ 0.49共1/kT). [3a] The 95% conÞdence intervals for the intercept, mass (F1,47 ⫽ 274.66, P ⬍ 0.001), and temperature (F1,47 ⫽ 106.31, P ⬍ 0.001) coefÞcients were 14.56 Ð22.08, 0.721Ð 0.92, and 0.58 Ð 0.39, respectively. Exponentiation of both sides of equation 3a gave the nonlinear form of the Þnal model: Q ⫽ e18.32M0.82e⫺0.49/kT.

Fig. 2. Mass and temperature dependence of carbon dioxide production by three species of centipedes. (a) x-axis is natural log of live mass (mg) and y-axis is the natural log of CO2 production (␮l/h) corrected for environmental temperature (K), where 0.49 eV is the critical thermal increment from equation 3 and k is BoltzmannÕs constant (8.62 ⫻ 10⫺5 eV/K). (b) x-axis is inverse of environmental temperature multiplied by BoltzmannÕs constant and y-axis is natural log of CO2 production corrected for live mass, where 0.82 is the mass scaling exponent from equation 3. E, A. umbraticus; ‚, G. glyptocephalus; 䉫, Oabius sp.

Analysis of variance (ANOVA) indicated that there was not a signiÞcant interaction between taxon and mass (b4 in equation 2; F2,41 ⫽ 1.21, P ⫽ 0.31) or between taxon and temperature (b5 in equation 2; F2,41 ⫽ 1.92, P ⫽ 0.16). This indicated that the scaling exponents for mass and the critical thermal increments were not signiÞcantly different across the three species. When we removed the interaction terms from the model, there was not a signiÞcant effect of taxonomic group (b3 in equation 2; F2,45 ⫽ 1.84, P ⫽ 0.17) on CO2 production rate. This indicated that the model intercept was not signiÞcantly different across the three species. Thus, ANOVA suggested that the mass

[3b]

According to equation 3, centipede CO2 production scaled with body mass raised to the power of 0.82. This mass scaling exponent was comparable to that found in a variety of empirical studies of terrestrial invertebrate metabolic rate. For example, other studies have given mass-scaling exponents of 0.81 (Ryszkowski 1975) and 0.82 (Riechle 1968) for multiple terrestrial invertebrate taxa; 0.62 (Kayser and Huesner 1964), 0.76 (Zotin and Konoplev 1978), 0.66 (Niven and Scharlemann 2005), and 0.77 (Addo-Bediako et al. 2002) for insects; 0.73 for ants, beetles, spiders, and millipedes (Lighton and Fielden 1995, Frears et al. 1996); 0.77 for spiders, oribatid mites, and springtails (Meehan 2006b); and 0.77 (Kayser and Huesner 1964) and 0.74 (Persson and Lohm 1977) for beetles. The critical thermal increment associated with centipede CO2 production was 0.49 eV (equation 3). This value was within the range of values observed for 46 species of spiders, 42 species of oribatid mites, and 24 species of springtails (0.58 eV), 11 species of earthworms (0.25 eV), and 14 species of isopods (0.48 eV) reported by Meehan (2006b). The observed thermal increment was also within the range of 0.39 Ð 0.79 eV found for different collections of terrestrial and aquatic invertebrates (Gillooly et al. 2001, Vasseur and McCann 2005). Critical thermal increments and Q10 values can be equated to one another using the for2 mula Q10 ⫽ e␮/0.1(kT0) , where T0 is the midpoint of the temperature range (K) over which Q10 was estimated (Gillooly et al. 2001, Vasseur and McCann 2005). Using this equation, we found that the critical thermal increment from our study (equation 3) corresponded with a Q10 factor of 1.93 for the temperature range of 15Ð25⬚C. This value is close to those reported in large scale studies on the temperature dependence of metabolic rate (Robinson et al. 1983, Clarke and Johnston 1999) and is close to the range of 2Ð3 that is often cited for the Q10 of biological rates in general (Withers 1992, Hill et al. 2004). Our data can be combined with those from other studies to produce an updated general model for the mass and temperature dependence of centipede metabolism (Table 1). For instance, Albert (1983b) studied O2 consumption by variously sized individuals from two species of centipedes at 1, 5, 10, 12, and 15⬚C.

August 2007 Table 1.


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Metabolic rate (␮W) for 12 centipede species with associated environmental temperatures (°C) and live body masses (mg)

Taxon

Body temp

Cormocephalus morsitans Cormocephalus brevicornis Cormocephalus elegans Scutigerina weberi Lithobius melanops Scolopendra polymorpha

20 20 20 20 20 20

Nadabius coloradensis Lithobius mutibilis

Lithobius curtipes

Oabius sp.

Arctogeophilus umbraticus

Gonibius glyptocephalus

Metabolic rate

Rate type

1,612 77 1,175 106 21 1,500

237.55 19.71 474.60 103.35 30.96 581.56

SMR SMR SMR SMR SMR SMR

20

13

9.59

SMR

1 5 10 12 15 1 5 10 12 15 9 19 29 9 19 29 9 19 29

5 10 15 20 25 5 10 15 20 25 4.6 5.4 6.1 12.2 6.3 11.3 52.5 44.3 47.4

1.27 3.30 7.72 11.89 19.52 1.15 3.43 8.71 14.23 24.41 3.78 8.49 21.88 8.35 11.07 34.08 47.54 48.87 117.02

RMR RMR RMR RMR RMR RMR RMR RMR RMR RMR RMR RMR RMR RMR RMR RMR RMR RMR RMR

Mass

Like our study, the measurements of Albert were conducted in constant-pressure respirometers under RMR conditions. We used equations provided by Albert to calculate average O2 consumption rates for 5Ð25 mg centipedes at the Þve experimental temperatures. We converted O2 consumption rates to metabolic rates in microwatts using an oxyenergetic coefÞcient of 20.05 J/ml O2 (Albert 1983b). Next, we used an assumed respiratory quotient of 0.84 (Klok et al. 2002) and the same oxyenergetic coefÞcient of 20.05 J/ml O2 to convert CO2 production rates found during this study to metabolic rates in microwatts. We combined the converted RMR estimates from this and the study of Albert (1983b) with data from Klok et al. (2002), who reported SMR for Þve species of centipedes at 20⬚C. The study of Klok et al. also included SMR data originally reported by Crawford et al. (1975) and Riddle (1975) for two additional centipede species. We analyzed this new compilation of data for 12 species (Table 1) using a general linear model with the same form as equation 1b, but with an additional term that indicated whether measurements were SMR or RMR. The resulting dependence of metabolic rate, R (␮W), on body mass (F1,22 ⫽ 162.04, P ⬍ 0.001), absolute temperature (F1,22 ⫽ 82.41, P ⬍ 0.001), and experimental conditions, C (C ⫽ 0 for SMR and one for RMR; F1,22 ⫽ 6.65, P ⫽ 0.02), was as follows: ln(R) ⫽ 26.64 ⫹ 0.79共ln[M]) ⫺ 0.66共1/kT) ⫹ 0.61(C) [4a] Exponentiation of both sides of equation 4a gave the nonlinear form of the model: R ⫽ e26.64M0.79e⫺0.66/kTe0.61C.

[4b]

Reference Klok et al. 2002 Klok et al. 2002 Klok et al. 2002 Klok et al. 2002 Klok et al. 2002 Crawford et al. 1975 in Klok et al. 2002 Riddle 1975 in Klok et al. 2002 Albert 1983b Albert 1983b Albert 1983b Albert 1983b Albert 1983b Albert 1983b Albert 1983b Albert 1983b Albert 1983b Albert 1983b This study This study This study This study This study This study This study This study This study

When equation 4 (F3,22 ⫽ 147.81, P ⬍ 0.001, R2 ⫽ 0.95; Fig. 3) is viewed in light of the above discussion, it is clear that the mass and temperature dependence of centipede metabolism is comparable with that of other invertebrates. Equation 4 also shows that, for centipedes, estimates of metabolic rate made under RMR conditions were e0.61 ⫽ 1.83 times estimates made under of SMR conditions. This 83% increase in energy use likely reßects the energy spent on occasional spontaneous activity in respirometers and the digestion of prey consumed before metabolic rate measurements were conducted. Regarding absolute metabolic rates, equation 4 predicts that the SMR of a 25-mg centipede at 25⬚C would be 28.51 ␮W. According to the SMR equation of Lighton and Fielden (1995), a “typical” arthropod at that size and temperature would have an SMR of 43.19 ␮W. Hence, centipede SMR seems to be 66% of that of a typical arthropod. This result supports the suggestion by Klok et al. (2002) that centipede metabolic rates tend to be lower than those of other invertebrates. Models of metabolic rate produced from respiration studies conducted in the laboratory can be expected to underestimate the energy consumed by centipedes in the wild (Wightman 1981). However, with some modiÞcation, the models resulting from this study can be adjusted to approximate centipede Þeld metabolic rate (FMR). Researchers using radioisotopic methods to estimate the FMR of various terrestrial invertebrates have found that those estimates range from 1.45 (Nielsen and Jensen 1977) to 3.57 (Van Hook 1971) times FMR estimates calculated from RMR measurements conducted in constant-pressure or constantvolume respirometers. Given these results, Albert

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between SMR and FMR in other organisms (Withers 1992). With these adjustments in mind, information on abundance, body mass, and environmental temperature can be combined with models presented here to estimate the metabolic rates of centipedes in the wild and assess the energetic roles of centipedes in detrital food webs.

Acknowledgments We thank S. L. Brantley from the Arthropod Division of the Museum of Southwestern Biology at the University of New Mexico for assistance with centipede identiÞcation and the Espanola Ranger District of the USDA Forest Service for permission to conduct this research on the Santa Fe National Forest.

References Cited

Fig. 3. Mass and temperature dependence of RMR (Þlled symbols) and SMR (empty symbols) in 12 species of centipede. (a) x-axis is natural log of live mass (mg) and y-axis is the natural log of metabolic rate (␮W) corrected for environmental temperature (K), where 0.66 eV is the critical thermal increment from equation 4 and k is BoltzmannÕs constant (8.62 ⫻ 10⫺5 eV/K). General linear model analysis indicated that RMR (solid line) was e0.61 ⫽ 1.83 times SMR (dashed line). (b) x-axis is inverse of environmental temperature multiplied by BoltzmannÕs constant and y-axis is natural log of metabolic rate corrected for live mass, where 0.79 is the mass scaling exponent from equation 4. F, A. umbraticus; , G. glyptocephalus; Œ, Oabius sp.; E, S. polymorpha; f, L. curtipes; v, L. melanops; ‚, S. weberi; Q, C. elegans; 䡺, C. brevicornis; 䉬, L. mutabilis; ƒ, N. coloradensis; 䉫, C.ormocephalus mortisans.

(1983b) suggested that predictions of centipede FMR from RMR should be increased by a factor of 1.75 (Albert 1983a). This factorial increase of 1.75, combined with the factorial increase of 1.83 noted for the difference between SMR and RMR (equation 4), indicates that FMR of centipedes is ⬇2.58 times SMR. This value falls midway between the range of 2Ð3, which is often reported as the factorial difference

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