Skip to main content
Springer Nature Link
Log in

Predation selects for low resting metabolic rate and consistent individual differences in anti-predator behavior in a beetle

  • Original Paper
  • Published:
acta ethologica Aims and scope Submit manuscript

Abstract

Significant between-individual variation in resting metabolic rate (RMR) of animals is a widespread phenomenon that may have important implications for our understanding of variation in behavior and animal personality. By using wild caught mealworm beetles, Tenebrio molitor, we examined the relationships among survival rate under predator tests, individual response latency time to become immobile under the risk of predation, duration of immobility time, and RMR. Individuals with higher levels of RMR were bold, and bold individuals were found to be more exposed to the risk of bird predation. We found that RMR was positively correlated with the latency of immobility response and negatively correlated with the total duration of immobility. The correlation between behavioral responses suggests a behavioral syndrome in the anti-predator behavior of T. molitor. The results indicate that energy metabolism may be part of a syndrome that involves behavior and life history traits in animals.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Alcock J (2001) Animal behavior: an evolutionary approach. Sinauer, Sunderland

    Google Scholar 

  • Alvarez D, Nicieza AG (2005) Is metabolic rate a reliable predictor of growth and survival of brown trout (Salmo trutta) in the wild? Can J Fish Aquat Sci 62:643–649

    Google Scholar 

  • Artacho P, Nespolo RF (2009) Natural selection reduces energy metabolism in the garden snail, Helix aspersa (Cornu aspersum). Evolution 63:1044–1050

    PubMed  CAS  Google Scholar 

  • Barnard C (2007) Ethical regulation and animal science: why animal behaviour is special. Anim Behav 74:5–13

    Google Scholar 

  • Bell AM, Sih A (2007) Exposure to predation generates personality in threespined sticklebacks (Gasterosteus aculeatus). Ecol Lett 10:828–834

    PubMed  Google Scholar 

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

    Google Scholar 

  • Bhattacharya AK, Ameel JJ, Waldbaue GP (1970) Method for sexing living pupal and adult yellow mealworms. Ann Entomol Soc Am 63:1783

    Google Scholar 

  • Biro PA, Stamps JA (2008) Are animal personality traits linked to life-history productivity? Trends Ecol Evol 23:361–368

    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

    PubMed  Google Scholar 

  • Biro PA, Abrahams MV, Post JR, Parkinson EA (2006) Behavioural trade-offs between growth and mortality explain evolution of submaximal growth rates. J Anim Ecol 75:1165–1171

    PubMed  Google Scholar 

  • Biro PA, Beckmann C, Stamps JA (2010) Small within-day increases in temperature affects boldness and alters personality in coral reef fish. Proc R Soc B Biol Sci 277:71–77

    Google Scholar 

  • Boratynski Z, Koteja P (2009) The association between body mass, metabolic rates and survival of bank voles. Funct Ecol 23:330–339

    Google Scholar 

  • Burton T, Killen SS, Armstrong JD, Metcalfe NB (2011) What causes intraspecific variation in resting metabolic rate and what are its ecological consequences? Proc R Soc B Biol Sci 278:3465–3473

    CAS  Google Scholar 

  • Butler SJ, Whittingham MJ, Quinn JL, Cresswell W (2005) Quantifying the interaction between food density and habitat structure in determining patch selection. Anim Behav 69:337–343

    Google Scholar 

  • Candolin U (1998) Reproduction under predation risk and the trade-off between current and future reproduction in the threespine stickleback. Proc R Soc B Biol Sci 265:1171–1175

    Google Scholar 

  • Careau V, Thomas D, Humphries MM, Réale D (2008) Energy metabolism and animal personality. Oikos 117:641–653

    Google Scholar 

  • Castañeda LE, Figueroa CC, Bacigalupe LD, Nespolo RF (2010) Effects of wing polyphenism, aphid genotype and host plant chemistry on energy metabolism of the grain aphid, Sitobion avenae. J Insect Physiol 56:1920–1924

    PubMed  Google Scholar 

  • Chappell MA, Garland T, Rezende EL, Gomes FR (2004) Voluntary running in deer mice: speed, distance, energy costs and temperature effects. J Exp Biol 207:3839–3854

    PubMed  Google Scholar 

  • Cuthill IC (2007) Ethical regulation and animal science: why animal behaviour is not so special. Anim Behav 74:15–22

    Google Scholar 

  • Daan S, Masman D, Strijkstra AM, Kenagy GJ (1990) Daily energy turnover during reproduction in birds and mammals: its relationships to basal metabolic rate. Acta XX Congr Int Ornithol IV:1976–1987

    Google Scholar 

  • Dall SRX, Witter MS (1998) Feeding interruptions, diurnal mass changes and daily routines of behaviour in the zebra finch. Anim Behav 55:715–725

    PubMed  Google Scholar 

  • Dall SRX, Houston AI, McNamara JM (2004) The behavioural ecology of personality: consistent individual differences from an adaptive perspective. Ecol Lett 7:734–739

    Google Scholar 

  • Daukste J, Kivleniece I, Krama T, Rantala MJ, Krams I (2012) Senescence in immune priming and attractiveness in a beetle. J Evol Biol 25:1298–1304

    PubMed  CAS  Google Scholar 

  • Dingemanse NJ, Réale D (2005) Natural selection and animal personality. Behaviour 142:1159–1184

    Google Scholar 

  • Dingemanse NJ, Wolf M (2010) Recent models for adaptive personality differences: a review. Philos Trans R Soc B 365:3947–3958

    Google Scholar 

  • Dohm MR (2002) Repeatability estimates do not always set an upper limit to heritability. Funct Ecol 16:273–280

    Google Scholar 

  • Duncan FD (2003) The role of the subelytral cavity in respiration in a tenebrionid beetle, Onymacris multistriata (Tenebrionidae: Adesmiini). J Insect Physiol 49:339–346

    PubMed  CAS  Google Scholar 

  • Duncan FD, Byrne MJ (2005) The role of the mesothoracic spiracles in respiration in flighted and flightless dung beetles. J Exp Biol 208:907–914

    PubMed  Google Scholar 

  • Earle M, Lavigne DM (1990) Intraspecific variation in body size, metabolic rate, and reproduction of deer mice (Peromyscus maniculatus). Can J Zool 68:381–388

    Google Scholar 

  • Fedigan LM (2010) Ethical issues faced by field primatologists: asking the relevant questions. Am J Primatol 72:754–771

    PubMed  Google Scholar 

  • Finerty SE, Wolt RC, Davis RW (2009) Summer activity pattern and field metabolic rate of adult male sea otters (Enhydra lutris) in a soft sediment habitat in Alaska. J Exp Mar Biol Ecol 377:36–42

    Google Scholar 

  • Fu SJ, Xie XJ, Cao ZD (2005) Effect of fasting and repeat feeding on metabolic rate in southern catfish, Silurus meridionalis Chen. Mar Freshw Behav Physiol 38:191–198

    Google Scholar 

  • Fu SJ, Cao ZD, Peng JL, Wang YX (2008) Is peak postprandial oxygen consumption positively related to growth rate and resting oxygen consumption in a sedentary catfish Silurus meridionalis? J Fish Biol 73:692–701

    CAS  Google Scholar 

  • Gilliam JF, Fraser DF (1987) Habitat selection under predation hazard—test of a model with foraging minnows. Ecology 68:1856–1862

    Google Scholar 

  • Godin JGJ (1995) Predation risk and alternative mating tactics in male Trinidadian guppies (Poecilia reticulata). Oecologia 103:224–229

    Google Scholar 

  • Godin JGJ (1997) Evading predators. In: Godin JGJ (ed) Behavioural ecology of teleost fishes. Oxford University Press, New York, pp 191–236

    Google Scholar 

  • Godin JGJ, Dugatkin LA (1996) Female mating preference for bold males in the guppy, Poecilia reticulata. Proc Natl Acad Sci USA 93:10262–10267

    PubMed  CAS  Google Scholar 

  • Gray EM, Bradley TJ (2006) Evidence from mosquitoes suggests that cyclic gas exchange and discontinuous gas exchange are two manifestations of a single respiratory pattern. J Exp Biol 209:1603–1611

    PubMed  Google Scholar 

  • Groothuis TGG, Carere C (2005) Avian personalities: characterization and epigenesis. Neurosci Biobehav Rev 29:137–150

    PubMed  Google Scholar 

  • Gyuris E, Feró O, Tartally A, Barta Z (2011) Individual behaviour in firebugs (Pyrrhocoris apterus). Proc R Soc B Biol Sci 278:628–633

    Google Scholar 

  • Hammond KA, Diamond J (1997) Maximal sustained energy budgets in humans and animals. Nature 386:457–462

    PubMed  CAS  Google Scholar 

  • Hammond KA, Wunder BA (1995) Effect of cold temperatures on the morphology of gastrointestinal tracts of two microtine rodents. J Mammal 76:232–239

    Google Scholar 

  • Hammond KA, Lam M, Lloyd KCK, Diamond J (1996) Simultaneous manipulation of intestinal capacities and nutrient loads in mice. Am J Physiol Gastrointest Liver 271:G969–G979

    CAS  Google Scholar 

  • Hayes JP, Garland T, Dohm MR (1992) Individual variation in metabolism and reproduction of Mus: are energetics and life history linked? Funct Ecol 6:5–14

    Google Scholar 

  • Hedrick AV, Kortet R (2006) Hiding behaviour in two cricket populations that differ in predation pressure. Anim Behav 72:1111–1118

    Google Scholar 

  • Hetz SK (1994) Untersuchung zu Atmung, Kreislauf und Säure-Basen-Regulation an Puppen der tropischen Schmetterlingsgattungen Ornithoptera, Troides and Attacus. Dissertation at Friedrich-Alexander-Universität, Erlangen-Nürnberg, p 216

  • Hollander FA, van Overveld T, Tokka I, Matthysen E (2008) Personality and nest defence in the great tit (Parus major). Ethology 114:405–412

    Google Scholar 

  • Hõrak P, Lauri S, Ots I, Kollist H (2002) Repeatability of condition indices in captive greenfinches (Carduelis chloris). Can J Zool 80:636–643

    Google Scholar 

  • Jackson DM, Trayhurn P, Speakman JR (2001) Associations between energetics and over-winter survival in the short-tailed field vole Microtus agrestis. J Anim Ecol 70:633–640

    Google Scholar 

  • Jones KA, Godin J-GJ (2010) Are fast explorers slow reactors? Linking personality type and anti-predator behaviour. Proc R Soc B Biol Sci 277:625–632

    Google Scholar 

  • Karise R, Kuusik A, Mänd M, Metspalu L, Williams IH, Hiiesaar K, Luik A, Muljar R, Liiv K (2010) Gas exchange patterns of bumble bee foragers before and after exposing to lowered temperature. J Insect Physiol 56:529–535

    PubMed  CAS  Google Scholar 

  • Kivleniece I, Krams I, Daukste J, Krama T, Rantala MJ (2010) Sexual attractiveness of immune-challenged male mealworm beetles suggests terminal investment in reproduction. Anim Behav 80:1015–1021

    Google Scholar 

  • Kortet R, Hedrick ANN (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

    Google Scholar 

  • Kortet R, Härkönen L, Hokkanen P, Härkönen S, Kaitala A, Kaunisto S, Laaksonen S, Kekäläinen J, Ylönen H (2010) Experiments on the ectoparasitic deer ked that often attacks humans; preferences for body parts, colour and temperature. Bull Entomol Res 100:279–285

    PubMed  CAS  Google Scholar 

  • Koteja P (2000) Energy assimilation, parental care and the evolution of endothermy. Proc R Soc B Biol Sci 267:479–484

    CAS  Google Scholar 

  • Kotiaho JS, Alatalo RV, Mappes J, Nielsen MG, Parri S, Rivero A (1998) Energetic costs of size and sexual signalling in a wolf spider. Proc R Soc B Biol Sci 265:2203–2209

    Google Scholar 

  • Krams I, Daukste J, Kivleniece I, Krama T, Rantala MJ (2013a) Previous encapsulation response enhances within individual protection against fungal parasite in the mealworm beetle Tenebrio molitor. Insect Science, doi:10.1111/j.1744-7917.2012.01574.x

  • Krams I, Daukste J, Kivleniece I, Kaasik A, Krama T, Freeberg TM, Rantala MJ (2013b) Trade-off between cellular immunity and life span in mealworm beetles Tenebrio molitor. Current Zoology 59 in press

  • Krause J, Ruxton GD (2002) Living in groups. Oxford University Press, New York

    Google Scholar 

  • Lantovį P, Zub K, Koskela E, Sķchovį K, Borowski Z (2011) Is there a linkage between metabolism and personality in small mammals? The root vole (Microtus oeconomus) example. Physiol Behav 104:378–383

    Google Scholar 

  • Larivee ML, Boutin S, Speakman JR, McAdam AG, Humphries MM (2010) Associations between over-winter survival and resting metabolic rate in juvenile North American red squirrels. Funct Ecol 24:597–607

    Google Scholar 

  • Lessells CM, Boag PT (1987) Unrepeatable repeatabilities: a common mistake. Auk 104:116–121

    Google Scholar 

  • Lighton JRB (2008) Measuring metabolic rate: a manual for scientists. Oxford University Press, New York

    Google Scholar 

  • Lima SL, Dill LM (1990) Behavioral decisions made under the risk of predation—a review and prospectus. Can J Zool 68:619–640

    Google Scholar 

  • Luttbeg B, Sih A (2010) Risk, resources and state-dependent adaptive behavioural syndromes. Philos Trans R Soc B 365:3977–3990

    Google Scholar 

  • Lynch M, Walsh B (1998) Genetics and analysis of quantitative traits. Sinauer, Sunderland

    Google Scholar 

  • Macleod R, Gosler AG, Cresswell W (2005) Diurnal mass gain strategies and perceived predation risk in the great tit Parus major. J Anim Ecol 74:956–964

    Google Scholar 

  • Magnhagen C (1990) Reproduction under predation risk in the sand goby, Pomatoschistus minutus, and the black goby, Gobius niger, the effect of age and longevity. Behav Ecol Sociobiol 26:331–335

    Google Scholar 

  • Mänd M, Kuusik A, Martin AJ, Williams IH, Luik A, Karise R, Metspalu L, Hiiesaar K (2005) Discontinuous gas exchange cycles and active ventilation in pupae of the bumblebee Bombus terrestris. Apidologie 36:561–570

    Google Scholar 

  • Mänd M, Kuusik A, Martin AJ, Williams IH, Luik A, Karise R (2006) Regular periods of abdominal contractions recorded from larvae of the bumblebee, Bombus terrestris (Hymenoptera: Apidae). Eur J Entomol 103:319–322

    Google Scholar 

  • McLean JA, Speakman JR (2000) Effects of body mass and reproduction on the basal metabolic rate of brown long-eared bats (Plecotus auritus). Physiol Biochem Zool 73:112–121

    PubMed  CAS  Google Scholar 

  • Metcalfe NB, Taylor AC, Thorpe JE (1995) Metabolic rate, social status and life-history strategies in Atlantic salmon. Anim Behav 49:431–436

    Google Scholar 

  • Metspalu L, Kuusik A, Hiiesaar K, Tartes U (2002) Tonic immobility in adult Colorado potato beetle, Leptinotarsa decemlineata (Coleoptera: Chrysomelidae) evoked by mechanical and optical stimuli. Eur J Entomol 99:215–219

    Google Scholar 

  • Miyatake T, Katayama K, Takeda Y, Nakashima A, Sugita A, Mizumoto M (2004) Is death-feigning adaptive? Heritable variation in fitness difference of death-feigning behaviour. Proc R Soc B Biol Sci 271:2293–2296

    Google Scholar 

  • Miyatake T, Nakayama S, Nishi Y, Nakajima S (2009) Tonically immobilized selfish prey can survive by sacrificing others. Proc R Soc B Biol Sci 276:2763–2767

    Google Scholar 

  • Moret Y (2006) ‘Trans-generational immune priming’: specific enhancement of the antimicrobial immune response in the mealworm beetle, Tenebrio molitor. Proc R Soc B Biol Sci 273:1399–1405

    CAS  Google Scholar 

  • Mueller P, Diamond J (2001) Metabolic rate and environmental productivity: well-provisioned animals evolved to run and idle fast. Proc Nat Acad Sci USA 98:12550–12554

    PubMed  CAS  Google Scholar 

  • Muljar R, Karise R, Viik E, Kuusik A, Williams I, Metspalu L, Hiiesaar K, Must A, Luik A, Mänd M (2012) Effects of Fastac 50 EC on bumble bee Bombus terrestris L. respiration: DGE disappearance does not lead to increasing water loss. J Insect Physiol 58:1469–1476

    PubMed  CAS  Google Scholar 

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

    PubMed  Google Scholar 

  • Nespolo RF, Roff DA, Fairbairn DJ (2008) Energetic trade-off between maintenance costs and flight capacity in the sand cricket (Gryllus firmus). Funct Ecol 22:624–631

    Google Scholar 

  • Niemelä PT, Vainikka A, Lahdenperä S, Kortet R (2012) Nymphal density, behavioural development, and life history in a field cricket. Behav Ecol Sociobiol 66:645–652

    Google Scholar 

  • Niemelä PT, Vainikka A, Forsman JT, Loukola OJ, Kortet R (2013) How does variation in the environment and individual cognition explain the existence of consistent behavioural differences? Ecol Evol 3:457–464

    PubMed  Google Scholar 

  • Niewiarowski PH, Balk ML, Londraville RL (2000) Phenotypic effects of leptin in an ectotherm: a new tool to study the evolution of life histories and endothermy? J Exp Biol 203:295–300

    PubMed  CAS  Google Scholar 

  • Quinlan MC, Lighton JRB (1999) Respiratory physiology and water relations of three species of Pogonomyrmex harvester ants (Hymenoptera: Formicidae). Physiol Entomol 24:293–302

    Google Scholar 

  • Quinn JL, Cresswell W (2005) Personality, anti-predation behaviour and behavioural plasticity in the chaffinch Fringilla coelebs. Behaviour 142:1377–1402

    Google Scholar 

  • Réale D, Reader SM, Sol D, McDougall PT, Dingemanse NJ (2007) Integrating animal temperament within ecology and evolution. Biol Rev 82:291–318

    PubMed  Google Scholar 

  • Réale D, Dingemanse NJ, Kazem AJN, Wright J (2010) Evolutionary and ecological approaches to the study of personality. Philos Trans R Soc B Biol Sci 365:3937–3946

    Google Scholar 

  • Rezende EL, Chappell MA, Gomes FR, Malisch JL, Garland T (2005) Maximal metabolic rates during voluntary exercise, forced exercise, and cold exposure in house mice selectively bred for high wheel-running. J Exp Biol 208:2447–2458

    PubMed  Google Scholar 

  • Rezende EL, Gomes FR, Chappell MA, Garland T (2009) Running behavior and its energy cost in mice selectively bred for high voluntary locomotor activity. Physiol Biochem Zool 82:662–679

    PubMed  Google Scholar 

  • Ruxton GD, Sherratt TN, Speed MP (2004) Avoiding attack: the evolutionary ecology of crypsis, aposematism and mimicry. Oxford University Press, Oxford

    Google Scholar 

  • Sadd B, Holman L, Armitage H, Lock F, Marland R, Siva-Jothy MT (2006) Modulation of sexual signalling by immune challenged male mealworm beetles (Tenebrio molitor, L.): evidence for terminal investment and dishonesty. J Evol Biol 19:321–325

    PubMed  CAS  Google Scholar 

  • Sadowska ET, Labocha MK, Baliga K, Stanisz A, Wroblewska AK, Jagusiak W, Koteja P (2005) Genetic correlations between basal and maximum metabolic rates in a wild rodent: consequences for evolution of endothermy. Evolution 59:672–681

    PubMed  Google Scholar 

  • Schmidt-Nielsen K (1991) Animal physiology. Cambridge University Press, Cambridge

    Google Scholar 

  • Schmitz A (2005) Metabolic rates in harvestmen (Arachnida, Opiliones): the influence of running activity. Physiol Entomol 30:75–81

    Google Scholar 

  • Sih A, Bell AM (2008) Insights for behavioral ecology from behavioral syndromes, chapter 5. In: Brockmann HJ, Roper TJ, Naguib M, Wynne-Edwards K, Barnard C, Mitani JC (eds) Advances in the study of behavior, vol 38. Academic, New York, pp 227–281

    Google Scholar 

  • Smith BR, Blumstein DT (2008) Fitness consequences of personality: a meta-analysis. Behav Ecol 19:448–455

    Google Scholar 

  • Smith BR, Blumstein DT (2010) Behavioral types as predictors of survival in Trinidadian guppies (Poecilia reticulata). Behav Ecol 21:919–926

    Google Scholar 

  • Speakman JR, Ergon T, Cavanagh R, Reid K, Scantlebury DM, Lambin X (2003) Resting and daily energy expenditures of free-living field voles are positively correlated but reflect extrinsic rather than intrinsic effects. Proc Natl Acad Sci 100:14057–14062

    PubMed  CAS  Google Scholar 

  • Speakman JR, Krol E, Johnson MS (2004) The functional significance of individual variation in basal metabolic rate. Physiol Biochem Zool 77:900–915

    PubMed  Google Scholar 

  • Stamps JA (2007) Growth-mortality tradeoffs and ‘personality traits’ in animals. Ecol Lett 10:355–363

    PubMed  Google Scholar 

  • Szafranska PA, Zub K, Konarzewski M (2007) Long-term repeatability of body mass and resting metabolic rate in free-living weasels, Mustela nivalis. Funct Ecol 21:731–737

    Google Scholar 

  • Tartes U, Kuusik A, Vanatoa A (1999) Diversity in gas exchange and muscular activity patterns in insects studied by a respirometer-actograph. Physiol Entomol 24:150–157

    Google Scholar 

  • Vainikka A, Seppala O, Loytynoja K, Rantala MJ (2006) Fitness consequences of female preference for male pheromones in Tenebrio molitor. Evol Ecol Res 8:943–957

    Google Scholar 

  • Van Oers K, Drent PJ, de Goede P, van Noordwijk AJ (2004) Realized heritability and repeatability of risk-taking behaviour in relation to avian personalities. Proc R Soc B Biol Sci 271:65–73

    Google Scholar 

  • Vezina F, Speakman JR, Williams TD (2006) Individually variable energy management strategies in relation to energetic costs of egg production. Ecology 87:2447–2458

    PubMed  Google Scholar 

  • West-Eberhard MJ (2003) Developmental plasticity and evolution. Oxford University Press, New York

    Google Scholar 

  • Wolf M, Weissing FJ (2010) An explanatory framework for adaptive personality differences. Philos Trans R Soc B Biol Sci 365:3959–3968

    Google Scholar 

  • Wolf M, van Doorn GS, Leimar O, Weissing FJ (2007) Life-history trade-offs favour the evolution of animal personalities. Nature 447:581–584

    PubMed  CAS  Google Scholar 

  • Wone B, Sears MW, Labocha MK, Donovan ER, Hayes JP (2009) Genetic variances and covariances of aerobic metabolic rates in laboratory mice. Proc R Soc B Biol Sci 276:3695–3704

    Google Scholar 

  • Worden BD, Parker PG (2001) Polyandry in grain beetles, Tenebrio molitor, leads to greater reproductive success: material or genetic benefits? Behav Ecol 12:761–767

    Google Scholar 

  • Worden B, Skemp A, Papaj D (2005) Learning in two contexts: the effects of interference and body size in bumblebees. J Exp Biol 208:2045–2053

    PubMed  Google Scholar 

  • Yamamoto T, Ueda H, Higashi S (1998) Correlation among dominance status, metabolic rate and otolith size in masu salmon. J Fish Biol 52:281–290

    Google Scholar 

  • Yeates LC, Williams TM, Fink TL (2007) Diving and foraging energetics of the smallest marine mammal, the sea otter (Enhydra lutris). J Exp Biol 210:1960–1970

    PubMed  Google Scholar 

  • Ylonen H (1994) Vole cycles and antipredatory behavior. Trends Ecol Evol 9:426–430

    PubMed  CAS  Google Scholar 

  • Zera AJ, Zhao ZW (2006) Intermediary metabolism and life-history trade-offs: differential metabolism of amino acids underlies the dispersal–reproduction trade-off in a wing-polymorphic cricket. Am Nat 167:889–900

    PubMed  Google Scholar 

Download references

Acknowledgments

The study was supported by the Academy of Finland to M.J.R. and I.K., by the Estonian Ministry of Education and Science to R.M. (target-financing project number 0180004s09) and to M.M. and A.K. (target-financing project number SF0170057s09), by the Estonian Science Foundation Grant No. 7391 to M.M. and A.K., and by the European Social Fund within the project “Support for the implementation of doctoral studies at Daugavpils University” (agreement number 2009/0140/1DP/1.1.2.1.2./09/IPIA/ VIAA/015) to I.K. and J.V. T.M.F. acknowledges the support of a Fulbright award during Spring 2012, which helped make his work on this manuscript possible.

Author information

Authors and Affiliations

  1. Institute of Systematic Biology, University of Daugavpils, 5401, Daugavpils, Latvia

    Indrikis Krams, Inese Kivleniece, Tatjana Krama & Jolanta Vrublevska

  2. Department of Plant Protection, Institute of Agricultural and Environmental Sciences, Estonian University of Life Science, 51014, Tartu, Estonia

    Aare Kuusik & Marika Mänd

  3. Department of Psychology and Department of Ecology and Evolutionary Biology, University of Tennessee, Knoxville, TX, USA

    Todd M. Freeberg

  4. Institute of Ecology and Earth Sciences, University of Tartu, 51014, Tartu, Estonia

    Indrikis Krams & Raivo Mänd

  5. Section of Ecology, Department of Biology, University of Turku, 20024, Turku, Finland

    Markus J. Rantala

Authors
  1. Indrikis Krams
    View author publications

    You can also search for this author inPubMed Google Scholar

  2. Inese Kivleniece
    View author publications

    You can also search for this author inPubMed Google Scholar

  3. Aare Kuusik
    View author publications

    You can also search for this author inPubMed Google Scholar

  4. Tatjana Krama
    View author publications

    You can also search for this author inPubMed Google Scholar

  5. Todd M. Freeberg
    View author publications

    You can also search for this author inPubMed Google Scholar

  6. Raivo Mänd
    View author publications

    You can also search for this author inPubMed Google Scholar

  7. Jolanta Vrublevska
    View author publications

    You can also search for this author inPubMed Google Scholar

  8. Markus J. Rantala
    View author publications

    You can also search for this author inPubMed Google Scholar

  9. Marika Mänd
    View author publications

    You can also search for this author inPubMed Google Scholar

Corresponding author

Correspondence to Indrikis Krams.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Krams, I., Kivleniece, I., Kuusik, A. et al. Predation selects for low resting metabolic rate and consistent individual differences in anti-predator behavior in a beetle. acta ethol 16, 163–172 (2013). https://doi.org/10.1007/s10211-013-0147-3

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10211-013-0147-3

Keywords