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Behavioral repeatability of flour beetles before and after metamorphosis and throughout aging

Behavioral Ecology and Sociobiology volume 70, pages 745–753 (2016)Cite this article

Abstract

Behavioral repeatability is an important trait relevant to personality research and to behavioral ecology in general. We examined here the behavioral repeatability of two activity-related traits: movement and edge preference (proportion of time spent next to the test arena edge). We used the red flour beetle as our test species in order to determine whether repeatability changes throughout metamorphosis and aging and whether there are inter-sexual differences. Young adults moved more than larvae, but movement activity generally declined with age. Behavioral repeatability was high between two successive measurements for larvae and young adults, but did not persist through metamorphosis. These findings support most of the previous studies on insects and probably reflect the occurrence of phenotypic reorganization during metamorphosis. Neither of our predictions of an increase in behavioral repeatability throughout aging and of a higher repeatability of young adults than larvae held true, as repeatability levels estimates remained similar across ontogeny and aging. Similar to other studies on repeatability, estimates declined with the time interval between two pairs of measurements, suggesting an episodic physiological basis for the documented behaviors. Finally, we detected several inter-sexual differences. Females were more active than males and expressed a shallower decline in movement with aging. Female movement activity was also more repeatable, but female edge preference was less repeatable than that of males. We reason that such differences in repeatability may be driven by sex-specific selection pressures on behavioral tendencies.

Significance statement

We investigate several questions regarding behavioral repeatability in insects. The two main questions asked are (1) whether inter-individual behavioral differences remain consistent across larvae and adult stage, and (2) how repeatability changes throughout aging. The first question has been only rarely tested in insects that undergo a full metamorphosis. It has been recognized as a timely question and as an opportunity for researchers studying animal personality. Previous results regarding amphibians and insects that undergo partial metamorphosis were inconclusive. The second question is important, because studies rarely follow individuals throughout their lives. This is essential to understand the consequences of aging. We also report on differences between males and females, probably indicating on differences in motivation for activity and in patterns of aging. Finally, the question, how behavior changes with ontogeny, has been already recognized by Tinbergen as a basic one in animal behavior.

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References

  • Alcalay Y, Barkae ED, Ovadia O, Scharf I (2014a) Consequences of the instar stage for behavior in a pit-building antlion. Behav Proc 103:105–111

    Article  Google Scholar 

  • Alcalay Y, Ovadia O, Scharf I (2014b) Behavioral repeatability and personality in pit-building antlion larvae under differing environmental contexts. Behav Ecol Socibiol 68:1985–1993

    Article  Google Scholar 

  • Bajer K, Horváth G, Molnár O, Török J, Garamszegi LZ, Herczeg G (2015) European green lizard (Lacerta viridis) personalities: linking behavioural types to ecologically relevant traits at different ontogenetic stages. Behav Proc 111:67–74

    Article  Google Scholar 

  • Bell AM, Hankison SJ, Laskowski KL (2009) The repeatability of behaviour: a meta-analysis. Anim Behav 77:771–783

    Article  PubMed  PubMed Central  Google Scholar 

  • Bengston SE, Pruitt JN, Riechert SE (2014) Differences in environmental enrichment generate contrasting behavioural syndromes in a basal spider lineage. Anim Behav 93:105–110

    Article  Google Scholar 

  • Besson M, Martin JR (2005) Centrophobism/thigmotaxis, a new role for the mushroom bodies in Drosophila. J Neurobiol 62:386–396

    Article  PubMed  Google Scholar 

  • Biro PA, Stamps JA (2010) Do consistent individual differences in metabolic rate promote consistent individual differences in behavior? Trends Ecol Evol 25:653–659

    Article  PubMed  Google Scholar 

  • Boulton K, Grimmer AJ, Rosenthal GG, Walling CA, Wilson AJ (2014) How stable are personalities? A multivariate view of behavioural variation over long and short timescales in the sheepshead swordtail, Xiphophorus birchmanni. Behav Ecol Sociobiol 68:791–803

    Article  Google Scholar 

  • Brodin T (2009) Behavioral syndrome over the boundaries of life—carryovers from larvae to adult damselfly. Behav Ecol 20:30–37

    Article  Google Scholar 

  • Brodin T, Lind MI, Wiberg MK, Johansson F (2013) Personality trait differences between mainland and island populations in the common frog (Rana temporaria). Behav Ecol Sociobiol 67:135–143

    Article  Google Scholar 

  • Brommer JE, Class B (2015) The importance of genotype-by-age interactions for the development of repeatable behavior and correlated behaviors over lifetime. Front Zool 12:S2

    Article  PubMed  PubMed Central  Google Scholar 

  • Campbell JF, Runnion C (2003) Patch exploitation by female red flour beetles, Tribolium castaneum. J Insect Sci 3:20

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Carere C, Drent PJ, Privitera L, Koolhaas JM, Groothuis TGG (2005) Personalities in great tits, Parus major: stability and consistency. Anim Behav 70:795–805

    Article  Google Scholar 

  • Carere C, Maestripieri D (2013) Introduction: animal personalities: who cares and why? In: Carere C, Masteripieri D (eds) Animal personalities: behavior, physiology, and evolution. University of Chicago Press, Chicago, IL, USA

    Chapter  Google Scholar 

  • Chapman RF (2013) The insects: structure and function (5th ed.). Cambridge University Press, Cambridge, UK.

  • Colomb J, Reiter L, Blaszkiewicz J, Wessnitzer J, Brembs B (2012) Open source tracking and analysis of adult Drosophila locomotion in Buridan’s paradigm with and without visual targets. PLoS ONE 7:e42247

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Dahlbom SJ, Lagman D, Lundstedt-Enkel K, Sundström LF, Winberg S (2011) Boldness predicts social status in zebrafish (Danio rerio). PLoS ONE 6:e23565

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Dammhahn M, Almeling L (2012) Is risk taking during foraging a personality trait? A field test for cross-context consistency in boldness. Anim Behav 84:1131–1139

    Article  Google Scholar 

  • Dangles O, Pierre D, Christides JP, Casas J (2007) Escape performance decreases during ontogeny in wild crickets. J Exp Biol 210:3165–3170

    CAS  Article  PubMed  Google Scholar 

  • David M, Auclair Y, Cézilly F (2012) Assessing short- and long-term repeatability and stability of personality in captive zebra finches using longitudinal data. Ethology 118:932–942

    Article  Google Scholar 

  • Dingemanse NJ, Both C, Drent PJ, Van Oers K, Van Noordwijk AJ (2002) Repeatability and heritability of exploratory behaviour in great tits from the wild. Anim Behav 64:929–938

    Article  Google Scholar 

  • Ducatez S, Legrand D, Chaput-Bardy A, Stevens VM, Fréville H, Baguette M (2012) Inter-individual variation in movement: is there a mobility syndrome in the large white butterfly Pieris brassicae? Ecol Entomol 37:377–385

    Article  Google Scholar 

  • Dzieweczynski TL, Hebert OL (2013) The effects of short-term exposure to an endocrine disrupter on behavioral consistency in male juvenile and adult Siamese fighting fish. Archiv Environ Contam Toxicol 64:316–326

    CAS  Article  Google Scholar 

  • Fedina TY, Lewis SM (2007) Female mate choice across mating stages and between sequential mates in flour beetles. J Evol Biol 20:2138–2143

    CAS  Article  PubMed  Google Scholar 

  • Fisher DN, David M, Tregenza T, Rodriguez-Munoz R (2015) Dynamics of among-individual behavioral variation over adult lifespan in a wild insect. Behav Ecol 26:975–985

    Article  PubMed  PubMed Central  Google Scholar 

  • Grim T, Samaš P, Hauber ME (2014) The repeatability of avian egg ejection behaviors across different temporal scales, breeding stages, female ages and experiences. Behav Ecol Sociobiol 68:749–759

    Article  Google Scholar 

  • Grotewiel MS, Martin I, Bhandari P, Cook-Wiens E (2005) Functional senescence in Drosophila melanogaster. Ageing Res Rev 4:372–397

    CAS  Article  PubMed  Google Scholar 

  • Gyuris E, Feró O, Barta Z (2012) Personality traits across ontogeny in firebugs, Pyrrhocoris apterus. Anim Behav 84:103–109

    Article  Google Scholar 

  • Halle S, Nowziki A, Scharf I (2015) The consequences of parental age for development, body mass and resistance to stress in the red flour beetle. Biol J Linn Soc 115:305–314

    Article  Google Scholar 

  • Halliday WD, Blouin-Demers G (2014) Red flour beetles balance thermoregulation and food acquisition via density-dependent habitat selection. J Zool 294:198–205

    Article  Google Scholar 

  • Hedrick AV, Kortet R (2012) Sex differences in the repeatability of boldness over metamorphosis. Behav Ecol Sociobiol 66:407–412

    Article  Google Scholar 

  • Herde A, Eccard JA (2013) Consistency in boldness, activity and exploration at different stages of life. BMC Ecol 13:49

    Article  PubMed  PubMed Central  Google Scholar 

  • Howe RW (1962) The effects of temperature and humidity on the oviposition rate of Tribolium castaneum (Hbst.) (Coleoptera, Tenebrionidae). Bull Ent Res 53:301–310

    Article  Google Scholar 

  • Ishizaki M, Watanabe T, Moriya S, Tabuchi K (2011) Diurnal locomotion activity of adult rice bug, Leptocorisa chinensis (Hemiptera: Alydidae), at different ages, measured by actograph and video camera. Appl Entomol Zool 46:135–142

    Article  Google Scholar 

  • Ismail MZBH, Hodges MD, Boylan M, Achall R, Shirras A, Broughton SJ (2015) The Drosophila insulin receptor independently modulates lifespan and locomotor senescence. PLoS ONE 10:e0125312

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 91:475–482

    Article  Google Scholar 

  • Kralj-Fišer S, Čandek K, Lokovšek T, Čelik T, Cheng RC, Elgar MA, Kuntner M (2016) Mate choice and sexual size dimorphism, not personality, explain female aggression and sexual cannibalism in raft spiders. Anim Behav 111:49–55

    Article  Google Scholar 

  • Kralj-Fišer S, Schuett W (2014) Studying personality variation in invertebrates: why bother? Anim Behav 91:41–52

    Article  Google Scholar 

  • Martin JR (2004) A portrait of locomotor behaviour in Drosophila determined by a video-tracking paradigm. Behav Proc 67:207–219

    Article  Google Scholar 

  • Moretz JA, Martins EP, Robison BD (2007) Behavioral syndromes and the evolution of correlated behavior in zebrafish. Behav Ecol 18:556–562

    Article  Google Scholar 

  • Müller T, Müller C (2015) Behavioural phenotypes over the lifetime of a holometabolous insect. Front Zool 12:S8

    Article  PubMed  PubMed Central  Google Scholar 

  • Nespolo RF, Franco M (2007) Whole-animal metabolic rate is a repeatable trait: a meta-analysis. J Exp Biol 210:2000–2005

    Article  PubMed  Google Scholar 

  • Niemelä PT, Vainikka A, Hedrick AV, Kortet R (2012) Integrating behaviour with life history: boldness of the field cricket, Gryllus integer, during ontogeny. Funct Ecol 26:450–456

    Article  Google Scholar 

  • Park T (1934) Observations on the general biology of the flour beetle, Tribolium confusum. Q Rev Biol 9:36–54

    Article  Google Scholar 

  • Preacher KJ (2002) Calculation for the test of the difference between two independent correlation coefficients [Computer software]. http://quantpsy.org

  • Ridgel AL, Ritzmann RE (2005) Insights into age-related locomotor declines from studies of insects. Ageing Res Rev 4:23–39

    Article  PubMed  Google Scholar 

  • Scharf I, Braf H, Ifrach N, Rosenstein S, Subach A (2015) The effects of temperature and diet during development, adulthood, and mating on reproduction in the red flour beetle. PLoS ONE 10:e0136924

    Article  PubMed  PubMed Central  Google Scholar 

  • Schuett W, Dall SRX (2009) Sex differences, social context and personality in zebra finches, Taeniopygia guttata. Anim Behav 77:1041–1050

    Article  Google Scholar 

  • Shukitt-Hale B, Casadesus G, Cantuti-Castelverti I, Joseph JA (2001) Effect of age on object exploration, habituation, and response to spatial and nonspatial change. Behav Neurosci 115:1059–1064

    CAS  Article  PubMed  Google Scholar 

  • Shuranova Z, Burmistrov Y, Abramson CI (2005) Habituation to a novel environment in the crayfish Procambarus cubensis. J Crustac Biol 25:488–494

    Article  Google Scholar 

  • Sih A, Bell A, Johnson JC (2004) Behavioral syndromes: an ecological and evolutionary overview. Trends Ecol Evol 19:372–378

    Article  PubMed  Google Scholar 

  • Simon AF, Liang DT, Krantz DE (2006) Differential decline in behavioral performance of Drosophila melanogaster with age. Mech Ageing Dev 127:647–651

    Article  PubMed  Google Scholar 

  • Simon P, Dupuis R, Costentin J (1994) Thigmotaxis as an index of anxiety in mice. Influence of dopaminergic transmissions. Behav Brain Res 61:59–64

    CAS  Article  PubMed  Google Scholar 

  • Sinn DL, Gosling SD, Moltschaniwskyj NA (2008) Development of shy/bold behaviour in squid: context-specific phenotypes associated with developmental plasticity. Anim Behav 75:433–442

    Article  Google Scholar 

  • Socha R, Zemek R (2000) Locomotor activity in adult Pyrrhocoris apterus (Heteroptera) in relation to sex, physiological status and wing dimorphism. Physiol Entomol 25:383–389

    Article  Google Scholar 

  • Sokoloff A (1974) The biology of Tribolium: with special emphasis on genetic aspects, vol 2. Oxford University Press, Oxford

    Google Scholar 

  • Sweeney K, Gadd RDH, Hess ZL, McDermott DR, MacDonald L, Cotter P, Armagost F, Chen JZ, Berning AW, DiRienzo N, Pruitt JN (2013) Assessing the effects of rearing environment, natural selection, and developmental stage on the emergence of a behavioral syndrome. Ethology 119:436–447

    Article  Google Scholar 

  • Tremmel M, Müller C (2013) Insect personality depends on environmental conditions. Behav Ecol 24:386–392

    Article  Google Scholar 

  • Truman JW, Riddiford LM (2002) Endocrine insights into the evolution of metamorphosis in insects. Annu Rev Entomol 47:467–500

    CAS  Article  PubMed  Google Scholar 

  • Van Allen BG, Bhavsar P (2014) Natal habitat effects drive density—dependent scaling of dispersal decisions. Oikos 123:699–704

    Article  Google Scholar 

  • Van Dongen WFD, Maldonado K, Sabat P, Vasquez RA (2010) Geographic variation in the repeatability of a personality trait. Behav Ecol 21:1243–1250

    Article  Google Scholar 

  • Via S (1999) Cannibalism facilitates the use of a novel environment in the flour beetle, Tribolium castaneum. Heredity 82:267–275

  • White CR, Schimpf NG, Cassey P (2013) The repeatability of metabolic rate declines with time. J Exp Biol 216:1763–1765

    Article  PubMed  Google Scholar 

  • Wilson ADM, Krause J (2012a) Metamorphosis and animal personality: a neglected opportunity. Trends Ecol Evol 27:529–531

    Article  PubMed  Google Scholar 

  • Wilson ADM, Krause J (2012b) Personality and metamorphosis: is behavioral variation consistent across ontogenetic niche shifts? Behav Ecol 23:1316–1323

    Article  Google Scholar 

  • Young AM (1970) Predation and abundance in populations of flour beetles. Ecology 51:602–619

    Article  Google Scholar 

  • Zajitschek F, Hunt J, Zajitschek SRK, Jennions MD, Brooks R (2007) No intra-locus sexual conflict over reproductive fitness or ageing in field crickets. PLoS ONE 2:e155

    Article  PubMed  PubMed Central  Google Scholar 

  • Zar JH (1999) Biostatistical analysis (4th ed). Prentice Hall, Upper Saddle River, NJ, USA

    Google Scholar 

  • Ziegler JR (1976) Evolution of migration response: emigration by Tribolium and the influence of age. Evolution 30:579–592

    Article  Google Scholar 

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Acknowledgments

This research was partially funded by a start-up grant of the US-Israel Binational Science Foundation no. 2013086 to IS and JNP.

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Authors and Affiliations

  1. Department of Zoology, Faculty of Life Sciences, Tel Aviv University, 69978, Tel Aviv, Israel

    Yonatan Wexler, Aziz Subach & Inon Scharf

  2. Department of Ecology, Evolution, and Marine Biology, University of California, Santa Barbara, CA, USA

    Jonathan N. Pruitt

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  1. Yonatan Wexler
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  2. Aziz Subach
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  3. Jonathan N. Pruitt
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  4. Inon Scharf
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Correspondence to Inon Scharf.

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Communicated by W. Hughes

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Wexler, Y., Subach, A., Pruitt, J.N. et al. Behavioral repeatability of flour beetles before and after metamorphosis and throughout aging. Behav Ecol Sociobiol 70, 745–753 (2016). https://doi.org/10.1007/s00265-016-2098-y

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  • DOI: https://doi.org/10.1007/s00265-016-2098-y

Keywords

  • Activity
  • Behavioral consistency
  • Centrophobism
  • Dispersal
  • Movement
  • Tenebrionidae
  • Tribolium castaneum