Advertisement

The Science of Nature

, 105:65 | Cite as

Increased lipid accumulation but not reduced metabolism explains improved starvation tolerance in cold-acclimated arthropod predators

  • Kim JensenEmail author
  • Jakob V. Michaelsen
  • Marie T. Larsen
  • Torsten N. Kristensen
  • Martin Holmstrup
  • Johannes Overgaard
Original Paper
  • 102 Downloads

Abstract

Predatory arthropods are used for biological control in greenhouses, but there is increasing interest to extend their use to the outdoor environment where temperatures are typically lower. Acclimation at low temperature increases the ability of ectotherms to cope with subsequent more extreme cold, but may involve costs or benefits to other performance traits. A recent study in mesostigmatid mites (Gaeolaelaps aculeifer) showed that starvation tolerance was improved following a period of cold exposure. However, the physiological mechanisms that underlie improved starvation tolerance following cold exposure were not investigated. To examine whether cold acclimation would also improve starvation tolerance in an insect, we repeated the starvation study in another arthropod predator, the pirate bug Orius majusculus, as well as in G. aculeifer. Before tests, the two species were acclimated at 10, 15, or 20 °C for 7 (G. aculeifer) or 16 (O. majusculus) days. We then analyzed the effects of thermal exposure on body composition, consumption, and basal metabolic rate in both species. Our results confirmed that exposure to low temperature improves starvation tolerance in these arthropod predators. Body composition analyses revealed that both species had accumulated larger lipid stores during exposure to colder temperature, which at least in part can explain the larger starvation tolerance following cold exposure. In contrast, consumption and basal metabolic rate were not changed by thermal acclimation. Our study indicates that predatory arthropods exposed to cold increase their physiological robustness and ability to endure environmental challenges, including low temperature and low prey availability.

Keywords

Cold acclimation Gaeolaelaps aculeifer Lipid storage Orius majusculus Starvation tolerance 

Notes

Acknowledgements

We thank Søren Toft and three anonymous reviewers for their constructive comments on earlier versions of the manuscript.

Funding

This study was funded by the Danish Council for Independent Research–Technology and Production Sciences (DFF-4184-00248).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. Addo-Bediako A, Chown S, Gaston K (2002) Metabolic cold adaptation in insects: a large-scale perspective. Funct Ecol 16:332–338CrossRefGoogle Scholar
  2. Alemu T, Alemneh T, Pertoldi C, Ambelu A, Bahrndorff S (2017) Costs and benefits of heat and cold hardening in a soil arthropod. Biol J Linn Soc 122:765–773CrossRefGoogle Scholar
  3. Alton LA, Condon C, White CR, Angilletta MJ (2017) Colder environments did not select for a faster metabolism during experimental evolution of Drosophila melanogaster. Evolution 71:145–152CrossRefGoogle Scholar
  4. Anderson JF (1970) Metabolic rates of spiders. Comp Biochem Physiol 33:51–72CrossRefGoogle Scholar
  5. Angilletta MJ (2009) Thermal adaptation: a theoretical and empirical synthesis. Oxford University Press, OxfordCrossRefGoogle Scholar
  6. Berrigan D (1997) Acclimation of metabolic rate in response to developmental temperature in Drosophila melanogaster. J Therm Biol 22:213–218CrossRefGoogle Scholar
  7. Bjørge JD, Overgaard J, Malte H, Gianotten N, Heckmann L-H (2018) Role of temperature on growth and metabolic rate in the tenebrionid beetles Alphitobius diaperinus and Tenebrio molitor. J Insect Physiol 107:89–96CrossRefGoogle Scholar
  8. Bubliy OA, Kristensen TN, Kellermann V, Loeschcke V (2012) Plastic responses to four environmental stresses and cross-resistance in a laboratory population of Drosophila melanogaster. Funct Ecol 26:245–253CrossRefGoogle Scholar
  9. Chown SL, Gaston KJ (1999) Exploring links between physiology and ecology at macro-scales: the role of respiratory metabolism in insects. Biol Rev 74:87–120CrossRefGoogle Scholar
  10. Chown SL, Nicolson S (2004) Insect physiological ecology: mechanisms and patterns. Oxford University Press, OxfordCrossRefGoogle Scholar
  11. Chown SL, Terblanche JS (2007) Physiological diversity in insects: ecological and evolutionary contexts. Adv Insect Physiol 33:50–152CrossRefGoogle Scholar
  12. Colinet H, Boivin G (2011) Insect parasitoids cold storage: a comprehensive review of factors of variability and consequences. Biol Control 58:83–95CrossRefGoogle Scholar
  13. DeWitt TJ, Sih A, Wilson DS (1998) Costs and limits of phenotypic plasticity. Trends Ecol Evol 13:77–81CrossRefGoogle Scholar
  14. Dussutour A, Poissonnier L-A, Buhl J, Simpson SJ (2016) Resistance to nutritional stress in ants: when being fat is advantageous. J Exp Biol 219:824–833CrossRefGoogle Scholar
  15. Ghazy NA, Osakabe M, Negm MW, Schausberger P, Gotoh T, Amano H (2016) Phytoseiid mites under environmental stress. Biol Control 96:120–134CrossRefGoogle Scholar
  16. Hahn DA, Denlinger DL (2007) Meeting the energetic demands of insect diapause: nutrient storage and utilization. J Insect Physiol 53:760–773CrossRefGoogle Scholar
  17. Hahn DA, Denlinger DL (2011) Energetics of insect diapause. Annu Rev Entomol 56:103–121CrossRefGoogle Scholar
  18. Harrison JF, Woods HA, Roberts SP (2012) Ecological and environmental physiology of insects. Oxford University Press, New YorkCrossRefGoogle Scholar
  19. Hart AJ, Bale JS, Tullett AG, Worland MR, Walters KFA (2002) Effects of temperature on the establishment potential of the predatory mite Amblyseius californicus McGregor (Acari: Phytoseiidae) in the UK. J Insect Physiol 48:593–599CrossRefGoogle Scholar
  20. Helgadóttir F, Toft S, Sigsgaard L (2017) Negative effects of low developmental temperatures on aphid predation by Orius majusculus (Heteroptera: Anthocoridae). Biol Control 114:59–64CrossRefGoogle Scholar
  21. Hodkinson I (2003) Metabolic cold adaptation in arthropods: a smaller-scale perspective. Funct Ecol 17:562–567CrossRefGoogle Scholar
  22. Hoffmann AA, Hallas R, Anderson AR, Telonis-Scott M (2005) Evidence for a robust sex-specific trade-off between cold tolerance and starvation tolerance in Drosophila melanogaster. J Evol Biol 18:804–810CrossRefGoogle Scholar
  23. Hoffmann AA, Sørensen JG, Loeschcke V (2003) Adaptation of Drosophila to temperature extremes: bringing together quantitative and molecular approaches. J Therm Biol 28:175–216CrossRefGoogle Scholar
  24. Jensen K, Kristensen TN, Overgaard J, Toft S, Sørensen JG, Holmstrup M (2017) Cold acclimation reduces predation rate and reproduction but increases cold- and starvation tolerance in the predatory mite Gaeolaelaps aculeifer Canestrini. Biol Control 114:150–157CrossRefGoogle Scholar
  25. Jensen K, Mayntz D, Wang T, Simpson SJ, Overgaard J (2010) Metabolic consequences of feeding and fasting on nutritionally different diets in the wolf spider Pardosa prativaga. J Insect Physiol 56:1095–1100CrossRefGoogle Scholar
  26. Jensen P, Overgaard J, Loeschcke V, Schou MF, Malte H, Kristensen TN (2014) Inbreeding effects on standard metabolic rate investigated at cold, benign and hot temperatures in Drosophila melanogaster. J Insect Physiol 62:11–20CrossRefGoogle Scholar
  27. Johnston IA, Bennett AF (1996) Animals and temperature: phenotypic and evolutionary adaptation. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  28. Kristensen TN, Hoffmann AA, Overgaard J, Sørensen JG, Hallas R, Loeschcke V (2008) Costs and benefits of cold acclimation in field-released Drosophila. Proc Natl Acad Sci U S A 105:216–221CrossRefGoogle Scholar
  29. Kristensen TN, Kjeldal H, Schou MF, Nielsen JL (2016) Proteomic data reveal a physiological basis for costs and benefits associated with thermal acclimation. J Exp Biol 219:969–976CrossRefGoogle Scholar
  30. Lee KP, Jang T (2014) Exploring the nutritional basis of starvation resistance in Drosophila melanogaster. Funct Ecol 28:1144–1155CrossRefGoogle Scholar
  31. Luczynski A, Nyrop J, Shi A (2008) Pattern of female reproductive age classes in mass-reared populations of Phytoseiulus persimilis (Acari: Phytoseiidae) and its influence on population characteristics and quality of predators following cold storage. Biol Control 47:159–166CrossRefGoogle Scholar
  32. Messamah B, Kellermann V, Malte H, Loeschcke V, Overgaard J (2017) Metabolic cold adaptation contributes little to the interspecific variation in metabolic rates of 65 species of Drosophilidae. J Insect Physiol 98:309–316CrossRefGoogle Scholar
  33. Nyamukondiwa C, Terblanche JS (2009) Thermal tolerance in adult Mediterranean and Natal fruit flies (Ceratitis capitata and Ceratitis rosa): effects of age, gender and feeding status. J Therm Biol 34:406–414CrossRefGoogle Scholar
  34. Overgaard J, MacMillan HA (2017) The integrative physiology of insect chill tolerance. Annu Rev Physiol 79:8.1–8.22CrossRefGoogle Scholar
  35. Pijpe J, Brakefield PM, Zwaan BJ (2007) Phenotypic plasticity of starvation resistance in the butterfly Bicyclus anynana. Evol Ecol 21:589–600CrossRefGoogle Scholar
  36. Prosser CL (1955) Physiological variation in animals. Biol Rev 30:229–261CrossRefGoogle Scholar
  37. Scharf I, Wertheimer KO, Xin JL, Gilad T, Goldenberg I, Subach A (2017) Context-dependent effects of cold stress on behavioral, physiological, and life-history traits of the red flour beetle. Insect Sci in press.  https://doi.org/10.1111/1744-7917.12497.
  38. Scharf I, Wexler Y, MacMillan HA, Presman S, Simson E, Rosenstein S (2016) The negative effect of starvation and the positive effect of mild thermal stress on thermal tolerance of the red flour beetle, Tribolium castaneum. Sci Nat 103:20CrossRefGoogle Scholar
  39. Sinclair BJ, Marshall KE (2018) The many roles of fats in overwintering insects. J Exp Biol 221:jeb161836CrossRefGoogle Scholar
  40. Smith CR, Tschinkel WR (2009) Ant fat extraction with a Soxhlet extractor. Cold Spring Harb Protoc 4:832–835Google Scholar
  41. Stamou GP, Asikidis MD, Argyropoulou MD, Iatrou GD (1995) Respiratory responses of oribatid mites to temperature changes. J Insect Physiol 41:229–233CrossRefGoogle Scholar
  42. Sørensen JG, Addison MF, Terblanche JS (2012) Mass-rearing of insects for pest management: challenges, synergies and advances from evolutionary physiology. Crop Prot 38:87–94CrossRefGoogle Scholar
  43. Terblanche JS (2014) Physiological performance of field-released insects. Curr Oppin Insect Sci 4:60–66CrossRefGoogle Scholar
  44. Terblanche JS, Clusella-Trullas S, Deere JA, Van Vuuren BJ, Chown SL (2009) Directional evolution of the slope of the metabolic rate–temperature relationship is correlated with climate. Physiol Biochem Zool 82:495–503CrossRefGoogle Scholar
  45. Vreysen MJB, Robinson AS, Hendrichs J (2007) Area-wide control of insect pests: from research to field implementation. Springer, DortrechtGoogle Scholar
  46. Williams CM, Szejner-Sigal A, Morgan TJ, Edison AS, Allison DB, Hahn DA (2016) Adaptation to low temperature exposure increases metabolic rates independently of growth rates. Integr Comp Biol 56:62–72CrossRefGoogle Scholar
  47. Williams CM, Thomas RH, MacMillan HA, Marshall KE, Sinclair BJ (2011) Triacylglyceride measurement in small quantities of homogenised insect tissue: comparisons and caveats. J Insect Physiol 57:1602–1613CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of Bioscience, Section for Soil Ecology and EcotoxicologyAarhus UniversitySilkeborgDenmark
  2. 2.Department of Bioscience, Section for ZoophysiologyAarhus UniversityAarhus CDenmark
  3. 3.Department of Chemistry and Bioscience, Section for Biology and Environmental ScienceAalborg UniversityAalborg EDenmark

Personalised recommendations