Behavioral Ecology and Sociobiology

, Volume 70, Issue 11, pp 1941–1947 | Cite as

Adult bacterial exposure increases behavioral variation and drives higher repeatability in field crickets

  • Nicholas DiRienzo
  • Petri T. Niemelä
  • Ann V. Hedrick
  • Raine Kortet
Original Article


Among-individual differences in behavior are now a widely studied research focus within the field of behavioral ecology. Furthermore, elements of an animal’s internal state, such as energy or fat reserves, and infection status can have large impacts on behaviors. Despite this, we still know little regarding how state may affect the expression of behavioral variation. Recent exposure to pathogens may have a particularly large impact on behavioral expression given that it likely activates costly immune pathways, potentially forcing organisms to make behavioral tradeoffs. In this study, we investigate how recent exposure to a common bacterial pathogen, Serratia marcescens, affects both the mean behavioral expression and the among-individual differences (i.e., variation) in boldness behavior in the field cricket, Gryllus integer. We find that recent pathogen exposure does not affect mean behavioral expression of the treatment groups, but instead affects behavioral variation and repeatability. Specifically, bacterial exposure drove large among-individual variation, resulting in high levels of repeatability in some aspects of boldness (willingness to emerge into a novel environment), but not others (latency to become active in novel environment), compared to non-infected crickets. Interestingly, sham injection resulted in a universal lack of among-individual differences. Our results highlight the sensitivity of among-individual variance and repeatability estimates to ecological and environmental factors that individuals face throughout their lives.

Significance statement

Animals are known to express consistent among-individual differences in behavior, also known as animal personalities, such that some individuals are always more bold, aggressive, or active relative to others. Yet it is relatively unknown how factors such as energy reserves and exposure to pathogens impact these differences in behavior. Here we investigated how exposure to a pathogenic bacteria as adults affects both the mean behavioral expression and the among-individual differences. Our results show that pathogen exposure results in large levels of among-individual differences in some aspects of boldness behavior (willingness to expose oneself to risk), but not others (latency to become active in a novel environment). These results highlight the sensitivity of behavioral differences to elements of state, such as infection status.


Animal personality Boldness Gryllus Field cricket Immune function Repeatability 



We thank the University of Oulu and UEF for hosting ND while conducting this research. We also thank the National Science Foundation Nordic Research Opportunity, the Orthopterists’ Society Theodore J. Cohn Research Fund, the Emil Aaltonen foundation, Academy of Finland (project 127398), and Tekes: The Finnish Funding Agency for Innovation for their support in this project. ND was supported by an NSF Graduate Research Fellowship. RK and PTN were supported by the Academy of Finland. We also thank Jouni Laakso and Lauri Mikonranta for providing the bacterial culture of Serratia marcescens used in this experiment.

Supplementary material

265_2016_2200_MOESM1_ESM.docx (14 kb)
ESM 1 (DOCX 14 kb)


  1. Adamo S (1998) The specificity of behavioral fever in the cricket Acheta domesticus. J Parasitol:529–533Google Scholar
  2. Adamo SA (2004) Estimating disease resistance in insects: phenoloxidase and lysozyme-like activity and disease resistance in the cricket Gryllus texensis. J Insect Physiol 50:209–216CrossRefPubMedGoogle Scholar
  3. Adamo SA, Kovalko I, Easy RH, Stoltz D (2014) A viral aphrodisiac in the cricket Gryllus texensis. J Exp Biol 217:1970–1976CrossRefPubMedGoogle Scholar
  4. Ahtiainen JJ, Alatalo RV, Kortet R, Rantala MJ (2006) Immune function, dominance and mating success in drumming male wolf spiders Hygrolycosa rubrofasciata. Behav Ecol Sociobiol 60:826–832CrossRefGoogle Scholar
  5. Ardia DR, Gantz JE, Brent C, Strebel S (2012) Costs of immunity in insects: an induced immune response increases metabolic rate and decreases antimicrobial activity. Funct Ecol 26:732–739CrossRefGoogle Scholar
  6. Bates D, Maechler M, Bolker B, Walker S (2013) lme4: linear mixed-effects models using Eigen and S4. R package version 1Google Scholar
  7. Briffa M, Weiss A (2010) Animal personality. Curr Biol 20:R912–R914CrossRefPubMedGoogle Scholar
  8. Briscoe AD, Chittka L (2001) The evolution of color vision in insects. Annu Rev Entomol 46:471–510CrossRefPubMedGoogle Scholar
  9. Butler MW, Toomey MB, McGraw KJ, Rowe M (2012) Ontogenetic immune challenges shape adult personality in mallard ducks. Proc R Soc Lond B 279:326–333CrossRefGoogle Scholar
  10. Carter AJ, Feeney WE, Marshall HH, Cowlishaw G, Heinsohn R (2013) Animal personality: what are behavioural ecologists measuring? Biol Rev 88:465–475CrossRefPubMedGoogle Scholar
  11. Coats J, Poulin R, Nakagawa S (2010) The consequences of parasitic infections for host behavioural correlations and repeatability. Behaviour 147:367–382CrossRefGoogle Scholar
  12. David M, Auclair Y, Giraldeau LA, Cézilly F (2012) Personality and body condition have additive effects on motivation to feed in zebra finches Taeniopygia guttata. Ibis 154:372–378CrossRefGoogle Scholar
  13. Dingemanse NJ, Dochtermann NA (2013) Quantifying individual variation in behaviour: mixed-effect modelling approaches. J Anim Ecol 82:39–54CrossRefPubMedGoogle Scholar
  14. DiRienzo N, Montiglio PO (2016) The contribution of developmental experience vs. condition to life history, trait variation and individual differences. J Anim Ecol 85(4):915–926Google Scholar
  15. DiRienzo N, Niemelä PT, Skog A, Vainikka A, Kortet R (2015) Juvenile pathogen exposure affects the presence of personality in adult field crickets. Front Ecol Evol 3:36Google Scholar
  16. DiRienzo N, Pruitt JN, Hedrick AV (2012) Juvenile exposure to acoustic sexual signals from conspecifics alters growth trajectory and an adult personality trait. Anim Behav 84:861–868CrossRefGoogle Scholar
  17. DiRienzo N, Pruitt JN, Hedrick AV (2013) The combined behavioural tendencies of predator and prey mediate the outcome of their interaction. Anim Behav 86:317–322CrossRefGoogle Scholar
  18. Fisher DN, David M, Tregenza, Tom, Rodríguez-Muñoz R (2015) Dynamics of among-individual behavioral variation over adult lifespan in a wild insect. Behav Ecol 26(4):975–985Google Scholar
  19. Freeman-Gallant CR, Taff CC, Morin DF, Dunn PO, Whittingham LA, Tsang SM (2010) Sexual selection, multiple male ornaments, and age-and condition-dependent signaling in the common yellowthroat. Evolution 64:1007–1017CrossRefPubMedGoogle Scholar
  20. Grimont PA, Grimont F (1978) The genus Serratia. Annu Rev Microbiol 32:221–248CrossRefPubMedGoogle Scholar
  21. Groothuis TG, Trillmich F (2011) Unfolding personalities: the importance of studying ontogeny. Dev Psychobiol 53:641–655CrossRefPubMedGoogle Scholar
  22. Hedrick AV (2000) Crickets with extravagant mating songs compensate for predation risk with extra caution. Proc R Soc Lond B 267:671–675CrossRefGoogle Scholar
  23. Hedrick AV, Kortet R (2006) Hiding behaviour in two cricket populations that differ in predation pressure. Anim Behav 72:1111–1118CrossRefGoogle Scholar
  24. Holzer B, Jacot A, Brinkhof MW (2003) Condition-dependent signaling affects male sexual attractiveness in field crickets, Gryllus campestris. Behav Ecol 14:353–359CrossRefGoogle Scholar
  25. Horváth G, Martín J, López P, Garamszegi LZ, Bertók P, Herczeg G (2016) Blood parasite infection intensity covaries with risk-taking personality in male carpetan rock lizards (Iberolacerta cyreni). EthologyGoogle Scholar
  26. Janssens L, Stoks R (2014) Reinforcing effects of non-pathogenic bacteria and predation risk: from physiology to life history. Oecologia 176:323–332CrossRefPubMedGoogle Scholar
  27. Kekäläinen J, Lai Y-T, Vainikka A, Sirkka I, Kortet R (2014) Do brain parasites alter host personality?—experimental study in minnows. Behav Ecol Sociobiol 68:197–204CrossRefGoogle Scholar
  28. Kortet R, Hedrick A (2007) A behavioural syndrome in the field cricket Gryllus integer: intrasexual aggression is correlated with activity in a novel environment. Biol J Linn Soc 91:475–482CrossRefGoogle Scholar
  29. Kortet R, Hedrick AV, Vainikka A (2010) Parasitism, predation and the evolution of animal personalities. Ecol Lett 13:1449–1458CrossRefPubMedGoogle Scholar
  30. Kortet R, Rantala MJ, Hedrick A (2007) Boldness in anti-predator behaviour and immune defence in field crickets. Evol Ecol Res 9:185–197Google Scholar
  31. Kortet R, Niemelä PT, Vainikka A, Laakso J (2012). Females prefer bold males; an analysis of boldness, mate choice, and bacterial resistance in the field cricket Gryllus integer. Ecological Parasitology and Immunology 1:1–6Google Scholar
  32. Kotiaho JS (2000) Testing the assumptions of conditional handicap theory: costs and condition dependence of a sexually selected trait. Behav Ecol Sociobiol 48:188–194CrossRefGoogle Scholar
  33. Liedtke J, Redekop D, Schneider JM, Schuett W (2015) Early environmental conditions shape personality types in a jumping spider. Front Ecol Evol 3:134CrossRefGoogle Scholar
  34. Louis C, Jourdan M, Cabanac M (1986) Behavioral fever and therapy in a rickettsia-infected Orthoptera. Am J Physiol-Reg I 250:R991–R995Google Scholar
  35. Luttbeg B, Sih A (2010) Risk, resources and state-dependent adaptive behavioural syndromes. Philos T R Soc B 365:3977–3990CrossRefGoogle Scholar
  36. Mappes J, Alatalo RV, Kotiaho J, Parri S (1996) Viability costs of condition-dependent sexual male display in a drumming wolf spider. Proc R Soc B 263:785–789CrossRefGoogle Scholar
  37. Márkus R, Kurucz É, Rus F, Andó I (2005) Sterile wounding is a minimal and sufficient trigger for a cellular immune response in Drosophila melanogaster. Immunol Lett 101:108–111CrossRefPubMedGoogle Scholar
  38. Martin JG, Réale D (2008) Temperament, risk assessment and habituation to novelty in eastern chipmunks, Tamias striatus. Anim Behav 75:309–318CrossRefGoogle Scholar
  39. McElreath R, Luttbeg B, Fogarty SP, Brodin T, Sih A (2007) Evolution of animal personalities. Nature 450:E5–E5CrossRefPubMedGoogle Scholar
  40. Nakagawa S, Schielzeth H (2010) Repeatability for Gaussian and non-Gaussian data: a practical guide for biologists. Biol Rev 85:935–956PubMedGoogle Scholar
  41. Niemelä PT, Vainikka A, Hedrick AV, Kortet R (2012b) Integrating behaviour with life history: boldness of the field cricket, Gryllus integer, during ontogeny. Funct Ecol 26(2):450–456Google Scholar
  42. Niemelä PT, Vainikka A, Lahdenperä S, Kortet R (2012c) Nymphal density, behavioral development, and life history in a field cricket. Behav Ecol Sociobiol 66:645–652CrossRefGoogle Scholar
  43. Niemelä PT, DiRienzo N, Hedrick AV (2012a) Predator-induced changes in the boldness of naïve field crickets, Gryllus integer, depends on behavioural type. Anim Behav 84:129–135CrossRefGoogle Scholar
  44. Niemelä PT, Lattenkamp EZ, Dingemanse NJ (2015) Personality-related survival and sampling bias in wild cricket nymphs. Behav Ecol 26:936–946CrossRefGoogle Scholar
  45. Pinheiro JC, Bates DM (2000) Linear mixed-effects models: basic concepts and examples. Mixed-Effects Models in S and S-Plus:3–56Google Scholar
  46. Poulin R (2010) Parasite manipulation of host behavior: an update and frequently asked questions. Adv Stud Behav 41:151–186CrossRefGoogle Scholar
  47. R Core Team (2014) R: A language and environment for statistical computing. The R Foundation for Statistical Computing, Vienna, Austria. Available online at
  48. Rantala M, Roff D (2005) An analysis of trade-offs in immune function, body size and development time in the Mediterranean field cricket, Gryllus bimaculatus. Funct Ecol 19:323–330CrossRefGoogle Scholar
  49. Rantala MJ, Kortet R (2003) Courtship song and immune function in the field cricket Gryllus bimaculatus. Biol J Linn Soc 79(3):503–510Google Scholar
  50. Rantala MJ, Kortet R (2004) Male dominance and immunocompetence in a field cricket. Behav Ecol 15:187–191CrossRefGoogle Scholar
  51. Réale D, Reader SM, Sol D, McDougall PT, Dingemanse NJ (2007) Integrating animal temperament within ecology and evolution. Biol Rev 82:291–318CrossRefPubMedGoogle Scholar
  52. Rigby MC, Jokela J (2000) Predator avoidance and immune defence: costs and trade-offs in snails. Proc R Soc Lond B 267:171–176CrossRefGoogle Scholar
  53. Seaman B, Briffa M (2015) Parasites and personality in periwinkles (Littorina littorea): infection status is associated with mean-level boldness but not repeatability. Behav Process 115:132–134CrossRefGoogle Scholar
  54. Sih A, Cote J, Evans M, Fogarty S, Pruitt J (2012) Ecological implications of behavioural syndromes. Ecol Lett 15:278–289CrossRefPubMedGoogle Scholar
  55. Sinn DL, Gosling SD, Moltschaniwskyj NA (2008) Development of shy/bold behaviour in squid: context-specific phenotypes associated with developmental plasticity. Anim Behav 75:433–442CrossRefGoogle Scholar
  56. West-Eberhard MJ (2003) Developmental plasticity and evolution. Oxford University PressGoogle Scholar
  57. Westneat DF, Hatch MI, Wetzel DP, Ensminger AL (2011) Individual variation in parental care reaction norms: integration of personality and plasticity. Am Nat 178:652–667CrossRefPubMedGoogle Scholar
  58. Wolf M, Weissing FJ (2012) Animal personalities: consequences for ecology and evolution. Trends Ecol Evol 27:452–461CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  • Nicholas DiRienzo
    • 1
    • 2
  • Petri T. Niemelä
    • 3
  • Ann V. Hedrick
    • 2
  • Raine Kortet
    • 4
    • 5
  1. 1.Department of Ecology and Evolutionary BiologyUniversity of ArizonaTucsonUSA
  2. 2.Department of Neurobiology Physiology and BehaviorUniversity of California—DavisDavisUSA
  3. 3.Department Biology IILudwig-Maximilians University of MunichPlanegg-MartinsriedGermany
  4. 4.Department of Environmental and Biological SciencesUniversity of Eastern FinlandJoensuuFinland
  5. 5.Department of Biology, Biological and Geological SciencesUniversity of Western OntarioLondonCanada

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