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Temperature and the energetics of development in the house cricket (Acheta domesticus)
ARTICLE IN PRESS
Journal of Insect Physiology 53 (2007) 950–953 www.elsevier.com/locate/jinsphys
Temperature and the energetics of development in the house cricket (Acheta domesticus) David T. Booth, Kirsty Kiddell Ecological Physiology Group, School of Integrative Biology, The University of Queensland, Qld 4072, Australia Received 20 February 2007; received in revised form 20 March 2007; accepted 20 March 2007
Abstract The influence of rearing temperature on the energetics of development was investigated in house crickets (Acheta domesticus). Crickets raised at 25 1C grew slower (0.51 mg d1, dry mass basis) and took longer to develop (119 d) but obtained a greater adult body mass (61 mg, dry mass) than crickets reared at 28 1C (0.99 mg d1, 49 d, 48 mg). Total metabolic energy consumed during development at 25 1C (1351 J) was twice that at 28 1C (580 J) primarily because of the longer development period, and as a consequence the specific net cost of growth was much greater for crickets reared at 25 1C (22.1 kJ g1) than 28 1C (11.9 kJ g1). r 2007 Elsevier Ltd. All rights reserved. Keywords: Insect; Growth; Oxygen consumption; Energy; Temperature
1. Introduction The metabolism of non-flying insects does not produce enough heat to increase their body temperature above ambient temperature, so their body temperature is determined by the surrounding environment as in other ectothermic organisms (Randall et al., 2002). Temperature is arguably the most important abiotic factor influencing the biology of insects. Through the Van’t Hoff effect (a description of the exponential relationship between absolute temperature and rates of chemical reactions) on biochemical and physiological processes temperature influences the processes of digestion, locomotion, reproduction, development and growth of ectotherms all of which play vital roles in insect biology. The influence of temperature on development and growth is particularly important in determining an insect’s life history strategy as growth rate and size at maturity are key traits in life-history evolution (Roff, 1992; Stearns, 1992; Charnov, 1993). Temperature strongly influences the rate of development (the rate of morphological change) and growth (the rate of mass increase), with higher Corresponding author. Tel.: +61 7 3365 2138; fax: +61 7 3365 1655.
E-mail address: [email protected] (D.T. Booth). 0022-1910/$ - see front matter r 2007 Elsevier Ltd. All rights reserved. doi:10.1016/j.jinsphys.2007.03.009
temperatures leading to faster rates as long as temperature remains within the viable development range for that organism (Jarosˇ ı´ k et al., 2004). However, development and growth have different temperature/rate trajectories (SmithGill and Berven, 1979; van de Have and de Jong, 1996; Jarosˇ ı´ k et al., 2004), the rate of development increasing faster than the rate of growth as temperature increases (van de Have and de Jong, 1996), so that ectotherms reared at low temperature take longer to develop but have larger bodies at equivalent developmental stages than ectotherms reared at high temperatures. This phenomenon has been termed the ‘‘temperature size rule’’ (Atkinson, 1994). The influence temperature has on patterns of growth and development of insects has been particularly well studied and modeled (for reviews see Wagner et al., 1984; Liu et al., 1995). However, the energetic aspect of the temperaturedevelopment relation in insects has rarely been investigated. Energy occurs in animals in two forms: (1) chemical energy which is stored in organic molecules, and (2) metabolic energy that is derived from chemical energy and used to power life processes and ultimately ends up being lost to the surrounding environment as heat. This study deals exclusively with metabolic energy expenditure. The most fundamental question: does the metabolic energy expenditure during development in ectotherms vary with
ARTICLE IN PRESS D.T. Booth, K. Kiddell / Journal of Insect Physiology 53 (2007) 950–953
different rearing temperatures has been largely ignored (Angilletta et al., 2006). Conceptually the energetic cost of a growing animal can be divided into three components: (1) energy used for biosynthesis, i.e. energy used to build new cells and tissues, (2) energy used to maintain cells and tissues once they are synthesized, and (3) activity energy, the energy used during locomotion and during the assimilation of nutrients during the digestion of food (Peterson et al., 1999). Temperature may affect each of these components. It is unknown if temperature affects the energetic cost of making new cells and tissues (Wieser, 1994; Angilletta et al., 2006), but because growth rate is faster at higher temperature; the rate of energy use for biosynthesis is expected to increase with increasing temperature. The maintenance component of energy expenditure will increase with increasing temperature because of the Van’t Hoff effect on biochemical processes at the cellular level. Activity levels of ectotherms and hence the energy expenditure associated with activity is also likely to increase at higher temperatures. From these observations one might predict that rearing ectotherms such as insects at high temperatures would be energetically more costly than at low temperatures. However, the time needed for development is considerably shortened at higher temperatures, so a trade-off between the increase in the rate of energy expenditure and the decrease in time taken to complete development at high temperatures may mean that rearing temperature has little overall influence on the total energy expended during development (Angilletta et al., 2006). In this study, we estimated the energetic cost of development from the metabolic energy expenditure rates in the house cricket Acheta domesticus (Linnaeus) at two different temperatures to discover if rearing temperature influenced the total energy expended from hatching to maturity. 2. Material and methods One-day-old house crickets, A. domesticus (Linnaeus) were obtained from a commercial supplier. This species typically undergoes eight instar stages before reaching maturity (Roe et al., 1985). Crickets were raised at two temperatures, 25 and 28 1C (71 1C), in constant temperature cabinets at a relative humidity of 60% and a daily 12L:12D light cycle. Approximately 200 individuals were reared together in opaque plastic containers (35 cm 25 cm 12 cm) which had lids with a 10 cm 10 cm hole covered with mosquito screening mesh to allow air circulation. The bottom of each container was lined with 3 cm of dry sand and pieces of folded cardboard to provide refuge. The sand and cardboard were changed every 2 weeks. Crickets were fed a mixture of Go-Cats dry cat food, and Friskiess goldfish flakes in excess daily. In addition fresh lettuce and celery were provided every 3 days. Water was provided via Petri dishes filled with wet cotton wool that were replaced every 2 days.
951
Oxygen consumption was measured every seventh day throughout development by closed system respirometry. Depending on cricket size one to six crickets were placed into a 60 mL syringe along with a drop of water (to insure the atmosphere within the syringe was saturated with water vapor), the syringe sealed and left at their rearing temperature for 2–3 h. The barometric pressure and time was recorded then the syringe was sealed. At the end of the measurement period, the time was recorded and the syringe gas injected through soda lime (to remove carbon dioxide) and Drierite (to remove water vapor) into an oxygen analyzer (Helox2, MBE Electronic, Switzerland). Oxygen consumption was then calculated using Eq. (9) of Vleck (1987). In cases where several individuals were measured simultaneously in the same syringe, oxygen consumption per individual was calculated by dividing the total oxygen consumption in the syringe by the number of individuals in the syringe. Five replicate measurements were made for each temperature on each measurement day. At the end of oxygen consumption measurements, the wet and dry mass of the crickets was determined. Live crickets were placed in a sealed plastic vial along with a cotton wool swab that had been sprayed with Morteins fly spray (active ingredients 2.09 g kg1 bioallethrin and 0.39 g kg1 bioresmethrin). This method insured that cricket mass was unaffected by the killing process. Dead crickets were then removed and weighed (71 mg) on an electronic balance to determine wet mass. Crickets were then desiccated in an oven at 55 1C for 24 h and dry mass determined by weighing them again. Data are presented as means7S.E. Comparisons of variables between temperatures were made with Student’s two-tail t-tests. Mass adjusted oxygen consumption and energy consumption values were compared by ANCOVA where dry mass was the covariate as recommended by Packard and Boardman (1999). Water content variation between developmental stages within each temperature was tested via one-way ANOVA on arcsine transformed percentage data. To enable statistical comparisons of total metabolic energy consumed during development, the five replicate measurements from each measurement day were ranked from highest to lowest, and individual oxygen consumption versus time curves constructed for each of the five ranks. The area under each of these curves was calculated to estimate the total amount of oxygen consumed for each rank, and these values converted to energy consumed using a conversion factor of 20.9 J mL1 O2 (Schmidt-Nielsen, 1997) based on the finding that growing house crickets have a respiratory quotient of 1.0 (Roe et al., 1980, 1985). Statistical significant was assumed if Po0.05. 3. Results Crickets raised at 28 1C reached maturity after 49 days and those raised at 25 1C reached maturity after 119 days (Fig. 1). Dry mass of newly enclosed adults at 25 1C (6171 mg) was greater (P ¼ 0.040) than those from 28 1C
ARTICLE IN PRESS D.T. Booth, K. Kiddell / Journal of Insect Physiology 53 (2007) 950–953
952
70
A
Dry mass (mg)
60
adult
start of last instar
50
adult
start of last instar
40 30 20 25°C
10
28°C
Oxygen consumption (µL/h)
0
B
160 140 120 100 80 60 40 20 0 0
20
40
60 80 100 Days of development
120
140
Fig. 1. The influence of rearing temperature on (A) growth and (B) oxygen consumption of house crickets (Acheta domesticus). Symbols are means and error bars standard errors of the mean.
(4874 mg), but average growth rate at 28 1C (0.997 0.09 mg d1, dry mass basis) was faster (P ¼ 0.004) than 25 1C (0.5170.02 mg d1). At both 25 and 28 1C growth rate was fastest during the final instar stage (Fig. 1A). Water content of crickets reared at 25 1C (7674%) was similar to crickets reared at 28 1C (7875%) and remained at these levels throughout development. Oxygen consumption of newly enclosed adult crickets reared at 25 1C (123720 mL h1) was similar to that of adult crickets reared at 28 1C (121730 mL h1) (Fig. 1B). Rate of oxygen consumption increased dramatically during the last instar in crickets reared at both temperatures (Fig. 1B). Total metabolic energy expenditure during development was greater (Po0.001) at 25 1C (13517 107 J) than at 28 1C (580772 J) and the specific net cost of growth which is the total metabolic energy expenditure during development divided by the dry mass of the adult (Wieser, 1994) was also greater (Po0.001) in crickets reared at 25 1C (22.170.7 kJ g1) than crickets reared at 28 1C (11.970.8 kJ g1). 4. Discussion As expected both growth and development rates of house crickets were faster at 28 1C than 25 1C and as predicted by the ‘‘temperature size rule’’ (Atkinson, 1994) newly enclosed adult crickets reared at 25 1C were larger
than those reared at 28 1C presumably because the rates of growth and development were thermally uncoupled to some extent. The pattern of growth at the two temperatures was similar, steady growth through the first seven instars and then very rapid growth with an approximate doubling of mass during the eighth instar. This growth pattern has been reported previously for house crickets (Lipsitz and McFarlane, 1971; Clifford et al., 1977). The extremely prolonged development time at 25 1C compared to 28 1C suggests that 25 1C is a sub-optimal temperature close to this species’ lower thermal limit for continuous growth. Support for this hypothesis comes from Busvine’s (1955) data that indicates development times of between 165 and 240 days at 23 1C, and the fact that we tried raising crickets at a constant temperature of 21 1C and found that they failed to thrive, only reaching a dry mass of 6 mg before dying between 80 and 100 days after hatching. The water content of our crickets (77%) is similar to values (70–77%) previously reported for house crickets (Woodring et al., 1977; Roe et al., 1980, 1985). However, the adult dry mass of our house crickets (45–70 mg) was much smaller than previously reported (100–120 mg; Woodring et al., 1977; Roe et al., 1980, 1985). This difference may be caused by differences in genetic strains of cricket colonies and/or differences in food and rearing techniques. The patterns of oxygen consumption at 25 and 28 1C were similar and reflected the growth patterns, i.e. a steady increase for the first seven instars, and then a rapid increase during the last instar before reaching maturity. The absolute peak rates of oxygen consumption (120 mL h1) were similar at both temperatures, which at first glance seem unusual as higher metabolic rates are expected in ectotherms at higher temperatures. This discrepancy may be explained by differences in body mass of crickets at each temperature as mass-specific metabolic rates (mass expressed on a dry mass basis) was greater at 28 1C (2.5 mL g1 h1) than at 25 1C (2.0 mL g1 h1) which corresponds to a Q10 of 2.1. Using ANCOVA adjusted means for a cricket weighing 55 mg oxygen consumption is calculated to be 100 and 138 mL h1 for 25 and 28 1C, respectively, which corresponds to a Q10 of 2.9. Both Q10 values are within the range expected for physiological processes (2.0–3.0, Schmidt-Nielsen, 1997). However, because of the extended development time at 25 1C, crickets at this temperature presumably spent much more time moving about than crickets at 28 1C and as a consequence of this greater period of activity had a much greater total oxygen consumption and hence energy expenditure. Roe et al. (1980, 1985) also found that female house crickets at 25 1C consumed more oxygen than crickets from 30 or 35 1C during the eighth instar because of the prolonged development period. In our study, the difference in energy expenditure between crickets reared at 25 and 28 1C was greater than the difference in dry mass of newly enclosed adults from these temperatures, and as a consequence the specific net cost of growth at 25 1C (22.1 kJ g1) was twice that at 28 1C (11.9 kJ g1).
ARTICLE IN PRESS D.T. Booth, K. Kiddell / Journal of Insect Physiology 53 (2007) 950–953
The small amount of data reporting the net cost of growth in ectotherms has been summarized by Peterson et al. (1999). For fish, an amphibian, and a mussel reared under captive conditions net cost of growth averaged 8 kJ g1, for a freeranging snake it also averaged 8 kJ g1, but for a free-ranging lizard the estimate was 34 kJ g1. To date no studies have reported the influence of temperature on net cost of growth in ectotherms, but calculations for the eighth instar of house crickets can be made from data reported in Woodring et al. (1977) and Roe et al. (1985). Values of 33, 23 and 23 kJ g1 were calculated for temperatures of 25, 30 and 35 1C. Values for the eighth instar of crickets in the current study were 26.9 and 13.5 kJ g1 at temperatures of 25 and 28 1C. The reason(s) why the net cost of growth of the eighth instar larvae measured at 28 1C in the current study was considerably less than that calculated for crickets in previous studies (Roe et al., 1985) may relate to different strains of house crickets and/or different rearing conditions. As previously mentioned the newly enclosed adult crickets in Roe et al.’s (1985) study were about twice the size of the crickets in the current study, and prior to the eighth instar crickets in Roe et al.’s (1985) study were reared at 30 1C while ours were reared at 25 1C. The net cost of growth for the entire larval period of blow flies (Lucilia illustris) at 20, 26, 29.5 and 35 1C temperatures was 9.6, 9.8, 13.4 and 12.8 kJ g1 (calculated from the data reported in Hanski (1976)). These limited data indicate that the specific net cost of growth varies greatly between different species, and can be affected by rearing temperature and rearing conditions. In house crickets, rearing at 25 1C (a temperature close to the lower thermal limit of successful development in this species (Busvine, 1955)) is more costly than at higher temperatures, the greater cost apparently being due to the prolonging of the development period at low temperature. In contrast, blow-fly larvae reared at higher temperatures had a higher specific net growth cost. When reviewing the insect literature, Roe et al. (1985) concluded most studies found growth and metabolic efficiencies to decrease at temperatures outside an optimal temperature range. The specific net cost of growth data presented here would support this conclusion if temperatures below 28 1C were sub-optimal for house crickets, and temperatures above 26 1C were sub-optimal for blow flies. Acknowledgment The experiments reported here comply with the current Australian animal experimentation laws. References Angilletta, M.J., Lee, V., Silva, A.C., 2006. Energetics of lizard embryos are not canalized by thermal acclimation. Physiological and Biochemical Zoology 79, 573–580.
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Atkinson, D., 1994. Temperature and organism size: a biological law for ectotherms? Advances in Ecological Research 25, 1–58. Busvine, J.R., 1955. Simple methods for rearing the cricket (Gryllulus domesticus L.) with some observations on speed of development at different temperatures. Proceedings of the Royal Entomological Society of London 30, 15–18. Charnov, E., 1993. Life History Invariants: Some Explorations of Symmetry in Evolutionary Ecology. Oxford University Press, Oxford. Clifford, C.W., Roe, R.M., Woodring, J.P., 1977. Rearing methods for obtaining house crickets, Acheta domesticus, of known age, sex and instar. Annals of the Entomological Society of America 70, 69–74. Hanski, I., 1976. Assimilation by Lucilia illustris (Diptera) larvae in constant and changing temperatures. OIKOS 27, 288–299. Jarosˇ ı´ k, V., Kratochvı´ l, K., Honeˇk, A., Dixon, A.F.G., 2004. A general rule for the dependence of developmental rate on temperature in ectothermic animals. Proceedings of the Royal Society of London B (Suppl) 271, s219–s221. Lipsitz, E.Y., McFarlane, J.E., 1971. Analysis of lipid during the life of the house cricket, Acheta domesticus. Insect Biochemistry 1, 446–460. Liu, S.S., Zhang, G.M., Zhu, J., 1995. Influence of temperature variations on rate of development in insects: analysis of case studies from entomological literature. Annals of the Entomological Society of America 88, 107–119. Packard, G.C., Boardman, T.J., 1999. The use of percentages and sizespecific indices to normalize physiological data for variation in body size: wasted time, wasted effort? Comparative Biochemistry and Physiology A 122, 37–44. Peterson, C.C., Walton, B.M., Bennett, A.F., 1999. Metabolic costs of growth in free-living garter snakes and the energy budgets of ectotherms. Functional Ecology 13, 500–507. Randall, R., Burggren, W., French, K., 2002. Eckert Animal Physiology Mechanisms and Adaptations. W.H. Freeman and Company, New York. Roe, R.M., Clifford, C.W., Woodring, J.P., 1980. The effect of temperature on feeding, growth, and metabolism during the last larval stadium of the female house cricket, Acheta domesticus. Journal of Insect Physiology 26, 639–644. Roe, R.M., Clifford, C.W., Woodring, J.P., 1985. The effect of temperature on energy distribution during the last-larval stadium of the female house cricket, Acheta domesticus. Journal of Insect Physiology 31, 371–378. Roff, D.A., 1992. The Evolution of Life-Histories: Theories and Analysis. Chapman & Hall, New York. Schmidt-Nielsen, K., 1997. Animal Physiology: Adaptation and Environment, fifth ed. Cambridge University Press, Cambridge. Smith-Gill, S.J., Berven, K.A., 1979. Predicting amphibian metamorphosis. American Naturalist 113, 563–585. Stearns, S.C., 1992. The Evolution of Life-Histories. Oxford University Press, Oxford. van de Have, T.M., de Jong, G., 1996. Adult size in ectotherms: temperature effects on growth and differentiation. Journal of Theoretical Biology 183, 329–340. Vleck, D., 1987. Measurement of oxygen consumption, carbon dioxide production and water vapor production in a closed system. Journal of Applied Physiology 62, 2103–2106. Wagner, T.L., Wu, H., Sharpe, P.J.H., Schoolfield, R.M., Coulson, R.N., 1984. Modeling insect development rates: a literature review and application of a biophysical model. Annals of the Entomological Society of America 77, 208–225. Wieser, W., 1994. Cost of growth in cells and organisms; general rules and comparative aspects. Biological Reviews 68, 1–33. Woodring, J.P., Roe, M.R., Clifford, C.W., 1977. Relation of feeding, growth, and metabolism to age in the larval, female house cricket. Journal of Insect Physiology 23, 207–212.
Journal of Insect Physiology 53 (2007) 950–953 www.elsevier.com/locate/jinsphys
Temperature and the energetics of development in the house cricket (Acheta domesticus) David T. Booth, Kirsty Kiddell Ecological Physiology Group, School of Integrative Biology, The University of Queensland, Qld 4072, Australia Received 20 February 2007; received in revised form 20 March 2007; accepted 20 March 2007
Abstract The influence of rearing temperature on the energetics of development was investigated in house crickets (Acheta domesticus). Crickets raised at 25 1C grew slower (0.51 mg d1, dry mass basis) and took longer to develop (119 d) but obtained a greater adult body mass (61 mg, dry mass) than crickets reared at 28 1C (0.99 mg d1, 49 d, 48 mg). Total metabolic energy consumed during development at 25 1C (1351 J) was twice that at 28 1C (580 J) primarily because of the longer development period, and as a consequence the specific net cost of growth was much greater for crickets reared at 25 1C (22.1 kJ g1) than 28 1C (11.9 kJ g1). r 2007 Elsevier Ltd. All rights reserved. Keywords: Insect; Growth; Oxygen consumption; Energy; Temperature
1. Introduction The metabolism of non-flying insects does not produce enough heat to increase their body temperature above ambient temperature, so their body temperature is determined by the surrounding environment as in other ectothermic organisms (Randall et al., 2002). Temperature is arguably the most important abiotic factor influencing the biology of insects. Through the Van’t Hoff effect (a description of the exponential relationship between absolute temperature and rates of chemical reactions) on biochemical and physiological processes temperature influences the processes of digestion, locomotion, reproduction, development and growth of ectotherms all of which play vital roles in insect biology. The influence of temperature on development and growth is particularly important in determining an insect’s life history strategy as growth rate and size at maturity are key traits in life-history evolution (Roff, 1992; Stearns, 1992; Charnov, 1993). Temperature strongly influences the rate of development (the rate of morphological change) and growth (the rate of mass increase), with higher Corresponding author. Tel.: +61 7 3365 2138; fax: +61 7 3365 1655.
E-mail address: [email protected] (D.T. Booth). 0022-1910/$ - see front matter r 2007 Elsevier Ltd. All rights reserved. doi:10.1016/j.jinsphys.2007.03.009
temperatures leading to faster rates as long as temperature remains within the viable development range for that organism (Jarosˇ ı´ k et al., 2004). However, development and growth have different temperature/rate trajectories (SmithGill and Berven, 1979; van de Have and de Jong, 1996; Jarosˇ ı´ k et al., 2004), the rate of development increasing faster than the rate of growth as temperature increases (van de Have and de Jong, 1996), so that ectotherms reared at low temperature take longer to develop but have larger bodies at equivalent developmental stages than ectotherms reared at high temperatures. This phenomenon has been termed the ‘‘temperature size rule’’ (Atkinson, 1994). The influence temperature has on patterns of growth and development of insects has been particularly well studied and modeled (for reviews see Wagner et al., 1984; Liu et al., 1995). However, the energetic aspect of the temperaturedevelopment relation in insects has rarely been investigated. Energy occurs in animals in two forms: (1) chemical energy which is stored in organic molecules, and (2) metabolic energy that is derived from chemical energy and used to power life processes and ultimately ends up being lost to the surrounding environment as heat. This study deals exclusively with metabolic energy expenditure. The most fundamental question: does the metabolic energy expenditure during development in ectotherms vary with
ARTICLE IN PRESS D.T. Booth, K. Kiddell / Journal of Insect Physiology 53 (2007) 950–953
different rearing temperatures has been largely ignored (Angilletta et al., 2006). Conceptually the energetic cost of a growing animal can be divided into three components: (1) energy used for biosynthesis, i.e. energy used to build new cells and tissues, (2) energy used to maintain cells and tissues once they are synthesized, and (3) activity energy, the energy used during locomotion and during the assimilation of nutrients during the digestion of food (Peterson et al., 1999). Temperature may affect each of these components. It is unknown if temperature affects the energetic cost of making new cells and tissues (Wieser, 1994; Angilletta et al., 2006), but because growth rate is faster at higher temperature; the rate of energy use for biosynthesis is expected to increase with increasing temperature. The maintenance component of energy expenditure will increase with increasing temperature because of the Van’t Hoff effect on biochemical processes at the cellular level. Activity levels of ectotherms and hence the energy expenditure associated with activity is also likely to increase at higher temperatures. From these observations one might predict that rearing ectotherms such as insects at high temperatures would be energetically more costly than at low temperatures. However, the time needed for development is considerably shortened at higher temperatures, so a trade-off between the increase in the rate of energy expenditure and the decrease in time taken to complete development at high temperatures may mean that rearing temperature has little overall influence on the total energy expended during development (Angilletta et al., 2006). In this study, we estimated the energetic cost of development from the metabolic energy expenditure rates in the house cricket Acheta domesticus (Linnaeus) at two different temperatures to discover if rearing temperature influenced the total energy expended from hatching to maturity. 2. Material and methods One-day-old house crickets, A. domesticus (Linnaeus) were obtained from a commercial supplier. This species typically undergoes eight instar stages before reaching maturity (Roe et al., 1985). Crickets were raised at two temperatures, 25 and 28 1C (71 1C), in constant temperature cabinets at a relative humidity of 60% and a daily 12L:12D light cycle. Approximately 200 individuals were reared together in opaque plastic containers (35 cm 25 cm 12 cm) which had lids with a 10 cm 10 cm hole covered with mosquito screening mesh to allow air circulation. The bottom of each container was lined with 3 cm of dry sand and pieces of folded cardboard to provide refuge. The sand and cardboard were changed every 2 weeks. Crickets were fed a mixture of Go-Cats dry cat food, and Friskiess goldfish flakes in excess daily. In addition fresh lettuce and celery were provided every 3 days. Water was provided via Petri dishes filled with wet cotton wool that were replaced every 2 days.
951
Oxygen consumption was measured every seventh day throughout development by closed system respirometry. Depending on cricket size one to six crickets were placed into a 60 mL syringe along with a drop of water (to insure the atmosphere within the syringe was saturated with water vapor), the syringe sealed and left at their rearing temperature for 2–3 h. The barometric pressure and time was recorded then the syringe was sealed. At the end of the measurement period, the time was recorded and the syringe gas injected through soda lime (to remove carbon dioxide) and Drierite (to remove water vapor) into an oxygen analyzer (Helox2, MBE Electronic, Switzerland). Oxygen consumption was then calculated using Eq. (9) of Vleck (1987). In cases where several individuals were measured simultaneously in the same syringe, oxygen consumption per individual was calculated by dividing the total oxygen consumption in the syringe by the number of individuals in the syringe. Five replicate measurements were made for each temperature on each measurement day. At the end of oxygen consumption measurements, the wet and dry mass of the crickets was determined. Live crickets were placed in a sealed plastic vial along with a cotton wool swab that had been sprayed with Morteins fly spray (active ingredients 2.09 g kg1 bioallethrin and 0.39 g kg1 bioresmethrin). This method insured that cricket mass was unaffected by the killing process. Dead crickets were then removed and weighed (71 mg) on an electronic balance to determine wet mass. Crickets were then desiccated in an oven at 55 1C for 24 h and dry mass determined by weighing them again. Data are presented as means7S.E. Comparisons of variables between temperatures were made with Student’s two-tail t-tests. Mass adjusted oxygen consumption and energy consumption values were compared by ANCOVA where dry mass was the covariate as recommended by Packard and Boardman (1999). Water content variation between developmental stages within each temperature was tested via one-way ANOVA on arcsine transformed percentage data. To enable statistical comparisons of total metabolic energy consumed during development, the five replicate measurements from each measurement day were ranked from highest to lowest, and individual oxygen consumption versus time curves constructed for each of the five ranks. The area under each of these curves was calculated to estimate the total amount of oxygen consumed for each rank, and these values converted to energy consumed using a conversion factor of 20.9 J mL1 O2 (Schmidt-Nielsen, 1997) based on the finding that growing house crickets have a respiratory quotient of 1.0 (Roe et al., 1980, 1985). Statistical significant was assumed if Po0.05. 3. Results Crickets raised at 28 1C reached maturity after 49 days and those raised at 25 1C reached maturity after 119 days (Fig. 1). Dry mass of newly enclosed adults at 25 1C (6171 mg) was greater (P ¼ 0.040) than those from 28 1C
ARTICLE IN PRESS D.T. Booth, K. Kiddell / Journal of Insect Physiology 53 (2007) 950–953
952
70
A
Dry mass (mg)
60
adult
start of last instar
50
adult
start of last instar
40 30 20 25°C
10
28°C
Oxygen consumption (µL/h)
0
B
160 140 120 100 80 60 40 20 0 0
20
40
60 80 100 Days of development
120
140
Fig. 1. The influence of rearing temperature on (A) growth and (B) oxygen consumption of house crickets (Acheta domesticus). Symbols are means and error bars standard errors of the mean.
(4874 mg), but average growth rate at 28 1C (0.997 0.09 mg d1, dry mass basis) was faster (P ¼ 0.004) than 25 1C (0.5170.02 mg d1). At both 25 and 28 1C growth rate was fastest during the final instar stage (Fig. 1A). Water content of crickets reared at 25 1C (7674%) was similar to crickets reared at 28 1C (7875%) and remained at these levels throughout development. Oxygen consumption of newly enclosed adult crickets reared at 25 1C (123720 mL h1) was similar to that of adult crickets reared at 28 1C (121730 mL h1) (Fig. 1B). Rate of oxygen consumption increased dramatically during the last instar in crickets reared at both temperatures (Fig. 1B). Total metabolic energy expenditure during development was greater (Po0.001) at 25 1C (13517 107 J) than at 28 1C (580772 J) and the specific net cost of growth which is the total metabolic energy expenditure during development divided by the dry mass of the adult (Wieser, 1994) was also greater (Po0.001) in crickets reared at 25 1C (22.170.7 kJ g1) than crickets reared at 28 1C (11.970.8 kJ g1). 4. Discussion As expected both growth and development rates of house crickets were faster at 28 1C than 25 1C and as predicted by the ‘‘temperature size rule’’ (Atkinson, 1994) newly enclosed adult crickets reared at 25 1C were larger
than those reared at 28 1C presumably because the rates of growth and development were thermally uncoupled to some extent. The pattern of growth at the two temperatures was similar, steady growth through the first seven instars and then very rapid growth with an approximate doubling of mass during the eighth instar. This growth pattern has been reported previously for house crickets (Lipsitz and McFarlane, 1971; Clifford et al., 1977). The extremely prolonged development time at 25 1C compared to 28 1C suggests that 25 1C is a sub-optimal temperature close to this species’ lower thermal limit for continuous growth. Support for this hypothesis comes from Busvine’s (1955) data that indicates development times of between 165 and 240 days at 23 1C, and the fact that we tried raising crickets at a constant temperature of 21 1C and found that they failed to thrive, only reaching a dry mass of 6 mg before dying between 80 and 100 days after hatching. The water content of our crickets (77%) is similar to values (70–77%) previously reported for house crickets (Woodring et al., 1977; Roe et al., 1980, 1985). However, the adult dry mass of our house crickets (45–70 mg) was much smaller than previously reported (100–120 mg; Woodring et al., 1977; Roe et al., 1980, 1985). This difference may be caused by differences in genetic strains of cricket colonies and/or differences in food and rearing techniques. The patterns of oxygen consumption at 25 and 28 1C were similar and reflected the growth patterns, i.e. a steady increase for the first seven instars, and then a rapid increase during the last instar before reaching maturity. The absolute peak rates of oxygen consumption (120 mL h1) were similar at both temperatures, which at first glance seem unusual as higher metabolic rates are expected in ectotherms at higher temperatures. This discrepancy may be explained by differences in body mass of crickets at each temperature as mass-specific metabolic rates (mass expressed on a dry mass basis) was greater at 28 1C (2.5 mL g1 h1) than at 25 1C (2.0 mL g1 h1) which corresponds to a Q10 of 2.1. Using ANCOVA adjusted means for a cricket weighing 55 mg oxygen consumption is calculated to be 100 and 138 mL h1 for 25 and 28 1C, respectively, which corresponds to a Q10 of 2.9. Both Q10 values are within the range expected for physiological processes (2.0–3.0, Schmidt-Nielsen, 1997). However, because of the extended development time at 25 1C, crickets at this temperature presumably spent much more time moving about than crickets at 28 1C and as a consequence of this greater period of activity had a much greater total oxygen consumption and hence energy expenditure. Roe et al. (1980, 1985) also found that female house crickets at 25 1C consumed more oxygen than crickets from 30 or 35 1C during the eighth instar because of the prolonged development period. In our study, the difference in energy expenditure between crickets reared at 25 and 28 1C was greater than the difference in dry mass of newly enclosed adults from these temperatures, and as a consequence the specific net cost of growth at 25 1C (22.1 kJ g1) was twice that at 28 1C (11.9 kJ g1).
ARTICLE IN PRESS D.T. Booth, K. Kiddell / Journal of Insect Physiology 53 (2007) 950–953
The small amount of data reporting the net cost of growth in ectotherms has been summarized by Peterson et al. (1999). For fish, an amphibian, and a mussel reared under captive conditions net cost of growth averaged 8 kJ g1, for a freeranging snake it also averaged 8 kJ g1, but for a free-ranging lizard the estimate was 34 kJ g1. To date no studies have reported the influence of temperature on net cost of growth in ectotherms, but calculations for the eighth instar of house crickets can be made from data reported in Woodring et al. (1977) and Roe et al. (1985). Values of 33, 23 and 23 kJ g1 were calculated for temperatures of 25, 30 and 35 1C. Values for the eighth instar of crickets in the current study were 26.9 and 13.5 kJ g1 at temperatures of 25 and 28 1C. The reason(s) why the net cost of growth of the eighth instar larvae measured at 28 1C in the current study was considerably less than that calculated for crickets in previous studies (Roe et al., 1985) may relate to different strains of house crickets and/or different rearing conditions. As previously mentioned the newly enclosed adult crickets in Roe et al.’s (1985) study were about twice the size of the crickets in the current study, and prior to the eighth instar crickets in Roe et al.’s (1985) study were reared at 30 1C while ours were reared at 25 1C. The net cost of growth for the entire larval period of blow flies (Lucilia illustris) at 20, 26, 29.5 and 35 1C temperatures was 9.6, 9.8, 13.4 and 12.8 kJ g1 (calculated from the data reported in Hanski (1976)). These limited data indicate that the specific net cost of growth varies greatly between different species, and can be affected by rearing temperature and rearing conditions. In house crickets, rearing at 25 1C (a temperature close to the lower thermal limit of successful development in this species (Busvine, 1955)) is more costly than at higher temperatures, the greater cost apparently being due to the prolonging of the development period at low temperature. In contrast, blow-fly larvae reared at higher temperatures had a higher specific net growth cost. When reviewing the insect literature, Roe et al. (1985) concluded most studies found growth and metabolic efficiencies to decrease at temperatures outside an optimal temperature range. The specific net cost of growth data presented here would support this conclusion if temperatures below 28 1C were sub-optimal for house crickets, and temperatures above 26 1C were sub-optimal for blow flies. Acknowledgment The experiments reported here comply with the current Australian animal experimentation laws. References Angilletta, M.J., Lee, V., Silva, A.C., 2006. Energetics of lizard embryos are not canalized by thermal acclimation. Physiological and Biochemical Zoology 79, 573–580.
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