Camp. 5iochem. Physioi. Vol. 9lA, No. I, pp. 147-151, 1988 Prmted in Great Britain

0300-9629/88 %3.00 + 0.00 Q 1988 Pergamon Press plc

THE SEAS~NALITY OF RESPIRATION IN TWO TEMPERATE CQLLEMBOLA AS RELATED TO

STARVATION, TEMPERATURE AND PHOTOPERI~D

Il. A. VAN DER WOUDE and E. N. G. JOOSSE

Department of Biology, Free University, Amsterdam. Telephone: 020-5482401

(Received 4 January 1988)

Abstract--l ~ The seasonal respiratory activity of field specimens of Orchesella cincia and ~o~ocer~ minor measured at IYC, fluctuated within a range corresponding to the variation found during the moulting cycle.

2. During a frost period and summer drought the respiration was significantly lowered by starvation. 3. The temperature response of winter and summer specimens of both species measured at 5, 10 and

ISC was similar. 4. A laboratory acclimation to temperature (0.5, IO, WC) and day length regimes revealed no

acclimation effects: only temperature effects were apparent. 5. The effects of starvation, growth, reproduction and moulting on respiration are discussed.

INTRODUCTION

The respiration of arthropods is in~uenc~d by many factors. as starvation, season, diapause and tem- perature. In Collembola 6&70% of the total energy metabolism is respiration; the remainder is used in production, i.e. growth (increase in biomass), moulting products and eggs (Testerink, 1982a). Starvation results in a decreasing metabolic rate (Zinkler, 1966; Testerink, 1982a). This decrease is shown in many other species like spiders (Anderson, 1974). a mite (Young and Block, 19801, a centipede (Riddle, I976), an amphipod (Van Senus, 1985) and many be effective in saving energy for survival (Anderson, 1979). In Collembola starvation can oc- cur repeatedly during summer due to drought, as observed in the field by the fact that these animals have empty guts. During these periods moulting and reproductive activity are terminated. As soon as the adverse weather conditions are ended the activities are resumed as shown by a synchronized moulting which is followed by reproduction (Joosse and Testerink, 1977). As an immediate response to ad- verse conditions this temporary state of dormancy could be called a quiescence (Beck, 1980). During winter reproductive diapause and increased cold har- diness has been observed in temperate Collembola (van der Woude and Verhoef, 1987). Testerink (1982a) described a type of dormancy, which seemed to be accompanied by a depression in metabolic rate and which is often called diapause. This occurs when the environmental changes induce diapause in ad- vance of the adverse conditions. As shown by van der Woude and Verhoef (1987) seasonality in CoIlemboIa is caused by photoperiod for reproductive diapause and temperature for cold hardiness under field condi- tions.

The aim of the present study was to establish seasonality of respiration of Orchesellu cincta (L.) and Tomocerus minor (Lubbock) and to relate it to other energy consuming activities, like ~production

and growth. Compared to 0. cincta, T. minor lives in a more stable microhabitat, which has repercussions for reproductive diapause and coId hardiness (van der Woude and Verhoef, 1987). On this basis a seasonal course of respiration was to be expected. One of the complicating factors which may affect the interpretation of metabolic activities is the type of acclimation to seasonal temperatures (Precht et al., 1958; Prosser, 1973). To explain the expected sea- sonal course of respiration an acclimation experi- ment was performed in which both temperature and photoperiod were varied.

MATERIALS AND METHODS

For this respiration study adults of 0. cincta and r. minor weighing 0.65tH ,000 mg were used. To study the seasonal variation of respiration the two species were collected from the litter of a pine plantation near Dronten, the Nether- lands. Collection was monthly, from October 1982 till November 1983. The weather conditions during that period are described in detail elsewhere (van der Woude. 1987). During February 1983 there was a-short period of frost for one week. In summer the months June and July 1983 were very dry. In July the litter was very dry with only locally wet places, from where the animals could be collected. Prior, during and after a frost period in February 1983 collection was repeated at two-weekly intervals. After one night storage, at 5°C (at 20°C during summer), the oxygen consumption was measured at 15°C. Measurements of the direct influence of temperature (5, 10 and 15°C) on the metabolic rate were carried out on field collected animals in January and June 1982. After collection they were kept at IYC, LD 12:12 for three weeks and fed with epiphytal green algae (De~~oc~eeus spec.). The measurements were done on resting animals to produce a standard rate.

In an acclimation experiment cultured animals (20°C; LD 12:12) were used, o~ginatin~ from the above mentioned pine plantation. Six r$mes were investigated: three tem- peratures (20, 12 and 4°C) combined with two nhotooeriods (LD 16: 18 and LD 8: 16). The acclimation’ lasteh 8-10 weeks. From each regime 5 specimens of each species were used for oxygen consumption determination at three tem-

f47

148 H. A. VAN DER WOUDE and E. N. G. JOOSSE

I0 A

____-_---------------- SO0

$ 100

2 s. 300 01

t

; ---_--- 200

B lo

zJ 100

0

loo- 0 B

.- LL

1982 1983

Fig. IA. Annual cycle of the metabolic rate (means + S.E.M.) of Orchesella cincfa (0-O) and Tomocerus minor (A-A). The solid horizontal lines refer to the maximal and minimal level of the metabolic rate due to the moulting cycle for 0. cincfa and the dashed lines for those for T. minor. B.

Annual cycle of the percentage of animals with full guts.

peratures (0.5, IO and 20°C) Only feeding animals were selected to minimize physiological variation. These mea- surements were repeated after exposure to - 2°C for one week.

The oxygen consumption (i.e. resting metabolism) was measured by means of a Cartesian Diver microrespirometer (Lindestrem-Lang, 1943; Halter, 1943). Details are given by Testerink(l982a,b).Stoppedglassdivers(Zeuthen, 1964)were used in the experiment on the influence of temperature on the respiration of field collected animals. For the year cycle experiment and the acclimation experiment open divers, made of poly-acrylamide (Plexiglas), were used, which have the advantage of being unbreakable, so having a long life span. After correction for gas leak, to be determined for each temperature used, these divers gave exactly the same results as the stopped glass divers. The gas volumes of the open divers were in the range of 89.4-92.5 ~1 measured by calibration and checked by calculation.

RESULTS

Year cycle of the metabolic rate

The metabolic rate of 0. cincta and T. minor during a year is presented in Fig. 1A. The large fluctuations of the metabolic rate occurring during a moulting interval (Testerink, 1982b) are indicated for both species as maximal and minimal level. Most

fluctuations fall within the indicated variation. A seasonal effect on the metabolic rate is not apparent. The course of the metabolic rate of both species, however, is strikingly similar. Both species show a decrease at the same time of the year during a frost period in February. The percentage of individuals with a filled gut was zero for 0. cincta and had the lowest value of the year for T. minor, indicating starvation (Fig. IB).

During summer, when the litter had become very dry (July), the metabolic rate gradually decreased to a value below the indicated minimum level for both species. The percentages of animals with a filled gut were not as low as during the frost period, but lower than the expected values (Joosse and Testerink, 1977).

Acclimation

The effects of acclimation temperature and photo- period on the metabolic rate measured at 20, 10 and 0.5”C were studied on 0. cincta and T. minor accli- mated at 20, 12 and 4°C and short and long day. The results appear in Table 1. Statistical analysis (two way ANOVA with replications) revealed significant differences due to exposition temperature (P < 0.001)

Respiration in two temperate Collembola 149

Table I. Effect of temperature on the metabolic rate of 0. &cm and T. minor at six acclimation regimes

\ AT 20 I2 4

LD EJ- \. SD LD SD LD SD

Ox. 20 553.8 _+ 59.5 5305+ 60.0 548. I F 57.8 499.6 4 47.5 434.0 k 64.8 424.Ot41.1

IO 267.6 i 10.5 223.4 + 20.8 226.9 f 36.2 255.7 + 30.9 242.6 i I I .7 192.4 37.5 +

0.5 73.9 * 10.5 55.8 & 8.7 33.9 2 6.4 45.9 i. 11.7 17.4 * 14.4 33.6 7.5 +

T.m. 20 671.1 +67.3 638.2 2 75.8 603.9 i 25.2 534.8 $39.0 560.5 + 28.4 580.0 f 32.9

10 272.6 + 18.8 224.2 & 12.4 215.2 + 17.5 240.1 k21.9 285.3 i_ 41 .O 312.3 f 33.5

0.5 124.OF21.1 79.8 + 17.8 54.6 + 4.0 47.4 + 7.2 24.0 f 3.9 48.0 t 4.6

AT = acclimation temuerature C CI: ET = exmsure temperature ( C); LD = long day (16L:SD); SD = short day (8L:l6D). * . r

whereas there was no effect of the accIimination temperature and photoperiod.

A sudden exposure to - 2°C for one week resulted in the death of all animals acclimated at 20°C. The metabolic rate of the other acclimation groups did not differ from that prior to the exposure (two way ANOVA with replications). It is concluded that no acclimation occurs.

Because of the absence of effects due to accli- mation, all observations were pooled to present the direct effect of temperature on the metabolic rate. The data appear in Fig. 2. The pooled observation on animals collected from the field in January and June 1982 are added. These data showed no effect of sampling date (two way ANOVA with replications). The data show a decrease of the metabolic rate below 5°C. It is apparent that at 0S”C the metabolic rate is lower than expected from extrapolation of that of higher temperatures. The Q,,, in the temperature range 5-20°C within the two experiments varied for 0. cincta from 2.2-3.4 and for T. minor from 2.2-2.6. In the range OS-5°C the Q,,, was 9.7 and 6.7 re- spectively.

DISCUSSION

The respiration of 0. cincta and T. minor shows no changes to seasonal temperatures nor to the experi- mental acclimation conditions. On the basis of different metabolic rates measured on populations sampled by Testerink (1982a) in April and November I978 respectively a decrease in the metabolic rate during winter was expected, at least for 0. cincta. This decrease, however, fell within the range of changes in respiration, due to moulting (Testerink, 1982b), so can be explained by synchronized moult- ing (Joosse and Testerink, 1977).

The respiration of both species did not show changes to the ex~~mental acclimation conditions. Respiratory changes due to acclimation by field temperatures are absent in quite a number of Col- lembola. All species investigated by Peterson (1981) on which the respiration was measured at the pre- vailing field temperature (6, 10 and 15’C), showed a linear response to temperature on a semi-log plot, like the species from this study. If acclimation was present, this was not to be expected.

Effects of temperatures on respiration is generally expressed as Q10 and provides a method to compare ecologicallqt different species and different seasonal activities. The Qlo of the respiration (2.2-3.4) in this study at temperatures of 5°C and higher are com- parable to those reported for temperate Collembola

by Zinkler (1966) and Peterson (1981). A similar Q),, is given for the antartic Collembola Cryptopygus antarricus (Block and Tilbrook, 1978) and can be calculated for Isotoma hiemalis (Zinkler, 1966). At the lower end of the temperature range (3-8°C) the metabolic rate of 8 Collembola species from antartic and alpine regions (Block and Tilbrook, 1978; Block, 1979; Zinkler, 1966; Steigen, 1975) appears to be elevated compared to that from more temperate regions (Peterson, 1981; Zinkler, 1966; this study). This trend for Collembola, already mentioned by Zinkler (1966), was also found in a comparison of polar and temperate terrestrial Mesostigmatid and Cryptostigmatid mites (Block and Young, 1978). Such an elevated respiration should be related to activities at low temperatures, at which the respira- tion of temperate species is near the null point as shown for 0. cincta and T. minor.

From a field study on population dynamics of the two species, van Straalen (1985) concluded a con- tinuing growth during winter. The animals feed throughout the year. With the reproductive diapause this could point to an energy trade off in the animals at temperatures above the null point for growth and reproduction (2-3”C, Joosse and Veltkamp, 1970; van Straalen and Joosse, 1985). In reproducing ani-

600- soo-

400.

300.

p 200.

2 zk 2 loo-

cr” EO-

1 60- 4 (0 f 50-

LOS

30-i

4

&

i i

x

20’ ? c 0 5 IO 15 20

Fig. 2. Effect of temperature on the metabolic rate (logar- ithmic means k S.E.M.) of Orchesda cincra (circles) and Tomocerus minor (triangles). Open symbols refer to laboratory-reared animals and filled symbols to field-

collected animals.

mals energy is divided between growth and re- REFERENCES

productive effort, resulting in a deflection of the growth (van Straalen, 1985) whereas in animals in a Anderson J. F. (1974) Responses to starvation in the spiders

reproductive dormancy all energy is invested in body Lycosa lenta Hentz and Filistata hihernalis (Hentz). Ecol-

growth, resulting in a continuing growth rate (van ogy 55, 576585.

Straalen, 1985). Such a trade off is also shown for Beck S. D. (1980) Insect Photoperiodism. Academic Press,

reproducing and non-reproducing females of 0. New York.

cincta at 20°C (pers. comm. G. M. Janssen): the Block W. (1979) Oxygen consumption of the Antarctic

reproducing females reached a lower maximal size springtail Parisotoma octooculafu (Willem) (Isotomidae).

than the non-reproducing ones. The difference in Reo. Ecol. Biol. Sol. 16, 227~ 233.

biomass was explained by the weight of the produced Block W. and Tilbrook P. J. (1978) Oxygen uptake by

Cryptopychus antarcticus (Collembola) at South Georgia.

eggs. Oikos 30, 61-67.

Two seasonal conditions appear to influence the Block W. and Young S. R. (1978) Metabolic adaptations of

respiration, i.e. frost and (summer) drought. Both Antarctic terrestrial microarthropods. Camp. Biochem.

conditions lead to starvation as observed by low Physiol. 61A, 363-368.

percentages of full guts (see also Joosse and Tester- Holter H. (1943) Technique of the Cartesian Diver. C.R.

ink, 1977 and de With and Joosse, 1971). Starvation Trav. Lab. Carfsberg Ser. Chim. 24, 399478.

in its turn leads to a lowered respiration as shown for Joosse E. N. G. and Veltkamp E. (1970) Some aspects of

0. cincta (Testerink, 1982a; Verhoef and Li, 1983). growth, moulting and reproduction in five species of

Such a phenomenon might also occur in the alpine I. surface dwelling Collembola. Nefh. J. 2001. 20, 315-325.

Joosse E. N. G. and Testerink G. J. (1977) The role of food viridis, showing a lowered metabolic rate during in the population dynamics of Orcheseliu cimfa (Linne)

winter (Kauri et al., 1975). Starvation of 0. cincta is (Collembola). Oecologiu (Berl.) 29, 189 204.

well investigated in the laboratory and in the field: Kauri H., Moldung T. J. and Fjellberg A. (1975) Respird-

when food reserves become depleted especially during tion rates, winter and summer activity in Collembola on

summer (Testerink, 1981) moulting, growth and Hardangervidda. In Ecological studies. Analysis and syn-

reproduction are arrested (Testerink, 1982a), but the thesis. Vol. 17. Fennoscandian Tundra Ecosystems, Part 2

longevity is enhanced (Joosse and Testerink, 1977). (Edited by Wielgolaski, F. E.) pp. I 17~ 12 [. Springer-

Important for survival of summer drought is that the Verlag, Berlin.

transpiration rate declines (Vannier and Verhoef, Lindstrom-Lang, K. U. (1943) On the theory of the

Cartesian Diver microspirometer. C.R. Trar. iah. Car- 1978; Verhoef and Li, 1983). Important for survival Isbern Ser. Chim. 24, 333-398. of frost is that the cold hardiness is increased (van der Petersen H. (1981) The respiratory metabolism of Col-

Woude, 1987). Under field conditions respiration is lembola species from a Danish beechwood. Oikos 37,

decreased thus saving metabolic costs during frost 373-386.

and drought. Starving T. minor did not decline its Precht H., Christopherson. J., Hunsel H. and Lather W.

transpiration rate nor its respiration as observed in (1958) Temperarure and Li/i,. Springer-Verlag, Berlin.

the laboratory (Verhoef and Li, 1983). Prosser C. L. (1973) Comparatiw Animal PhJ,.siology. 3rd

The temperature dependence of several phys- edn. W.B. Saunders. Philadelphia.

iological processes appear to show similarities and Riddle W. A. (1976) Respiratory metabolism of the centi-

pede Nadabius coioradensis (Cockerell): influence of tem- differences between 0. cincta and T. minor. Moulting perature, season and starvation. Comp. Biochem. Physiol.

frequency (Joosse and Veltkamp, 1970) and metabo- 55A, 147-151.

lism have about the same temperature dependency Steigen A. L. (1975) Respiratory rates and respiratory

for both species. Egg production and egg devel- energy loss in terrestrial Invertebrates from Hard-

opment have a steeper temperature dependency for angervidda. In Ecological Studies Vol. 17, Fennoscundian

0. cincta than for T. minor (van Straalen and Joosse. Tundra Ecosysfems. Part 2. (Edited by Wielgolaski F. E.)

1985) whereas the reverse accounts for growth pp: 122-128. Springer, Berlin.

(Joosse and Veltkamp, 1970). 0. cincta and T. minor Straalen N. M. van (1985) Comparative demography of

inhabit a different microhabitat. 0. cincta lives in the forest floor Collembola populations. Oikios 45, 2533265.

Straalen N. M. van and Joosse E. N. G. (1985) Temperature

fluctuating conditions of the upper limit layer and in responses of egg production and egg development in two

trees and T. minor is restricted to the more stable species of Collembola. Pedobiologia 28, 265 273.

habitat of the deeper litter layers (van der Woude and Testerink G. J. (1981) Starvation in a field population of

Verhoef, 1986). On the surface uncertain conditions litter-inhabiting springtails. Methods for determining

with respect to drought and temperature prevail more food reserves in small arthropods. Pedobiologia 21,

than deeper in the soil. Exposure to higher tem- 421427.

peratures at the surface permits a more rapid moult- Testerink G. J. (1982a) Metabolic adaptations to seasonal

ing rate and egg production for 0. cincta. This higher changes in humidity and temperature in litter-inhabiting springtails. Oikos 40, 234240.

reproductive effort coincides with a more pronounced Testerink G. J. (1982b) Strategies in energy consumption

deflection of growth upon reaching sexual maturity and partitioning in Collembola. Ecol. Entomol. 7,

(van Straalen, 1985). The responses of the species 341 ~351.

might thus be an adequate answer to the specific Vannier G. and Verhoef H. A. (1978) Effect of starvation on

environmental conditions of their microhabitat, transpiration and water content in the populations of two co-existing Collembola species. Camp. Biochem. Physiol. MIA, 483489.

Acknowledgemenfs-The authors are grateful to Dr. H. A. Van Senus P. (1985) The effects of temperature, size, season Verhoef for encouragement during the work and for and activity on the metabolic rate of the amphipod valuable comments on earlier drafts of this paper. Mr N. Schlffer is acknowledged for drawing the figures and

Talorchestiu capensis (Crustacea. Tdhtridae). Comp. Bio- them. Physiol. 81A, 263. 269.

MS D. Hoonhout for typing the manuscript. Verhoef H. A. and Li K. W. (1983) Physiological adapta-

150 H. A. VAN DER WO~DE and E. N. G. JOOSSE

Respiration in two temperate Collembola 151

tions to the effects of dry summer periods in Collembola. Proc. of the VIII Intl. CON. of Soil Biol. Louvain-la-Neuve, pp. 345-356.

With N. D. de and Joosse E. N. G. (1971) The ecological effects of moulting in Collembola. Rev. Ecol. Biol. Sol. 8, 111-117.

Woude H. A., van der and Verhoef H. A. (1986) A comparative study of winter survival in two temperate Collembola. Ecol. Entomol. 11. 3333340.

Woude H. A. van der and Verhoef H. A. (1988) Re- productive diapause and cold hardiness in temperate Collembola. J. Insecr Physiol. 34, 387-392.

Woude H. A. van der (1987) Seasonal changes in

cold-hardiness of temperate Collembola. Oikos 50, 231-238.

Young S. R. and Block W. (1980) Some factors affecting metabolic rate in an Antarctic mite. Oikos 34, 178-185.

Zeuthen E. (1964) Microgasometric Methods: Cartesian Divers. In 2nd Int. Congr. Histo- and Cytochemistry. (Edited by Schriebler T. H., Pearse A. G. E. and Wolf H. H.) pp. 70-80. Wiley, New York.

Zinkler D. (1966) Vergleichende Untersuchungen zur At- mungsphysiologie von Collembolen (Apterygota) und anderen Bodenkleinarthropoden. 2. uergl. Physiol. 52, 99-144.