Current parasite resistance trades off with future defenses and flight performance

  • Collin J. HornEmail author
  • Lien T. Luong
Original Article


Many animals use behavioral defenses such as grooming to avoid or mitigate the negative effects of infection by ectoparasites. Grooming can be energetically costly and may trade off with other host activities. We hypothesize that self-grooming comes at a cost and, therefore, compromises future parasite resistance and other energetically expensive activities, namely flight. We measured the rates of CO2 production (respiration is a proxy for energetic costs) in Drosophila nigrospiracula induced to groom with a non-pathogenic irritant (volcanic ash), allowing us to disentangle the cost of grooming from the cost of infection. The respiration rate of flies induced to groom was significantly higher compared to flies at rest. Results show that flies that spent time grooming, induced by an irritant, had higher average infection intensities upon subsequent exposure to the ectoparasitic mite Macrocheles subbadius. Additionally, flies induced to groom with an irritant suffered a ~ 30% reduction in flight performance compared to flies previously at rest, suggesting reduced ability to escape infested habitats. Lastly, we compared the behavioral response of flies to ectoparasites and irritants, as flies may be specific in their response to different types of threats. Behavioral observations revealed that flies exposed to an irritant increased self-grooming behavior and decreased movement (potentially suggesting reduced escape behavior), whereas flies exposed to mites exhibited increased ambulatory movement as well as increased grooming behavior. Overall, time spent grooming made flies more vulnerable to future infection and decreased flight endurance, a metric of dispersal capability.

Significance statement

Behavioral defenses are a major method by which animals defend themselves against ectoparasites. However, these defenses, such as rapid movement and intensive grooming, are often energetically costly. This study measures the energetic cost of grooming in Drosophila nigrospiracula and the knock-on effects on future parasite resistance and flight endurance. We measured the energetic cost of grooming using respirometry and observed that flies induced to groom with a non-pathogenic irritant were less able to defend themselves against future mite attack and had reduced flight endurance, likely due to energetic trade-offs. Our results suggest grooming reduces energy available for other energetically demanding activities. As dispersal can limit the long-term impacts of parasites, these trade-offs may indicate a broader trade-off between current and future parasite defense.


Bioenergetics Drosophila Macrocheles Parasitism Parasite resistance Grooming behavior Host behavior Respiration rate 



LTL is funded by an NSERC Discovery Grant (#435245). Organisms came from cultures maintained by T. Brophy and M. Elahi. Volcanic ash was donated by C. Mierzejewski.


  1. Auld S, Penczykowski RM, Ochs JH, Grippi DC, Hall SR, Duffy MA (2013) Variation in costs of parasite resistance among natural host populations. J Evol Biol 26:2479–2486CrossRefGoogle Scholar
  2. Barradale F, Sinha K, Lebestky T (2017) Quantification of Drosophila grooming behavior. Jove-J of Vis ExpGoogle Scholar
  3. Beenakke AM (1969) Carbohydrate and fat as a fuel for insect flight. A comparative study. J Insect Physiol 15:353–361CrossRefGoogle Scholar
  4. Boots M, Haraguchi Y (1999) The evolution of costly resistance in host-parasite systems. Am Nat 153:359–370PubMedGoogle Scholar
  5. Boroczky K, Wada-Katsumataa A, Batchelor D, Zhukovskaya M, Schal C (2013) Insects groom their antennae to enhance olfactory acuity. P Natl Acad Sci USA 110:3615–3620CrossRefGoogle Scholar
  6. Bradley CA, Altizer S (2005) Parasites hinder monarch butterfly flight: implications for disease spread in migratory hosts. Ecol Lett 8:290–300CrossRefGoogle Scholar
  7. Campbell EO, Luong LT (2016) Mite choice generates sex- and size-biased infection in Drosophila hydei. Parasitology 143:787–793CrossRefGoogle Scholar
  8. de la Flor M, Chen LJ, Manson-Bishop C, Chu TC, Zamora K, Robbins D, Gunaratne G, Roman G (2017) Drosophila increase exploration after visually detecting predators. PLoS One 12:e0180749CrossRefGoogle Scholar
  9. Eilam D (2005) Die hard: a blend of freezing and fleeing as a dynamic defense - implications for the control of defensive behavior. Neurosci and Biobehav Rev 29:1181–1191CrossRefGoogle Scholar
  10. Garrido M, Adler VH, Pnini M, Abramsky Z, Krasnov BR, Gutman R, Kronfeld-Schor N, Hawlena H (2016) Time budget, oxygen consumption and body mass responses to parasites in juvenile and adult wild rodents. Parasite Vector 9:120CrossRefGoogle Scholar
  11. Geraldi NR, Macreadie PI (2013) Restricting prey dispersal can overestimate the importance of predation in trophic cascades. PLoS One 8:1–9CrossRefGoogle Scholar
  12. Giorgi MS, Arlettaz R, Christe P, Vogel P (2001) The energetic grooming costs imposed by a parasitic mite (Spinturnix myoti) upon its bat host (Myotis myotis). P Roy Soc B-Biol Sci 268:2071–2075CrossRefGoogle Scholar
  13. Hawlena H, Bashary D, Abramsky Z, Krasnov BR (2007) Benefits, costs and constraints of anti-parasitic grooming in adult and juvenile rodents. Ethology 113:394–402CrossRefGoogle Scholar
  14. Hicks O, Burthe SJ, Daunt F, Newell M, Butler A, Ito M, Sato K, Green JA (2018) The energetic cost of parasitism in a wild population. P Roy Soc B-Biol Sci 285:8CrossRefGoogle Scholar
  15. Horn CJ, Luong LT (2018) Proximity to parasites reduces host fitness independent of infection in a Drosophila-Macrocheles system. Parasitology 145:1564–1569 1–6CrossRefGoogle Scholar
  16. Horn CJ, Mierzejewski MK, Luong LT (2018) Host respiration rate and injury-derived cues drive host preference by an ectoparasite of fruit flies. Physiol Biochem Zool 91:896–903CrossRefGoogle Scholar
  17. James WR, McClintock JB (2017) Anti-predator responses of amphipods are more effective in the presence of conspecific chemical cues. Hydrobiologia 797:277–288CrossRefGoogle Scholar
  18. Johnston JS, Heed WB (1976) Dispersal of desert-adapted Drosophila: the Saguaro-breeding D. nigrospiracula. Am Nat 110:629–651CrossRefGoogle Scholar
  19. Klemme I, Karvonen A (2017) Vertebrate defense against parasites: interactions between avoidance, resistance, and tolerance. Ecol Evol 7:561–571CrossRefGoogle Scholar
  20. Lefevre T, de Roode JC, Kacsoh BZ, Schlenke TA (2012) Defence strategies against a parasitoid wasp in Drosophila: fight or flight? Biol Lett 8:230–233CrossRefGoogle Scholar
  21. Li JF, Zhang W, Guo ZH, Wu S, Jan LY, Jan YN (2016) A defensive kicking behavior in response to mechanical stimuli mediated by Drosophila wing margin bristles. J Neurosci 36:11275–11282CrossRefGoogle Scholar
  22. Lighton JRB (2008) Measuring metabolic rates: a manual for scientists. Oxford University Press, New York, USACrossRefGoogle Scholar
  23. Luong LT, Brophy T, Stolz E, Chan SJ (2017a) State-dependent parasitism by a facultative parasite of fruit flies. Parasitology 144:1468–1475CrossRefGoogle Scholar
  24. Luong LT, Heath BD, Polak M (2007) Host inbreeding increases susceptibility to ectoparasitism. J Evol Biol 20:79–86CrossRefGoogle Scholar
  25. Luong LT, Horn CJ, Brophy T (2017b) Mitey costly: energetic costs of parasite avoidance and infection. Physiol Biochem Zool 90:471–477CrossRefGoogle Scholar
  26. Luong LT, Penoni LR, Horn CJ, Polak M (2015) Physical and physiological costs of ectoparasitic mites on host flight endurance. Ecol Entomol 40:518–524CrossRefGoogle Scholar
  27. Luong LT, Polak M (2007) Costs of resistance in the Drosophila-macrocheles system: a negative genetic correlation between ectoparasite resistance and reproduction. Evolution 61:1391–1402CrossRefGoogle Scholar
  28. Markow TA (1988) Reproductive behavior of Drosophila melanogaster and Drosophila nigrospiracula in the field and in the laboratory. J Comp Psychol 102:169–173CrossRefGoogle Scholar
  29. Niven JE, Scharlemann JPW (2005) Do insect metabolic rates at rest and during flight scale with body mass? Biol Lett 1:346–349CrossRefGoogle Scholar
  30. Nolan MP, Delaplane KS (2017) Parasite dispersal risk tolerance is mediated by its reproductive value. Anim Behav 132:247–252CrossRefGoogle Scholar
  31. Peckarsky B, Cowan C, Penton M, Anderson C (1993) Sublethal consequences of stream-dwelling predatory stoneflies on mayfly growth and fecundity. Ecology 74:1836–1846CrossRefGoogle Scholar
  32. Pfeiler E, Ngo NM, Markow TA (2005) Linking behavioral ecology with population genetics: insights from Drosophila nigrospiracula. Hereditas 142:1–6CrossRefGoogle Scholar
  33. Polak M (1996) Ectoparasitic effects on host survival and reproduction: the Drosophila-Macrocheles association. Ecology 77:1379–1389CrossRefGoogle Scholar
  34. Polak M (2003) Heritability of resistance against ectoparasitism in the Drosophila-Macrocheles system. J Evol Biol 16:74–82CrossRefGoogle Scholar
  35. Polak M, Markow TA (1995) Effect of ectoparasitic mites on sexual selection in a sonoran desert fruit-fly. Evolution 49:660–669CrossRefGoogle Scholar
  36. Poulin R (2007) Are there general laws in parasite ecology? Parasitology 134:763–776CrossRefGoogle Scholar
  37. Poulin R, Morand S (2000) The diversity of parasites. Q Rev Biol 75:277–293CrossRefGoogle Scholar
  38. R Studio Team (2015) R Studio: integrated development for R. RStudio, Inc, Boston, MAGoogle Scholar
  39. Raeymaekers JAM, Hablutzel PI, Gregoir AF, Bamps J, Roose AK, Vanhove MPM, Van Steenberge M, Pariselle A, Huyse T, Snoeks J, Volckaert FAM (2013) Contrasting parasite communities among allopatric colour morphs of the Lake Tanganyika cichlid Tropheus. BMC Evol Biol 13:41CrossRefGoogle Scholar
  40. Raffel TR, Martin LB, Rohr JR (2008) Parasites as predators: unifying natural enemy ecology. Trends Ecol Evol 23:610–618CrossRefGoogle Scholar
  41. Rigby MC, Hechinger RF, Stevens L (2002) Why should parasite resistance be costly? Trends Parasitol 18:116–120CrossRefGoogle Scholar
  42. Robar N, Burness G, Murray DL (2010) Tropics, trophics and taxonomy: the determinants of parasite-associated host mortality. Oikos 119:1273–1280CrossRefGoogle Scholar
  43. Robar N, Murray DL, Burness G (2011) Effects of parasites on host energy expenditure: the resting metabolic rate stalemate. Can J Zool 89:1146–1155CrossRefGoogle Scholar
  44. Rohr JR, Swan A, Raffel TR, Hudson PJ (2009) Parasites, info-disruption, and the ecology of fear. Oecologia 159:447–454CrossRefGoogle Scholar
  45. Schulenburg H, Kurtz J, Moret Y, Siva-Jothy MT (2009) Introduction ecological immunology. Philos T Roy Soc B 364:3–14CrossRefGoogle Scholar
  46. Sheldon BC, Verhulst S (1996) Ecological immunology: costly parasite defences and trade-offs in evolutionary ecology. Trends Ecol Evol 11:317–321CrossRefGoogle Scholar
  47. Thornhill R, Fincher CL (2013) The parasite-driven-wedge model of parapatric speciation. J Zool 291:23–33CrossRefGoogle Scholar
  48. Tollrian R, Duggen S, Weiss LC, Laforsch C, Kopp M (2015) Density-dependent adjustment of inducible defenses. Sci Rep-UK 5:12736CrossRefGoogle Scholar
  49. Yanagawa A, Guigue AMA, Marion-Poll F (2014) Hygienic grooming is induced by contact chemicals in Drosophila melanogaster. Front Behav Neurosci 8:254CrossRefGoogle Scholar
  50. Yanagawa A, Neyen C, Lemaitre B, Marion-Poll F (2017) The gram-negative sensing receptor PGRP-LC contributes to grooming induction in Drosophila. PLoS One 12:e0185370CrossRefGoogle Scholar
  51. Zhukovskaya M, Yanagawa A, Forschler BT (2013) Grooming behavior as a mechanism of insect disease defense. Insects 4:609–630CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Department of Biological SciencesUniversity of AlbertaEdmontonCanada

Personalised recommendations