Metabolic Transitions During Feast and Famine in Spiders

Chapter

Abstract

Spiders are a diverse group of invertebrates that successfully inhabit most terrestrial ecosystems. Part of their success can be ascribed to a remarkable feeding ecology that allows spiders to tolerate prolonged periods of starvation and provide the capacity to feed on very large prey. In this chapter, we review the existing knowledge on the physiological transitions in spiders during prolonged fasting and during consumption of (large) meals. We focus on the metabolic transitions between feast and famine as well as the use and uptake of macronutrients and water. Spiders reduce energy consumption during fasting and food deprivation is primarily associated with utilization of lipid stores. Also, despite the continuous catabolism of energy stores spiders defend body mass through a relative increase in body water. Feeding causes huge stimulation of energy consumption, where metabolic rate can increase more than 20-fold. The elevated metabolism persists for hours to days during the postprandial period and digestion is likely to constitute the largest sustained increase in metabolism of spiders. Because spiders use extraoral digestion, it is easy to investigate the energy balance of prey and predator during feeding. We argue, therefore, that spiders represent a promising animal model to study energy flux during feeding and fasting and hope this review will inspire further studies on the feeding physiology and ecology of this interesting animal group.

Keywords

Relative Water Content Food Deprivation Respiratory Exchange Ratio Meal Size Wolf Spider 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgments

We thank Marshall McCue for inviting us to write this review and for his constructive criticism to improve our chapter. We also thank David Mayntz and Peter Skødt Knudsen for helpful comments and suggestions. Finally, we would like to acknowledge the Danish Research Council (FNU) and Strategic Research Council (NOVENIA) for supporting our research.

References

  1. Aitchison C (1984) Low temperature feeding by winter active spiders. J Arachnol 12:297–305Google Scholar
  2. Anderson JF (1970) Metabolic rates of spiders. Comp Biochem Physiol 33:51–72PubMedCrossRefGoogle Scholar
  3. Anderson JF (1974) Responses to Starvation in the spiders Lycosa Lenta (Hentz) and Filistata Hibernalis (Hentz). Ecology 55:576–585CrossRefGoogle Scholar
  4. Bressendorff BB, Toft S (2011) Dome-shaped functional response induced by nutrient imbalance of the prey. Biol Lett 7(517):520Google Scholar
  5. Carrel J, Heathcote R (1976) Heart rate in spiders: influence of body size and foraging energetics. Science 193:148–150PubMedCrossRefGoogle Scholar
  6. Cohen AC (1995) Extra-oral digestion in predaceous terrestrial arthropoda. Ann Rev Ent 40:85–103CrossRefGoogle Scholar
  7. Collatz KG (1987) Structure and function of the digestive tract. In: Nentwig W (ed) Ecophysiology of spiders. Springer, BerlinGoogle Scholar
  8. Collatz K-G, Mommsen T (1975) Veränderung der körperzusammensetzung und der stoffwechselintensität der spinne Tegenaria atrica (C.L. Koch) (Agelenidae) nach kurzem und langem hunger. J Comp Physiol B 98:205–212CrossRefGoogle Scholar
  9. Foelix R (1996) Biology of spiders, 2nd edn. Oxford University Press, New YorkGoogle Scholar
  10. Ford MJ (1977) Metabolic costs of the predation strategy of the spider Pardosa amentata (Clerck) (Lycosidae). Oecologia 28:333–340CrossRefGoogle Scholar
  11. Furrer S, Ward PI (1995) Differential nutrient extraction in the funnel web spider Agelena labyrinthica. Physiol Entomol 20:18–22CrossRefGoogle Scholar
  12. Greenstone MH, Bennett AF (1980) Foraging strategy and metabolic rate in spiders. Ecology 61:1255–1259CrossRefGoogle Scholar
  13. Guppy M, Withers P (1999) Metabolic depression in animals: physiological perspectives and biochemical generalizations. Biol Rev 74:1–40PubMedCrossRefGoogle Scholar
  14. 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 56:1095–1100PubMedCrossRefGoogle Scholar
  15. Jensen K, Mayntz D, Toft S, Raubenheimer D, Simpson SJ (2011) Prey nutrient composition has different effects on Pardosa wolf spiders with dissimilar life histories. Oecologia 165:577–583PubMedCrossRefGoogle Scholar
  16. Knudsen PS (2011) Feeding following short- and long-term food deprivation in the giant white-knee tarantula Acanthoscurria geniculata. Masters thesis, Aarhus UniversityGoogle Scholar
  17. Korenko S, Pekár S (2010) Is there intraguild predation between winter-active spiders (Araneae) on apple tree bark? Biol Control 54:206–212CrossRefGoogle Scholar
  18. Laino A, Cunningham ML, García F, Heras H (2009) First insight into the lipid uptake, storage and mobilization in arachnids: role of midgut diverticula and lipoproteins. J Insect Physiol 55:1118–1124PubMedCrossRefGoogle Scholar
  19. Laino A, Cunningham ML, Heras H, Garcia F (2011) In vitro lipid transfer between lipoproteins and midgut-diverticula in the spider Polybetes pythagoricus. Comp Biochem Physiol B 160:181–186PubMedCrossRefGoogle Scholar
  20. Lang A, Klarenberg AJ (1997) Experiments on the foraging behaviour of the hunting spider Pisaura mirabilis (Araneae: Pisauridae): utilization of single prey items. Eur J Entomol 94:453–459Google Scholar
  21. Lauridsen H, Hansen K, Wang T, Agger P, Andersen JL, Knudsen PS, Rasmussen AS, Uhrenholt L, Pedersen M (2011) Inside out: modern imaging techniques to reveal animal anatomy. PLoS ONE 6:e17879. doi: 10.1371/journal.pone.0017879 PubMedCrossRefGoogle Scholar
  22. Lease HM, Wolf BO (2011) Lipid content of terrestrial arthropods in relation to body size, phylogeny, ontogeny and sex. Physiol Entomol 36:29–38CrossRefGoogle Scholar
  23. Lighton JRB, Fielden JL (1995) Mass scaling of standard metabolism in ticks—a valid case of low metabolic rates in sit-and-wait strategists. Physiol Zool 68:43–62Google Scholar
  24. Mayntz D, Toft S, Vollrath F (2003) Effects of prey quality and availability on the life history of a trap-building predator. Oikos 101:631–638CrossRefGoogle Scholar
  25. Mayntz D, Raubenheimer D, Salomon M, Toft S, Simpson SJ (2005) Nutrient-specific foraging in invertebrate predators. Science 307:111–113PubMedCrossRefGoogle Scholar
  26. McCormick S, Polis GA (1982) Arthropods that prey on vertebrates. Biol Rev 57:29–58CrossRefGoogle Scholar
  27. McCue (2004) General effects of temperature on animal biology. In: Valenzuela N, Lance VA (eds) Temperature dependent sex determination. Smithsonian Books, Washington, DC, pp 71–78Google Scholar
  28. McCue MD (2006) Specific dynamic action: a century of investigation. Comp Biochem Physiol A 144:381–394CrossRefGoogle Scholar
  29. McCue MD (2010) Starvation physiology: reviewing the different strategies animals use to survive a common challenge. Comp Biochem Physiol A 156:1–18Google Scholar
  30. Mommsen TP (1978a) Digestive enzymes of a spider (Tegenaria atrica Koch) I. General remarks, digestion of proteins. Comp Biochem Physiol A 60:365–370CrossRefGoogle Scholar
  31. Mommsen TP (1978b) Digestive enzymes of a spider (Tegenaria atrica Koch) II. Carbohydrases. Comp Biochem Physiol A 60:371–375CrossRefGoogle Scholar
  32. Mommsen TP (1978c) Digestive enzymes of a spider (Tegenaria atrica Koch) III. esterases, phosphatases, nucleases. Comp Biochem Physiol A 60:377–382CrossRefGoogle Scholar
  33. Nakamura K (1987) Hunger and starvation. In: Nentwig W (ed) Ecophysiology of spiders. Springer, BerlinGoogle Scholar
  34. Nentwig W (1987) The prey of spiders. In: Nentwig W (ed) Ecophysiology of spiders. Springer, BerlinGoogle Scholar
  35. Nespolo RF, Correa L, Perez-Apablaza CX, Cortes P, Bartheld JL (2011) Energy metabolism and the postprandial response of the Chilean tarantulas, Euathlus truculentus (Araneae: Theraphosidae). Comp Biochem Physiol A 159:379–382CrossRefGoogle Scholar
  36. Samu F, Biro Z (1993) Functional-response, multiple feeding and wasteful killing in a wolf spider (Araneae, Lycosidae). Eur J Entomol 90:471–476Google Scholar
  37. Sandidge JS (2003) Arachnology: scavenging by brown recluse spiders. Nature 426:30PubMedCrossRefGoogle Scholar
  38. Schmidt-Nielsen K (1984) Scaling: why is animal size so important?, 1st edn. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  39. Schmitz A (2004) Metabolic rates during rest and activity in differently tracheated spiders (Arachnida, Araneae): Pardosa lugubris (Lycosidae) and Marpissa muscosa (Salticidae). J Comp Physiol B 174:519–526PubMedGoogle Scholar
  40. Schmitz A (2005) Spiders on a treadmill: influence of running activity on metabolic rates in Pardosa lugubris (Araneae, Lycosidae) and Marpissa muscosa (Araneae, Salticidae). J Exp Biol 208:1401–1411PubMedCrossRefGoogle Scholar
  41. Secor SM (2008) Specific dynamic action: a review of the postprandial metabolic response. J Comp Physiol B 179:1–56PubMedCrossRefGoogle Scholar
  42. Seymour RS, Vinegar A (1973) Thermal relations, water loss and oxygen consumption of a North American tarantula. Comp Biochem Physiol A 44:83–96CrossRefGoogle Scholar
  43. Shillington C (2005) Inter-sexual differences in resting metabolic rates in the Texas tarantula, Aphonopelma anax. Comp Biochem Physiol A 142:439–445CrossRefGoogle Scholar
  44. Smith RB, Mommsen TP (1984) Pollen feeding in an orb-weaving spider. Science 226:1330–1332PubMedCrossRefGoogle Scholar
  45. Stewart DM, Martin AW (1970) Blood and fluid balance of the common tarantula, Dugesiella hentzi. Z Vergl Physiol 70:223–246CrossRefGoogle Scholar
  46. Tanaka K, Itô T (1982) Decrease in respiratory rate in a wolf spider, Pardosa astrigera (L. Koch), under starvation. Res Popul Ecol 24:360–374CrossRefGoogle Scholar
  47. Tanaka K, Itô Y, Saito T (1985) Reduced respiratory quotient by starvation in a wolf spider, Pardosa astrigera (L. Koch). Comp Biochem Physiol A 80:415–418CrossRefGoogle Scholar
  48. Toft S (1999) Prey choice and spider fitness. J Arachnol 27:301–307Google Scholar
  49. Turnbull AL (1973) Ecology of the true spiders (Araneomorphae). Ann Rev Entomol 18:305–348CrossRefGoogle Scholar
  50. Vetter RS (2011) Scavenging by spiders (Araneae) and its relationship to pest management of the brown recluse spider. J Econ Entomol 104:986–989PubMedCrossRefGoogle Scholar
  51. Wang T, Busk M, Overgaard J (2001) The respiratory consequences of feeding in amphibians and reptiles. Comp Biochem Physiol A 128:533–547CrossRefGoogle Scholar
  52. Wang T, Hung CCY, Randall DJ (2006) The comparative physiology of food deprivation: from feast to famine. Ann Rev Physiol 68:223–251CrossRefGoogle Scholar
  53. Wilder SM (2011) Spider nutrition: an integrative perspective. Adv Insect Physiol 40:87–136CrossRefGoogle Scholar
  54. Wise DH (1995) Spiders in ecological webs. Cambridge University Press, CambridgeGoogle Scholar
  55. Wu L, Yun Y, Li J, Chen J, Zhang H, Peng Y (2011) Preference for feeding on honey solution and its effect on survival, development, and fecundity of Ebrechtella tricuspidata. Entomol Exp Appl 140:52–58CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2012

Authors and Affiliations

  1. 1.Zoophysiology, Institute of BioscienceAarhus UniversityAarhusDenmark

Personalised recommendations