an altitudinal comparison of water and metabolic relations in two acridid grasshoppers (orthoptera)

Corni~. Biochem. Physiol. Vol. 74A. No. I. pp. 101 to 105. 1983 Printed in Great Britain.

0300-Y~~9.83/0l0l0l-05$03.00~0 0 1983 Pergamon Press Ltd

AN ALTITUDINAL COMPARISON OF WATER AND METABOLIC RELATIONS IN TWO ACRIDID

GRASSHOPPERS (ORTHOPTERA)

DENNIS DANIEL MASSION*

Department of Zoology, Arizona State University, Tempe, AZ 85287, USA

(Rrceiard 24 March 1982)

Abstract-l. Water loss rates (WLR) and oxygen consumption rates (r’oJ were determined for two species of grasshoppers inhabiting hot, low elevation deserts to cool, high altitude meadows,

2. Water loss rates and oxygen consumption rates were positively correlated with increasing elevation.

3. Decreased WLR in desert animals and increased Ijo in high elevation animals are considered important adaptations to xeric conditions and short growing seasons respectively.

INTRODUCTION

Desert regions are typically characterized as areas where the potential rate of evaporation far exceeds the rate of precipitation (Logan, 1968). Low atmos- pheric moisture fails to dampen the thermal flux caused by intense diurnal insolation and rapid noctur- nal reradiation. Consequently arid lands experience a wide range of circadian and seasonal temperatures. The low-latitude Sonoran Desert is considered one of the hottest deserts of the world. As one moves either poleward or to higher elevations, the increased atmos- pheric moisture and subsequent denser canopy of vegetation reduce temperature fluctuations and increase soil moisture. At very high elevations, however, the atmosphere is much colder and holds very little moisture. Intense solar insolation penetrates this arid and rarified atmosphere causing rapid surface heating which results in a high rate of evaporation. At night alpine temperatures plummet due to rapid reradiation and convective cooling of the substrate. As a result, high elevation organisms may actually experience conditions harsher than those experienced by desert species since they must cope with the daily extremes of hot and cold and an extremely short growing season.

Grasshoppers have successfully adapted to most terrestrial habitats, including both desert and alpine regions. Their small size has permitted them to exploit numerous microhabitats, thus behaviourally avoiding climatic extremes. Nevertheless, certain species routinely bask regardless of the habitat. An excel- lent example is the banded-wing grasshopper, Trimer- otropis pallidipennis (Burmeister), of the Sonoran Desert. During a typical summer day this grasshopper basks on open ground for all but a few hours even though soil temperatures may surpass 65°C (Patten & Smith, 1975). Whereas 7: pnllidipennis is restricted to elevations below 2440 m, a congeneric species, Trimrr-

* Present address and all correspondence: Department of Biology, Scottsdale Community College, 9000 E. Cha- parral Road, Scottsdale, AZ 85253, USA.

otropis sc&iisa Scudder, can be found basking on the windy, south-facing outcroppings up to 3350m in southern Colorado (Alexander & Hilliard, 1969). 7: s@iisu prefers open forested areas, where the increased temperatures (from solar insolation on the exposed rocky slopes) lengthens the growing season and raises the summer temperatures at these elevations.

Few studies correlating physiological responses of grasshoppers to their environment over altitudinal gradients have been reported. Suanraksa (1956) compared oxygen consumption of two grasshoppers Melanoplus dodgei and Aeropedullus ciavatus and found increased oxygen consumption in high elevation populations. Abushama (1970) reported greater water loss in a mesic grasshopper, Anucridium m. melanorhodon, compared with a more xeric form, Poe- cilocerus hierglyphicus. Dearn (1977) found a relatively smaller clutch size in the alpine grasshopper, Kosciu- sola asitatus, when compared with two lower elevation species (Kosciuscolu cogantus and Praxibulus sp.).

This paper compares the thermal, water and metabolic relations of low latitude, xeric population of Tri- merotropis pullidipetmis with those of a mid-elevation population of the same species and a high elevation population of the congeneric species. Trirncrotropis st4fliisu.

MATERIALS AND METHODS

Trimrrotropis pallidipennis (Burmeister) was collected from two study sites: a Palo Verde-Saguaro community [elevation 427 m (1400 ft)] in the Sonoran Desert approx. 45 km west of Phoenix, Arizona and a sdgebru&&om- munity [elevation 2300 m (7546 ft)] found ah&:&illside above the Gunnison River approximately 48 km west of Gunnison, Colorado. Samples were also taken from a montane population of Trimerotropis sy&@,&udder ‘inhabiting steep, south-facing slate outcroppin@ [elevation 3900m (12,800 ft)] 0.8 km south of Mount Crested Butte (Gunnison Co.). Colorado.

101

102 DENNIS DANIEL MASSION

Grasshoppers were maintained in the laboratory at 24 f 1°C for two or more days before testing. They were fed mixed vegetation, primarily filaree (Erodium cicutar- ium), Muhly grass (Muhlmberyiu sp.) and lettuce. Animals were starved for several hours and placed in a desiccator for 30 min before weighing. Laboratory runs were made between 0700 and 1900 hr, a period which corresponds to diurnal activity for the grasshoppers in the field.

Water loss measurements

Water loss was measured gravimetrically to the nearest 0.1 mg. Preweighed grasshoppers were placed in a desiccator having a dry air (< 5% r.h.) flow of 1500 ml/min and kept in a constant temperature chamber. After six hours, animals were reweighed and total water loss calculated. Fecal weights were included with the final weights; there- fore, any change in mass must be considered water loss. Animals that exuded material from the mouth, egg pods, or more than two feces were not used in the analysis.

Oxygen consumption measurements

Oxygen consumption was determined using standard manometric procedures (Umbreit et al., 1964). Animals were placed in large (220ml) Warburg flasks containing approx. 20g of Drierite (anhydrous calcium sulfate). A plastic disc separated the grasshopper from the Drierite and provided a resting substrate. A paper wick was inserted into the side arm which contained 0.5 ml of IO% KOH for CO1 absorption. A small piece of screen pre- vented the animal from coming into contact with the KOH. Warburg manometers and flasks containing the animals were then placed under a constant temperature bath for 30 min before measuring oxygen consumption.

Data were keypunched, entered into Arizona State Uni- versity’s UNIVAC 1105 computer and treated statistically using the Statistical Package for Social Sciences (SPSS)

(Nie et al., 1975). A statistical level of deviation of P < 0.05 was considered significant.

RESULTS

Intra- and interspec$c weight dtfferences The mean wet weight for each population of grass-

hoppers is compared in Fig. 1. No significant difference in weight and body size was found when desert (Trimerotropis pallidipennis) males were compared with montane (7: s@usa) males or when desert females were compared with montane females. Males and females, however, from the sagebrush habitat (7: pallidipennis) were significantly smaller than individuals of the same sex from the other two sites. Signifi- cant weight differences (P < 0.001) between sexes in all populations were observed. The desert female grasshoppers averaged over twice the weight of the males and the montane females were 1.8 times heavier than their male counterparts.

Water loss rates Live body weight water loss rates (WLR) for both

species (three populations) of grasshoppers are plotted as a function of chamber temperature in Figs 2 and 3. Water loss rates were positively correlated (r2 > 0.30; P < 0.01) with increasing temperatures in all cases. The greatest WLR occurred in montane (7: sufisa) males (X = 21.55 mg/g per hr at 40°C) with a value 2.2 times greater than the WLR for desert (T. pallidipennis) males at the same temperature (9.85 mg/g per h). The lowest WLR were measured for desert females

564.5 ( 14.50)

b ID x P.lUdhMI. T. wffusa r. p.uIdlmmnls E *.ln*,~lln~ duwi sagebrush

r. sum.. montano dermrt l gobrush montano

. Fig. 1. Mean body weights (mg) of three populations of Pimerotropis from different localities. Mean . body weights of both male and female sagebrush grasshopper (T. pallidipennis) were significantly smaller

than those of the desert (7: pallidipennis) and the montane (a sufisa) individuals. Two standard errors are given in parentheses.

A comparison of water and metabolic relations in grasshoppers

, r-1139.005x (r2= 614) I

2440

.210 I

ot .25 265 280 295 310 25 340 3% 370 365 400

Temperature, ‘C

Fig. 2. Comparison of live body-weight water loss rates mg/g per hr) for three populations of male grasshoppers desert Trbnerotropis pullidipennis = ----; sagebrush 7: 7allidipeks = ---------; montane 7: xtfisa = -).

Data points are means +2 SE.

with mean values ranging from 2.92 mg/g per hr at 25°C to 7.51 mg/g per hr at 40°C.

Although the mean WLR values of sagebrush grasshoppers (7: pullidipennis) were consistently intermediate to the other two populations, the wide range of recorded values prevents most results from being statistically different from other populations.

Osyym consmption rutcs

Manometrically determined mean oxygen consumption rates (voJ of the three populations of grasshoppers are shown in Figs 4 and 5. Metabolic patterns were similar for both sexes and were positively correlated (P < 0.01) with increasing temperatures for all cases. Between 25 and 40°C the mean voio, doubled for most populations, with males having con-

: yr-500*409x (i-2, 3l1)

240

I

; y--079*488x $=720)

y--386+.276x (r2=357) 210

188 250 265 2m 2% no 325 340 355 370 385 402

Fig. 4. Comparison of oxygen consumption rates (~1 0,/g per hr) of three populations of male grasshoppers over a 15°C temperature range (desert Trimerotropis pallidipennis = ----; sagebrush 7: pallidipennis = ----- -; montane 7: s@iisa = -). Data points are means +2 SE.

sistently higher vo, than females within each population.

Mean PO2 ranged from 308.5 ~1 0,/g per h at 25°C for desert females to 2366.4 ~1 0,/g per hr at 40°C for montane males. Over a 10°C temperature range (25-35”C), the lowest Qto values for vo, were found in the desert populations (males = 2.14; females = 2.72), while the montane species showed the highest Qlo values (males = 4.11; females = 4.07). At 30°C montane males metabolized 1.86 times faster than desert males and montane females 1.36 times faster than desert females. At 35°C the metabolic rates of both montane males and females were 1.7 times higher than their desert counterparts. The greatest differences were found between the males of the desert population and montane population at 40°C where there was a 1008 ~1 0,/g per hr mean difference in lioi At this temperature many of the montane indi-

, y.-2249.-042x tr2z653) I

+y=-673.570x (r2=461)

~ Y.-1413.674~ (r2 = 709)

O’,. 250 265 280 295 310 325 340 355 370 335 433

Temperature, ‘C

Fig. 3. Comparison of live body-weight water loss rates (mg/cm’ per hr) for three populations of female grasshoppers (desert Trimerotropis pakdipennis = ----; sagebrush 7: paflidipennis = ----; montane 7: s&iisa = -).

Data points are means + 2 SE.

Temwature , *C

Fig. 5. Comparison of oxygen consumption rpeq@ OJg per hr) of three populations of female grash s’ovef a 15°C range (desert Trimerotroois pallidioennk~.---: - . . sagebrush T pallidipennis = -------; montanl il: s@ii-

SO = -). Data points are means _+2 SE.

104 DENNIS DANIEL MASSION

viduals died during the three hours required for laboratory measurements.

The tic,, of the sagebrush population were generally intermediate to those of the desert and montane populations with the notable exception of a drastic reduction of l$, by both sexes at 40°C. Comparisons of sagebrush Vo2 values with the other two populations must be done cautiously because of the significant size difference between the sagebrush population and the other two populations.

DISCUSSION

Water loss Small terrestrial animals are extremely vulnerable

to desiccation because they expose large surface areas relative to the small volume of body fluids available to buffer any evaporative water loss (Kennedy, 1927). This problem is magnified when the habitat is hot and dry. Nevertheless, desert animals often show greater resistance to water loss than closely related mesic species (Edney, 1977).

Water loss rates (WLR) were strongly correlated to habitat with the desert population of 7: pallidipennis losing significantly less water than either other population of Trimerotropis. The greatest WLR occurred in the montane population (T st&‘i~u) which normally is able to replace any lost water by feeding on readily available, succulent vegetation. WLR were significantly different at all temperatures above 25°C. Simi- lar body size simplifies comparisons of WLR of the desert population of 7: pallidipennis with those of the montane population of 7: scflusa, whereas comparisons of either population with the sagebrush population of 7: pal/idipennis are complicated by the small body size of these individuals (Fig. 1). Even with this complication the WLR of grasshoppers from the sagebrush habitat are intermediate to the other populations, as would be predicted on the basis of moisture availability in respective habitats.

Any organism must replenish lost water if it is to maintain a positive water balance. The primary source of water for grasshoppers is dietary although there is considerable difference in the water content in the food of the three populations investigated. The desert population feeds on vegetation with low water content and seems to prefer fields of dried stubble over neighboring green fields (Barnes, 1960). The montane population was observed feeding on fresh grasses and shrubs with high moisture content. There was also a significant difference in the tolerance to dehydration between the two species. When kept in the laboratory, individuals from both populations of 7: pallidipennis survived for some time on dried grass; however, captured ?: s@iisa required fresh grass daily. The survival of laboratory-maintained 7: s@iusu was increased if the grass is placed in a beaker of water.

The WLR of Eimerotropis are not exceptional when compared with other arthropods, but they sup- port existing data showing low WLR in species from xeric habitats (Edney, 1977). At 35°C the cuticular permeability of the desert individuals (15.2 pg/cm’ per hr per mmHg) was lower than either the montane, 7: s@iisa (24.4pg/cm2 per hr per mmHg) or reported

values for the xeric locust, Locusta migratoria (22.0 pg/cm’ per hr per mmHg) (Loveridge, 1968).

Oxygen consumption Reported values of oxygen consumption rates (vob,)

in grasshoppers and locusts are highly variable, reflec- ting a combination of conditions which will alter the physiological state of the grasshopper. In this study, live body weight was used as a common denominator in an attempt to stabilize any artificially-induced metabolic changes. However, changes in live weight do not totally compensate for changes in pol. For example, Keister & Buck (1974) reported a five times greater drop in respiration than in live weight for Locusta migratoria during the first fifty hours of star- vation, whereas Bailey & Mukerji (1977) found Ijo2 fluctuations during aging in several species of Mela- noplus which were not mirrored in weight changes. Even though live weight may not effectively reflect physiological changes, other suggested units, such as dry weight, surface area (Bodine, 1921; Butler & Innes, 1936), and age (Hamilton, 1958) have not been shown to be any better correlated to voi. Most inves- tigators conclude that some unit of live body weight is the most acceptable and practical unit of measure- ment available (Gardiner, 1958; Keister & Buck, 1974; Loveridge & Bursell, 1975).

In this study, increased oxygen consumption rates ( lioJ were strongly correlated with grasshoppers living at higher elevations (Figs 4 and 5). The lowest metabolic rates at all temperatures measured above 25°C were found in the desert 7: pallidipennis, while the highest rates were found in the montane 7: s@iusa. Generally the V,, of the sagebrush population were intermediate. In addition, increased oxygen consumption was strongly correlated to increasing temperatures in all three populations and both sexes. PO1 appeared to be linearly correlated to temperature, at least for the desert and montane populations, with the desert population showing the lowest metabolic response to temperature and the montane population showing the highest response over a temperature range of 2554OC. Data for the sagebrush population exhibited a sharp initial response of increased oxygen consumption from 25 to 35°C (Qie = 2.94 males; 3.20 females); however, the oxygen consumption rates actually dropped at 40°C. Two independent sets of manometric data on oxygen consumption at 40°C showed similar findings for this population. It is possible that the sagebrush grasshoppers become debili- tated at this temperature; however, thermal studies indicated that they are able to tolerate 45°C for three hours with no mortality (N = 12). Measurements of tab, at 40°C were performed several days later than Vo2 measurements at lower temperatures, and once tested at either 35 or 40°C individuals were never used again. Although individual tic,2 may show significant changes due to feeding, state of hydration, or age (Clarke, 1957; Keister & Buck, 1974) all populations of fiimerotropis were subjected to the same procedures, and a drop in PO, with increasing temperature was observed only in the sagebrush population. It is possible that the size of the sagebrush grasshoppers, which is considerably smaller than that of the other groups, was responsible for its lower metabolic rate at 40°C.

A comparison of water and metabolic relations in grasshoppers 105

Suanraksa (1956) compared the poio, of high and low Acrididae) in a grassland community. Curl. Ent. 109, elevation populations of two Colorado grasshopper 605-614. species. He found that samples of Aeropedellus cla- BARNES 0. L. (1960) Observations on the desert grass- vatus from low elevations (2638-3346m) had signifi- hopper, Trimerotropis pullidipennis pallidipennis. in Ari- cantly lower metabolic rates and a lower metabolic zona. J. econ. Em. 53, 721-724.

response to temperature (Q10 = 1.53 males; 1.93 BODINE J. H. (1921) Factors influencing the water content

females) than did high elevation forms (433&4674 m) and the rate of metabolism of certain Orthoptera. J. exp.

(Qlo = 1.60 males; 2.15 females) over a temperature Zool. 32. 137.-164.

range of 27-37°C. When Suanraksa compared the V,,, BUTLER C. G. & INNES J. M. (1936) A comparison of the

rate of metabolic activity in the solitary and migratory of individuals of Melanoplus dodgei, he found conflict- phases of Locusta miyratoria. Proc. R. Sot. Ser. B 119. ing results. In general, the V,, and metabolic response 296-304. to temperature in females of M. dodgei followed pat- CLARKE K. U. (I 957) The relationship of oxygen consump-

terns similar to females of A. clavatus, but the alpine tion to age and weight during the post-embryonic

males of M. dodgei exhibited a much lower tempera- growth of Locusta miyratoria L. J. exp. Bial. 34, 29-41.

ture coefficient (Qlo = 2.00) than did the foothill DEARN J. M. (1977) Variable life history characteristics

males (Qlo = 3.00). Suanraksa attributed the inconsis- along an altitudinal gradient in three species of Austrd-

tent results found in M. dodegi to possible acclimation lian grasshoppers. Oecoloyia 28, 67-86.

of the alpine group in the laboratory prior to measur- EDNEY E. B. (1977) Water balance in land arthropods. Zoo-

ing P&‘,, When montane adults (7: s@iusa) were accli- physiology and Ecoloyy Vol. 9. Springer New York.

GARDINER B. G. (1958) Some observations on the respir- mated to higher temperatures at low elevation, over 60% died within two days forcing future studies to be

ation of young nymphs of Schistocerca yregaria (ForskBl) in relation to phase and rearing density. Proc. R. Em.

conducted adjacent to their habitat. Sot. Lond. A 33, 159-166.

Both species of Trimerotropis have a wide elevation- HAMILTON A. G. (1958) Variations in the metabolic rate in

al distribution. These populations living at higher male desert locusts (Schistocerca gregaria (Forsk.). 10th

altitudes are faced with much shorter growing seasons Int. Conur. Ent. Montreal 1956 2. 343-347.

than their low elevation counterparts. Spring is gener- KEISTER MI & BUCK J. (1974) Respiration: some exogenous

ally delayed four days for every 157 m increase in and endogenous effects on rate of respiration. In The Physiology of Irlsectu. (Edited by ROCKSTEIN M. ). pp.

elevation (Hopkins Law) and fall events also occur 619-658. much earlier, further shortening the growing season KENNEDY C. H. (1927) Some non-nervous factors that con- (Alexander & Hilliard, 1969). At higher elevations an dition the sensitivity of insects to moisture, temperature,

increased metabolic rate is an important adaptation, light and odors. Ann. ent. Sot. Am. 20, 87-106.

for it reduces the time required for an insect to com- LOGAN R. F. (1968) Causes, climates, and distribution of

plete its life cycle. deserts. In Desert Biology, Vol. 1 (Edited by BROWN G. W.) pp. 21-50. Academic Press, New York.

LOVERIDGE J. P. (1968) The control of water loss in Locusta A~knowledyements-This work is part of a dissertation migratoriu migratoriodes R & F. II. Water loss through

submitted in partial fulfillment of the requirements for the the spiracles. J. exp. Biol. 49, 15-29. PhD degree at Arizona State University and was funded in LOVERIDGE J. P. & BURSELL E. (1975) Studies of the water parts by NSF Grant PCM 77-23803 to N. F. Hadley. I relations of adult locusts (Orthoptera, Acrididae). II. thank N. F. Hadley for advice and assistance. I am Resoiration and the uroduction of metabolic water. Bull. indebted to the Science Department of Western State Col- ent.‘Res. 65, 13-20. ’ lege of Colorado for their assistance and laboratory space. NIE N. H.. HULL. C. H.. JENKINS J. G.. STEINBREENER K. &

BENT D. H. (1975) SPSS: Sratisticul parkuge,for the socia! sciences, 2nd edn. McGraw-Hill, New York.

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Poecilocerus hieroglyphicus (Klug), compared with the I-19. Dowden, Hutchinson & Ross, Stroudsburg, Penn. tree locust Anacridium melanorhodon melanorhodon SUANRAKSA S. (1956) Differences in metabolic rate between (Walker). Z. angew. ht. 66, 16&167. grasshoppers from high and low altitudes. Master’s

ALEXANDER G. & HILLIARD J. R. JR (1969) Altitudinal and thesis. University of Colorado,Boulder. seasonal distribution of Orthoptera in the Rocky Moun- UMBREIT W. W.. BURRIS R. H. & STAUFFER J. F. (1964) tains of northern Colorado. Ecol. Monogr. 39, 385-431. Manometric tec,hniques: a manual describing methods

BAILEY C. G. & MUKERJI M. K. (1977) Energy dynamics of applicable to the .studJ of tissue merabolism. 4th edn. Bur- Melanoplus hicittatus and M. femurruhrum (Orthoptera: gess. Minneapolis.

an altitudinal comparison of water and metabolic relations in two acridid grasshoppers (orthoptera)

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