Springer Nature is making SARS-CoV-2 and COVID-19 research free. View research | View latest news | Sign up for updates

Are most samples of animals systematically biased? Consistent individual trait differences bias samples despite random sampling


Sampling animals from the wild for study is something nearly every biologist has done, but despite our best efforts to obtain random samples of animals, ‘hidden’ trait biases may still exist. For example, consistent behavioral traits can affect trappability/catchability, independent of obvious factors such as size and gender, and these traits are often correlated with other repeatable physiological and/or life history traits. If so, systematic sampling bias may exist for any of these traits. The extent to which this is a problem, of course, depends on the magnitude of bias, which is presently unknown because the underlying trait distributions in populations are usually unknown, or unknowable. Indeed, our present knowledge about sampling bias comes from samples (not complete population censuses), which can possess bias to begin with. I had the unique opportunity to create naturalized populations of fish by seeding each of four small fishless lakes with equal densities of slow-, intermediate-, and fast-growing fish. Using sampling methods that are not size-selective, I observed that fast-growing fish were up to two-times more likely to be sampled than slower-growing fish. This indicates substantial and systematic bias with respect to an important life history trait (growth rate). If correlations between behavioral, physiological and life-history traits are as widespread as the literature suggests, then many animal samples may be systematically biased with respect to these traits (e.g., when collecting animals for laboratory use), and affect our inferences about population structure and abundance. I conclude with a discussion on ways to minimize sampling bias for particular physiological/behavioral/life-history types within animal populations.

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

Fig. 1
Fig. 2


  1. Allison PD (1995) Survival analysis using the SAS system: a practical guide. SAS Institute, Cary

  2. Askey PJ, Richards SA, Post JR, Parkinson EA (2006) Linking angling catch rates and fish learning under catch-and-release regulations. North Am J Fish Manag 26:1020–1029

  3. Askey PJ, Post JR, Parkinson EA, Rivot E, Paul AJ, Biro PA (2007) Estimation of gillnet efficiency and selectivity across multiple sampling units: a hierarchical Bayesian analysis using mark-recapture data. Fish Res 83:162–174

  4. Beckmann C, Biro PA, Post JR (2006) Asymmetric effect of bird predation on fish population size-structure in whole-lake experiments. Can J Zool 84:1584–1593

  5. Biro PA, Dingemanse NJ (2009) Sampling bias resulting from animal personality. Trends Ecol Evol 24:66–68

  6. Biro PA, Post JR (2008) Rapid depletion of genotypes with fast growth and bold personality traits from harvested fish populations. Proc Natl Acad Sci USA 105:2919–2922

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

  8. Biro PA, Post JR, Parkinson EA (2003) From individuals to populations: risk-taking by prey fish mediates mortality in whole-system experiments. Ecology 84:2419–2431

  9. Boon A, Reale D, Boutin S (2008) Personality, habitat use, and their consequences for survival in North American red squirrels Tamiasciurius hudsonicus. Oikos 117:1321–1328

  10. Boulanger J, Kendall KC, Stetz JB, Roon DA, Waits LP, Paetkau D (2008) Multiple data sources improve DNA-based mark-recapture population estimates of grizzly bears. Ecol Appl 18:577–589

  11. Boyer N, Réale D, Marmet J, Pisanu B, Chapuis J-L (2010) Personality, space use and tick load in an introduced population of Siberian chipmunks Tamias sibiricus. J Anim Ecol 79:538–547

  12. Burnham KP, Overton WS (1978) Estimation of the size of a closed population when capture probabilities vary among animals. Biometrika 65:625–633

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

  14. Carter AJ, Heinsohn R, Goldizen AW, Biro PA (2012) Boldness, trappability and sampling bias in wild lizards. Anim Behav 83:1051–1058

  15. Crespin L, Choquet R, Lima M, Merritt J, Pradel R (2008) Is heterogeneity of catchability in capture–recapture studies a mere sampling artifact or a biologically relevant feature of the population? Popul Ecol 50:247–256

  16. Crowcroft P, Jeffers JNR (1961) Variability in the behaviour of wild house mice (mus musculus l.) towards live traps. Proc Zool Soc Lond 137:573–582

  17. Gabriel PO, Black JM (2010) Behavioural syndromes in Steller’s jays: the role of time frames in the assessment of behavioural traits. Anim Behav 80:689–697

  18. Garamszegi LZ, Eens M, Török J (2009) Behavioural syndromes and trappability in free-living collared flycatchers, Ficedula albicollis. Anim Behav 77:803–812

  19. Gérard D, Bauchau V, Smets S (1994) Reduced trappability in wild mice, Mus musculus domesticus, heterozygous for Robertsonian translocations. Anim Behav 47:877–883

  20. Gimenez O, Viallefont A, Charmantier A, Pradel R, Cam E, Brown CR, Anderson MD, Brown MB, Covas R, Gaillard J-M (2008) The risk of flawed inference in evolutionary studies when detectability is less than one. Am Nat 172:441–448

  21. Gjedrem T (2000) Genetic improvement of cold-water fish species. Aquacult Res 31:25–36

  22. Guillette LM, Reddon AR, Hurd PL, Sturdy CB (2009) Exploration of a novel space is associated with individual differences in learning speed in black-capped chickadees, Poecile atricapillus. Behav Process 82:265–270

  23. Jørgensen C, Enberg K, Dunlop ES, Arlinghaus R, Boukal DS, Brander K, Ernande B, Gårdmark A, Johnston F, Matsumura S, Pardoe H, Raab K, Silva A, Vainikka A, Dieckmann U, Heino M, Rijnsdor AD (2007) Managing evolving fish stocks. Science 318:1247–1248

  24. MacKenzie DI, Kendall WL (2002) How should detection probability be incorporated into estimates of relative abundance? Ecology 83:2387–2393

  25. Martins CIM, Schrama JW, Verreth JAJ (2005) The consistency of individual differences in growth, feed efficiency and feeding behaviour in African catfish Clarias gariepinus (Burchell 1822) housed individually. Aquacult Res 36:1509–1516

  26. Patterson LD, Schulte-Hostedde AI (2011) Behavioural correlates of parasitism and reproductive success in male eastern chipmunks, Tamias striatus. Anim Behav 81:1129–1137

  27. Pellegrini A, Wisenden B, Sorensen P (2010) Bold minnows consistently approach danger in the field and lab in response to either chemical or visual indicators of predation risk. Behav Ecol Sociobiol 64:381–387

  28. Post JR, Parkinson EA, Johnston NT (1999) Density-dependent processes in structured fish populations: assessment of interaction strengths in whole-lake experiments. Ecol Monogr 69:155–175

  29. Pradel R, Choquet R, Lima M, Merritt J, Crespin L (2010) Estimating population growth rate from capture–recapture data in presence of capture heterogeneity. J Agric Biol Environ Stat 15:248–258

  30. Reale D, Gallant BY, Leblanc M, Festa-Bianchet M (2000) Consistency of temperament in bighorn ewes and correlates with behaviour and life history. Anim Behav 60:589–597

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

  32. Rodríguez-Prieto I, Martín J, Fernández-Juricic E (2011) Individual variation in behavioural plasticity: direct and indirect effects of boldness, exploration and sociability on habituation to predators in lizards. Proc R Soc Lond B 278:266–273

  33. Sih A, Bell AM (2008) Insights for behavioral ecology from behavioral syndromes. Adv Study Behav 38:227–281

  34. Sih A, Bell AM, Johnson JC, Ziemba RE (2004) Behavioural syndromes: an integrative overview. Q Rev Biol 79:241–277

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

  36. Stamps JA, Groothuis TGG (2010) The development of animal personality: relevance, concepts and perspectives. Biol Rev 85:301–325

  37. Werner EE, Anholt BR (1993) Ecological consequences of the trade-off between growth and mortality rates mediated by foraging activity. Am Nat 142:242–272

  38. Williams TD (2008) Individual variation in endocrine systems: moving beyond the ‘tyranny of the Golden Mean’. Philos Trans R Soc Lond B 363:1687–1698

  39. Wilson DS, Coleman K, Clark AB, Biederman L (1993) Shy–bold continuum in pumpkinseed sunfish (Lepomis gibbosus): an ecological study of a psychological trait. J Comp Psychol 107:250–260

  40. Wilson ADM, Godin J-GJ, Ward AJW (2010) Boldness and reproductive fitness correlates in the Eastern Mosquitofish, Gambusia holbrooki. Ethology 116:96–104

  41. Wilson ADM, Binder TR, McGrath KP, Cooke SJ, Godin J-GJ (2011) Capture technique and fish personality: angling targets timid bluegill sunfish, Lepomis macrochirus. Can J Fish Aquat Sci 68:749–757

Download references


This study was supported by NSERC Canada and ARC Future Fellowship Australia. Thanks to C. Beckmann, J.A. Endler, B. Adriaenssens, J.A. Stamps, and two anonymous reviewers for valuable and constructive comments on earlier drafts.

Author information

Correspondence to Peter A. Biro.

Additional information

Communicated by Pedro Peres-Neto.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Biro, P.A. Are most samples of animals systematically biased? Consistent individual trait differences bias samples despite random sampling. Oecologia 171, 339–345 (2013). https://doi.org/10.1007/s00442-012-2426-5

Download citation


  • Selection
  • Life history
  • Behavior
  • Harvest
  • Fishing
  • Personality
  • Temperament