Effect of temperature on the metabolic rate and evaporative water loss of the scorpion Urodacus armatus

J. therm. Biol. Vol. 18, No. 1, pp. 13-18, 1993

0306-4565/93 $6.00+ 0.00 PergamonPressLtd

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EFFECT OF TEMPERATURE ON THE METABOLIC RATE A N D EVAPORATIVE WATER LOSS OF THE SCORPION URODACUS ARMA TUS PHILIP C. WITHERS1 and G g ~

T. SMITHz

tDepartment of Zoology, The University of Western Australia, Nedlands 6009, Western Australia and 2Division of Wildlife and Ecology, CSIRO, LMB 4, PO Midland 6056, Western Australia (Received 11 August 1992; accepted in revised form 25 October 1992)

Abstraet--l. There is a highly significanteffect of body mass and ambient temperature on metabolic rate and evaporative water loss for the scorpion Urodacus armatus. 2. The combined effects of body mass and ambient temperature on metabolic rate are summarized by the multiple regression equation; Vo: (,ul h -m) = 5.07 mass°'gt' 10°°37r'. The combined effects of body mass and ambient temperature on evaporative water loss (EWL) are summarized by the multiple regression equation; EWL (mg h -t) = 0.204 mass°'6~ I0°°26r'. 3. The pooled allometric mass exponent for metabolic rate of 0.92 is significantlydifferent from 1.0, 0.75 and 0.67. The pooled allometric mass exponent for evaporative water loss of 0.63 is significantly different from 0.75 and 1.0, but not from 0.67, and hence is similar to the allometric relationship for surface area of scorpions. 4. The calculated cutaneous component of evaporative water loss was 66.7% at 20°C, 72.9% at 25°C, and 74.0% of total EWL at 30°C. Key Word Index: Scorpion; temperature; metabolic rate; evaporative water loss; aUometry; Urodacus armatus

INTRODUCTION

20-30 cm deep. This species forages from the burrow entrance; few individuals are found away from their burrows, except adult males during the breeding season.

Scorpions are a conspicuous and important faunal element in desert and semi-desert habitats (Polis, 1990). They and other arachnids generally have low metabolic rates and low rates of evaporative water loss (EWL) (Anderson, 1970; Hadley, 1970); this is an adaptation or preadaptation to existing in desert and semi-desert environments. A number of studies have examined rates of metabolism and/or EWL, and the influence of body mass in North American, African and Eurasian scorpions (Dresco-Derouet, 1960, 1964; Hadley and Hill, 1969; Crawford and Women, 1973; Toolson and Hadley, 1977; Robertson et al., 1982). This study examines the rates of metabolism and EWL for an Australian scorpion, Urodacus armatus (scorpiones, Scorpionidae). Urodacus armatus is widely distributed and abundant (up to 4000 per hectare; Smith, unpublished results) in arid and semiarid Australia. It is found in a wide range of vegetation associations and in soils ranging from sand to heavy loam. It constructs a quasi-spirai burrow to

METHODS

Scorpions were collected from a study area located 30kin north of Kellerberrin (31°38'S, 117°43'E), Western Australia. The climate is mediterranean; the mean annual rainfall is 334mm and the mean monthly maximum temperature ranges from 16.2°C in July to 33.9°C in January. The scorpions were collected from a patch of Kwongan (sandplain heath) on light-grey sandy soil, in an isolated 50 ha patch of native vegetation. Urodacus armatus burrows were abundant throughout the area, most were in open areas of bare soil between the shrubs. Scorpions were collected by pit-trapping at the burrow entrance; they were then placed in 50 ml plastic containers and kept cool while returned to the laboratory, where they were maintained for more than 2 weeks at 20°C, with drinking water but no food. 13

14

PHILIP C. WITHERSand GRAEMET. SMITH

Metabolic rate and EWL were measured for animals maintained in plastic 60ml syringes at ambient temperatures of 20-40°C. Ambient temperature was maintained to _ I°C by immersing the sealed syringes in a Tecmar TE7 water bath. Scorpions were weighed to +0.0001 g and placed in the syringe, previously flushed with room air, with a preweighed package (4-8 g) of silica gel, in a nylon mesh bag. Scorpions were left in the sealed syringes, submerged in the water bath, for periods of 4-12 h (shorter periods at higher ambient temperatures). Then the syringes were removed and about 40 ml of air injected by hand, at about 100ml min -~ through a column of drierite and ascarite to remove H20 and CO2, respectively, into a Servomex 574 paramagnetic 02 analyser and the output monitored with a Fluke digital voltmeter. The percentage 02 content of air was determined to +0.01%. The oxygen consumption rate (Vo2; ml O 2 STPD g-~ h 1) was calculated using standard equations (Withers, 1977). The volume of air in the syringe was calculated assuming a density of 1.0 for the scorpions and 1.6 for the silica gel. The scorpions were reweighed immediately after the O2 content of the air was measured, and rate of weight loss calculated. This rate is presumed to be the rate of EWL (mg H20 g h-l); there was no evidence for either urinary or fecal water loss during measurements. The rate of evaporative water loss was converted into a resistance to evaporative water loss (R) (s cm -1) by expressing EWL per body surface area, and per water vapour density gradient between the scorpion (assumed to be 100% saturated at ambient temperature) and the ambient air (assumed to be 0% RH at ambient temperature). Resistance to evaporative water loss of the scorpion was calculated from the mean EWL value at each ambient temperature. Surface area was calculated as cm 2 = 15 g0.rs (Toolsen and Hadley, 1977).

RESULTS

Circadian rhythm Initially, metabolic and water loss rates were determined during the day and overnight, at 20, 25 and 30°C. During the day, both metabolic rate and evaporative water loss increased with higher temperature, as expected. During the night, however, the metabolic rate and EWL was higher at an ambient temperature of 20°C than 25°C. Metabolic rate was significantly lower during the day than at night for each ambient temperature, with the night rate being from 1.9 times higher (at 30°C) to 7.0 times higher (at 20°C) than the day rate (Table 1). Similarly, the EWL was significantly higher at night than during the day, except at Ta = 30°C. These differences in metabolic rate and EWL presumably reflect higher activity levels at night and at 20°C. All further analyses of metabolic rate and evaporative water loss are for the minimal day-time rates.

Effects of temperature There was a significant effect of ambient temperature on day-time rates of oxygen consumption (ANOVA; F4. ~,2 = 79; P < 0.05) and EWL (F4. tl2 = 20; P < 0.05), from 20 to 40°C (Table 2). There was a significant difference between the metabolic rate, and the evaporative water loss, for each ambient temperature comparison (Newman-Keuls multiple comparison test). The Q10 values for Vo2 were; 3.06 (20-25°C), 1.50 (25~30°C), 3.46 (30-35°C), and 2.62 (35~,0°C). The Q~0 values for EWL were; 2.59 (20-25°C), 1.14 (25-30°C), 2.30 (30-35°C), and 2.34 (35--40°C). The ratio of EWL/Vo2 decreased significantly (ANOVA; F4.1~2= 2.46; P < 0.05) from about 0.033 at an ambient temperature of 20°C, to 0.022 at 35°C and 0.020 at 40°C (Table 2). The only significant

Table 1. Rate of oxygen consumption (Vo2;/al 02 g-t h-t) and rate of EWL (mg H20 g-Z h-t), for scorpions during the day and night, at ambient temperatures (T,) from 20 to 30°C Ta

Vo2

20 25 30

Day

Night

N/D

n

29.6-t-3.5 66.1 -t- 8.0 80.3-t-7.4

186.4-t-15.1 134.0 4- 17.8 147.7-t-17.5

7.04-0.9 1.9 4- 1.0 1.94-0.2

9 ts= -11.3 7 t6 = -5.2 20 /19= --5.3

P <0.001 P < 0.002 P<0.001

0.81+0.11 0.954-0.16 1.805:0.17

2.25 4-0.19 1.444-0.15 2.204-0.17

3.1 4-0.3 1.3+0.2 1.34-0.1

9 ts=-8.1 7 tr= -7.0 20 tt9 = --4.3

P<0.001 P<0.001 P < 0.001

EWL 20 25 30

Values are mean + SE, with the number of olnervations (n), with paired t-test value and

probability level for the day-night comparison.

Effect of temperature on Vo2 and EWL in scorpion

15

Table 2. Body mass (g), rate of oxygen consumption (Vo2; #1 O 2g-l h-'), rate of EWL (mg H20 g-l h-i), and ratio of EWL/Vo2 (nag H20 pl Ofl), for scorpions during the day, at ambient temperatures from 20 to 40°C T,

Mass

Vo~

EWL

EWL/Vo2

20 25 30 35 40

0.51±0.08 0.50±0.08 0.59±0.06 0.48 ± 0.08 0.47 4- 0.09

32.3-+2.0 56.6--+4.5 69.2±5.0 128.8± 12.6 208.5± 13.6

1.06±0.10 1.70+0.19 1.81 ± 0.13 2.75 ± 0.35 4.21 :[: 0.48

0.0325 ± 0.0025 0.0326±0.0044 0.0279±0.0020 0.0224 ± 0.0224 0.0204 ± 0.0020

n 22 23 33 20 16

Values are mean ± SE, with the number of observations (n). changes were for 20-35°C and 20-40°C (NewmanKeuls multiple comparison test). Calculated values for R to EWL are; 1109 s cmat 20°C, 917 at 25°C, 1094 at 30°C, 986 at 35°C and 835 at 40°C.

Effects of body mass Body mass ranged from <0.1 to > 1.0 g. There was a significant effect of body mass on Vo2 and EWL at each ambient temperature, and the allometric relationship was examined for the double-logarithmic transformation, i.e. logl0 Vth = a + b lOgl0 mass (Table 3). There was no significant difference in the slope (b) values for Vth at any Ta (ANCOVA, F4.10~ = 1.5, P > 0.05); the common slope was 0.916. There were significant differences in Vo2 elevation values, for all temperature comparisons except 25 and 30°C (Newman-Keuls multiple comparison test). There was no significant difference in the slope (b) values for EWL at any T, (ANCOVA, F4. ~06= 2.1, P > 0.05); the common slope was 0.628. There were significant differences in EWL elevation values, for all temperature comparisons (Newman-Keuls multiple comparison test).

Effects of temperature and body mass The significant effects of ambient temperature and body mass on Vo2 and EWL were simultaneously analysed by multiple regression. The relationship for Vo2 was: logl0 (Vo:) = 0.7048 +0.911 ( _ S E 0.037) logl0 (grams)+0.037 ( _ S E 0.003) Tm (r2=0.89, F2,10~ =422, n = 104). The untransformed relationship is thus Vo2 (ml h -l) --5.07 mass °'gll 10°'°37r.. The mass coefficient for Vo2 was significantly different from 0, 0.67, 0.75 and 1. The multiple regression relationship for EWL was; l o g l o ( E W L ) = - 0 . 6 9 1 + 0 . 6 3 4 (_+SE 0.036) loglo (grams) + 0.026 (-}-SE 0.003) T, (r2ffi 0.81, F,. 101 ffi 219, n ffi 105). The detransformed relationship is thus EWL (mg h -l) =0.204 mass °.634 10°'°26to. TB 18/]--B

The mass coefficient was significantly different from 0, 0.75, and 1, but not 0.67.

Partitioning of total EWL The total rate of evaporative water loss was partitioned at ambient temperatures of 20, 25 and 30°C into its cutaneous (CEWL) and respiratory (REWL) components by assuming that the ratio of Vth to respiratory water loss was constant, at each Ta. This might be a reasonable assumption if gas exchange was by ventilation of the book lung, or if the spiracles were periodically opened and closed, but might overestimate the ratio of VoJEWL if O 2 and water exchange were by continuous diffusion through permanently open spiracles. Metabolic rate measurements for the scorpion Centruroides exilicauda (as C. scupturatus) suggest that 02 uptake is discontinuous (Hadley and Hill, 1969), and so respiratory water loss might be expected to be correlated with Oz uptake. Thus, the low Vo2 and EWL during the day and the elevated values at night allow the ratio of VoJREWL

Table 3. Effect of body mass on rate of oxygen consumption (Vo2; pl 02 h-') and rate of EWL (mg H20 h-'), for scorpions during the day, at ambient temperatures from 20 to 40°C Ta

•02 20 25 30 35 40

a

b

r2

n

0.05 0.914± 0.084~: 0.04 1.037± 0.073t~ 0.05 0.891± 0.075~/ 0.04 0.894± 0.0577:[:

0.91 0.85 0.86 0.89 0.94

22 23 35 20 16

-0.17 +0.05 0.662±0.072" -0.08 +0.05 0.481± 0.081"?~ 0.13 ±0.04 0.751±0.072" 0.18 ± 0.04 0.589+ 0.053*?

0.80 0.63 0.77 0.87

23 23 35 20

0.93

16

1.40 ± 0.04 0.807± 0.057":[: 1.69 ± 1.82 + 2.03 + 2.25 ±

EWL 20 25 30 35

40

0.41 ± 0.03

0.646± 0.047"t

Linear regression relationship is of the form log~0 (Y) -- a + b logl0 (g). Regression coefficients a and b are given with +SE. *Significantly different from l.O. tSignificantly different from 0.75. ~Significantly different from 0.67.

16

PHILIPC. WITHEgSand GRAEMET. SMITH

to be estimated as (EWL~ight-EWLa~y)/(Vo2,,~ Vo:~,~), i.e. 9.1 ml O2 mg H2O-I at 20°C, 7.3 at 25°C and 5.7 at 30°C. The CEWL is consequently calculated to be 0.54 mg g-~ h-~ (66.7% of the total EWL) at 20°C, 0.467 (72.9%) at 25°C, and 1.554 (74.0%) at 30°C. Estimation of CEWL in the above manner enables the cutaneous resistance to evaporative water loss to be calculated as 1665 s cm -~ at 20°C, 1861 at 25°C and 1466 at 30°C.

consistent increase in elevation with increasing ambient temperature, as expected from a Qt0 effect, but no variation in slope with ambient temperature. At the different ambient temperatures, the slope was consistently higher than 0.67 (the expected slope if metabolic rate is proportional to body surface area) and was generally intermediate between 0.75 (the generally expected value) and 1.0 (which corresponds to a mass-independent metabolic rate). For example, at 20°C, the slope was 0.807 (_+0.057) for U. armatus. Metabolic rates of other scorpions conform to a similar slope but generally were higher than for U. armatus (Fig. 1). The common slope from the ANCOVA analysis was 0.915. From the multiple regression analysis, Vo2oCmass °'9n. This indicates that metabolic rate increases more in proportion to body mass (slope = 1.0), than with the slope of 0.75 which is generally observed in many animals (see Withers, 1992). Thus, there is a more pronounced effect of body mass on Vo2 for U. armatus than is observed for many other animals. However, the allometric slope is < 1.0, and there is still a significant inverse effect of body mass on mass-specific metabolic rate, Allomettic relationships for other scorpions indicate either no or a slight negative relationship between mass-specific metabolic rate and body mass. There is no significant correlation between mass-specific metabolic rate and body mass for C. exilicauda (Hadley and Hill, 1969) and Parabuthus sp. (Robertson et al., 1982). Riddle (1978) reports no effect of body mass on mass-specific

DISCUSSION

There was a clear circadian cycle in metabolic rate and evaporative water loss for U. armatus. A similar circadian variation, with higher rates at night, has been reported for Euscorpius italicus and E. carpathicus by Dresco-Derouet (1960). In contrast, Hadley and Hill (1969) reported no circadian rhythm for C. exilicauda. The circadian variation reported here for U. armatus most likely reflects day-night differences in activity. All further discussion of metabolism and water loss is restricted to the minimal, day-time values. The standard rate of oxygen consumption of U. armatus is comparable to values reported for other scorpions, and is influenced by body mass and ambient temperature in a similar fashion to that reported for other scorpions (e.g. Figs 1 and 2). The allomettic relationship between absolute metabolic rate (ml 02 h-l) and body mass (g) indicated a

It- 1 0 0 0

LU

Z

100

O I-Q.

Z

10

0 0

Z

1.1.1

1

0.01

~t"

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0.1

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BODY M A S S (grams) Fig. 1. Allometric relationship for standard metabolic rate of U. armatus (solid line) compared with values for other species of scorpion, at an ambient temperature of approx. 20°C. V a h ~ from: thh study (thick line); (1) Riddle (1978) (thin ~ ~ by arrows); (2) Hadley (1970); (3) R o a n et al. (1982); (4) Crawford and Wooten (1973); (5) ~ ( I 9 ~ 0 ) ; (6) Hadley and Hill (1969); (7) Drescc~Deronet (1964). Values from Hadley (1970) and Crawford and Wooten (1973) were corrected from T. = 25 to 20°C assuming a Qi0 of 2.5. Hemmingsen's (1960) predicted metabolic rate for a ectotherms is also shown.

Effect of temperature on Vo2 and EWL in scorpion

17

600 • Urodacus a m a f u s l Euscorpius c a r p a f h l c u s 2 Euscorpius ifallcus 3 Nebo hierochonficus 4 P a r a b u f h u s villosus 5 H a d r u r u s arizonensis 6 Oiplocenfrus spifzeri 7 Cenfruroides s c u l p f u r a f u s 8 Parurocfonus ufahensis

600

•" ~ ~" 4 0 0 t-

2

5

6

3OO

0 200 ~>

t

8

lOO

0

I

!

I

I

I

10

20

30

40

50

(o C)

Ambient Temperature

Fig. 2. Relationship between Standard metabolic rate and ambient temperature for U. armatus and a variety of other species of scorpion; values from this study, Riddle (1978), Hadley (1970), Dresco-Derouet (1964), Robertson et aL (1982), Crawford and Wooten (1973) and Hadley and Hill (1969), metabofic rate at low ambient temperatures but a significant inverse effect at high temperatures, for Paruroctonus. Shorthouse (1971) indicates a significant effect of mass on mass-specific metabolic rate for U. yaschenkoi.

Scorpions, like spiders, tend to have a low metabolic rate, compared to other invertebrates. All values for standard metabolic rate of scorpions are considerably lower than the predicted metabolic rate for an ectotherm (e.g. Hemmingsen, 1960; Fig. 1).

Ambient temperature has the expected effect on the metabolic rate of scorpions (Fig. 2), with Q~0 values of about 2-3. From the multiple regression analysis, Vo2oc 100.037r,. ANCOVA also indicated a highly significant effect of ambient temperature on metabolic rate. Scorpions generally have a low rate of evaporative water loss, and this is adaptive, or preadaptive, to their successful habitation of xeric habitats. The rate of EWL of U. armatus is intermediate to values reported for other scorpions (Fig. 3). EWL is lowest,

10

°,,,9/

/ /

/

0.1

/ 0.01

.

./zo

o,3/"

/ J I

Op

":', ,,',

I II

0.1

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BODY MASS (grams) Fig. 3. Allometric relationship for total EWL of U. armatus (solid line) compared with values for a variety of other species of scorpions, at an ambient temperature of 30°C and approximately equivalent ambient conditions. Values for other species are: Di, Dipiocentrus spitzeri adults and juveniles (Crawford and Wooten, 1973); Op, Opisthophthalmus capensis (Robertson et al., 1982); Pa, Parabuthus villosus (Robertson et aL, 1982); Ha, Hadrurus arizonensb (Hadley, 1970); Ce, Centruroides exilicauda (Hadley, 1970).

18

PHILIPC. WITHEgSand GgAEMET. SMITH

at a given body mass, for the xeric scorpions Centruroides, Hadrurus and Parabuthus, and highest for the more mesic species Diplocentrus and Opisthophthalmus. The EWL was affected by body mass in the expected manner, i.e. in proportion to body surface area. From the multiple regression analysis, EWLoc mass °634. This slope is similar to the slope for the relationship between body mass and surface area of cm 2= 15 mass °68 (Toolson and Hadley, 1977). ANCOVA also indicated a highly significant effect of body mass on EWL at each Ta, but no significant difference between the allometric mass coefficient (b) at any Ta; the pooled b value for EWL was 0.628. Thus, EWL of Urodacus is highly correlated with body surface area, whereas metabolic rate is not. A similar allometry of evaporative water loss has been reported for other scorpions. For D. spitzeri, EWLoc mass °'627 (Crawford and Wooten, 1973). For Opisthophthalmus and Parabuthus, the allometric relationship for EWL and mass is not different from that for surface area and mass (Robertson et al., 1982). Ambient temperature has a marked effect on EWL for scorpions. For Urodacus, the Q~0 ranged from 1.14 to 2.56. The resistance to total evaporative water loss was from 835 to 1109 s cm -1, and did not vary consistently with temperature. Consequently, the effect of ambient temperature on EWL was explained by temperature effects per se; presumably the highest temperature examined here (40°C) is less than the transition temperature for Urodacus, at which EWL is markedly elevated by temperature. A number of studies have attempted to partition the total evaporative water loss of scorpions into its cutaneous and respiratory components, by measuring EWL for live scorpions and dead scorpions with the book lung openings sealed (Hadley, 1970; Crawford and Wooten, 1973). Unfortunately, cutaneous water loss often equals or exceeds total water loss in these experiments and so the exact partitioning of total EWL into respiratory cutaneous fractions is not clear, although it appears that cutaneous water loss is a major component (except at high ambient temperatures). In this study, the calculated ratio of TEWL/Vo2 was about 5-9 mg H:O ml O~-1. This total EWL was partitioned into REWL and CEWL components by using a physiological approach, assuming that Vo2/REWL is constant at a specific T,, because of intermittent book lung ventilation (by either intermittent convective or diffusive ventilation of the lung). This approach indicates that about 50-75% of

TEWL is cutaneous. This is a lower estimate than has been obtained in some other studies at equivalent ambient temperatures, but is similar to the estimate of 60% cutaneous evaporative water loss for living Paruroctonus at 24°C (Yokota, 1978; cited by Robertson et al., 1982). Acknowledgement--We thank Michael Warburg for help with collecting specimens and for discussion and encouragement with scorpion research. REFERENCES

Anderson J. F. (1970) Metabolic rates of spiders. Comp. Biochem. Physiol. 33, 51-72. Crawford C. S. and Wooten R. C. (1973) Water relations in Diplocentrus spitzeri, a semimontane scorpion from the southerwestern United States. Physiol. Zool. 46, 218-229. Dresco-Derouet L. (1960) L¢ m~tabolisme respiratoire des scorpions. I. Existence d'un rythme nycth~m~ral de la consommation d'oxyg~ne. Bull. Mus. hath. Hist. nat., Ser. 2 32, 553-557. Dresco-Derouet L. (1964) Le m~tabolisme respiratoire des scorpions. II. Mesures de rintensit6 rcspiratoire chez quelques esp6ces a diff~rentes tc~np6ratures. Bull. Mus. natn. Hist. nat., Set. 2. 36, 97-99. Hadley N. F. (1970) Water relations of the dc~rt scorpion, Hadrurus arizonensis. J. exp. Biol. 53, 547-558. Hadley N. F. and Hill R. D. (1969) Oxygen consumption of the scorpion Centruroides sculpturatus. Comp. Biochem. Physiol. 29, 217-226. Hemmingsen A. M. (1960) Energy metabolism as related to body size and respiratory surfaces, and its evolution. Rep. Steno meml Hosp. 9, 1-I10. Polis G. A. (1990) The Biology of Scorpions. Stanford University Press, Stanford, Calif. Riddle W. A. (1978) Respiratory physiology of the desert grassland scorpion Paruroctonusutahensis. J. Arid Environ. 1, 243-251. Robertson H. G., Nicholson S. W. and Louw G. N. (1982) Osmoregulation and temperature effects on water loss and oxygen consumption in two species of African scorpion. Comp. Biochem. Physiol. 71A, 605-609. Shorthouse D. J. (1971) Studies on the biology and energetics of the scorpion Urodacus yaschenkoi (Birula 1904). Ph.D. thesis, Australian National University, Canberra, Australia. Toolson E. C. and Hadley N. F. (1977) Cuticular permeability and epieuticular lipid composition in two Arizona vejovid scorpions. Physiol. Zool. 50, 323-330. Withers P. C. (1977) Measurement of Vov Vco~and evaporative water loss with a flow-through mask. J. appl. Physiol. 42, 120-123. Withers P. C. (1992) ComparativeAnimal Physiology. Saunders, Philadelphia, Pa. Yokota S. D. (1978) Water, energy and nitrogen metabolism in the desert scorpion Paruroctonus mesaenJis. Ph.D. thesis, University of California at Riverside, U.S.A.