Behavioral responses are shaped by a complex interplay of extrinsic factors, such as predation and flow conditions, and intrinsic properties such as metabolic state. We investigated variations in boldness among four populations of zebrafish collected from widely varying habitat conditions across India. We measured feeding latencies of fish in four contexts: in a novel environment; in an environment with refuge and predators; in the presence of a shoal; and in the presence of a shoal and predators. The population from a high-flow and high-predation habitat was significantly bolder than populations from low-predation and low-flow/stagnant habitats. Individuals were significantly bolder in the presence of shoal and predators than in the other contexts. In general, males were significantly bolder than females. Smaller individuals took greater risks to feed than larger individuals only within two populations. The high-predation, high-flow habitat fish also showed significantly lower between- and within-individual variation in boldness than all the low-predation and low-flow populations. Furthermore, we found significantly repeatable responses across contexts within all populations, indicating behavioral consistency. Differences in response to variations in experimental contexts and stress and individual differences in metabolic rates could possibly explain the observed between- and within-individual variation among populations.
Get full access to this article
View all access options for this article.
References
1.
WardAJW, ThomasP, HartPJB, KrauseJ. Correlates of boldness in three-spined sticklebacks (Gasterosteus aculeatus). Behav Ecol Sociobiol, 2004; 55:561–568.
2.
ThomsonJS, WattsPC, PottingerTG, SneddonLU. Plasticity of boldness in rainbow trout, Oncorhynchus mykiss: Do hunger and predation influence risk-taking behaviour?. Horm Behav, 2012; 61:750–757.
3.
KrauseJ, ChengD, KirkmanE, RuxtonG. Species-specific patterns of refuge use in fish: The role of metabolic expenditure and body length. Behaviour, 2000; 137:1113–1127.
4.
BrownC, BraithwaiteVA. Size matters: A test of boldness in eight populations of the poeciliid Brachyraphis episcopi. Anim Behav, 2004; 68:1325–1329.
5.
HerczegG, GondaA, MerilÄJ. Predation mediated population divergence in complex behaviour of nine-spined stickleback (Pungitius pungitius). J Evol Biol, 2009; 22:544–552.
6.
ÁlvarezD, BellAM. Sticklebacks from streams are more bold than sticklebacks from ponds. Behav Processes, 2007; 76:215–217.
7.
BrydgesNM, ColegraveN, HeathcoteRJP, BraithwaiteVA. Habitat stability and predation pressure affect temperament behaviours in populations of three-spined sticklebacks. J Anim Ecol, 2008; 77:229–235.
8.
BrownC, JonesF, BraithwaiteVA. In situ examination of boldness–shyness traits in the tropical poeciliid, Brachyraphis episcopi. Anim Behav, 2005; 70:1003–1009.
9.
ArchardGA, BraithwaiteVA. Increased exposure to predators increases both exploration and activity level in Brachyraphis episcopi. J Fish Biol, 2011; 78:593–601.
10.
MesslerA, WundMA, BakerJA, FosterSA. The effects of relaxed and reversed selection by predators on the antipredator behavior of the threespine stickleback, Gasterosteus aculeatus. Ethology, 2007; 113:953–963.
11.
HerczegG, VälimäkiK. Intraspecific variation in behaviour: Effects of evolutionary history, ontogenetic experience and sex. J Evol Biol, 2011; 24:2434–2444.
12.
BrownC, WarburtonK. Predator recognition and anti-predator responses in the rainbowfish Melanotaenia eachamensis. Behav Ecol Sociobiol, 1997; 41:61–68.
13.
BiroPA, PostJR, ParkinsonEA. From individuals to populations: Prey fish risk-taking mediates mortality in whole-system experiments. Ecology, 2003; 84:2419–2431.
14.
MetcalfeNB, Van LeeuwenTE, KillenSS. Does individual variation in metabolic phenotype predict fish behaviour and performance?. J Fish Biol, 2016; 88:298–321.
15.
KillenSS, FuC, WuQ, WangY-X, FuS-J. The relationship between metabolic rate and sociability is altered by food deprivation. Funct Ecol, 2016; 30:1358–1365.
16.
HarrisS, RamnarineIW, SmithHG, PetterssonLB. Picking personalities apart: Estimating the influence of predation, sex and body size on boldness in the guppy Poecilia reticulata. Oikos, 2010; 119:1711–1718.
17.
PiyapongC, KrauseJ, ChapmanBB, RamnarineIW, LoucaV, CroftDP. Sex matters: A social context to boldness in guppies (Poecilia reticulata). Behav Ecol, 2010; 21:3–8.
18.
IngleySJ, RehmJ, JohnsonJB. Size doesn't matter, sex does: A test for boldness in sister species of Brachyrhaphis fishes. Ecol Evol, 2014; 4:4361–4369.
19.
NespoloRF, FrancoM. Whole-animal metabolic rate is a repeatable trait: A meta-analysis. J Exp Biol, 2007; 210:2000–2005.
20.
BellAM, HankisonSJ, LaskowskiKL. The repeatability of behaviour: A meta-analysis. Anim Behav, 2009; 77:771–783.
21.
QuinnJ, CresswellW. Personality, anti-predation behaviour and behavioural plasticity in the chaffinch Fringilla coelebs. Behaviour, 2005; 142:1377–1402.
22.
DammhahnM, AlmelingL. Is risk taking during foraging a personality trait? A field test for cross-context consistency in boldness. Anim Behav, 2012; 84:1131–1139.
23.
van OersK, MargreetK, DrentPJ. Context dependence of personalities: Risk-taking behavior in a social and a nonsocial situation. Behav Ecol, 2005; 16:716–723.
24.
WebsterMM, HartPJB, WardAJW. Boldness is influenced by social context in threespine sticklebacks (Gasterosteus aculeatus). Behaviour, 2007; 144:351–371.
25.
ColemanK, WilsonD. Shyness and boldness in pumpkinseed sunfish: Individual differences are context-specific. Anim Behav, 1998; 56:927–936.
26.
KareklasK, ArnottG, ElwoodRW, HollandRA. Plasticity varies with boldness in a weakly-electric fish. Front Zool, 2016; 13:22.
27.
WilsonADM, StevensED. Consistency in context-specific measures of shyness and boldness in rainbow trout, Oncorhynchus mykiss. Ethology, 2005; 111:849–862.
28.
Van DongenWFD, MaldonadoK, SabatP, VásquezRA. Geographic variation in the repeatability of a personality trait. Behav Ecol, 2010; 21:1243–1250.
29.
LessellsCM, BoagPT. Unrepeatable repeatabilities: A common mistake. Auk, 1987; 104:116–121.
30.
SpenceR, GerlachG, LawrenceC, SmithC. The behaviour and ecology of the zebrafish, Danio rerio. Biol Rev Camb Philos Soc, 2008; 83:13–34.
31.
EngeszerRE, PattersonLB, RaoAA, ParichyDM. Zebrafish in the wild: A review of natural history and new notes from the field. Zebrafish, 2007; 4:21–40.
32.
ArunachalamM, RajaM, VijayakumarC, MalaiammalP, MaydenRL. Natural history of zebrafish (Danio rerio) in India. Zebrafish, 2013; 10:1–14.
33.
RoyT, BhatA. Can outcomes of dyadic interactions be consistent across contexts among wild zebrafish?. R Soc Open Sci, 2015; 2:150282.
34.
RoyT, BhatA. Learning and memory in juvenile zebrafish: What makes the difference - population or rearing environment?. Ethology, 2016; 122:308–318.
35.
SuriyampolaPS, SheltonDS, ShuklaR, RoyT, BhatA, MartinsEP. Zebrafish social behavior in the wild. Zebrafish, 2016; 13:1–8.
OsbornA, BriffaM. Does repeatable behaviour in the laboratory represent behaviour under natural conditions? A formal comparison in sea anemones. Anim Behav, 2017; 123:197–206.
39.
ShuklaR, BhatA. Morphological divergences and ecological correlates among wild populations of zebrafish (Danio rerio). Environ Biol Fishes, 2017; 100:251–264.
40.
BatesD, MaechlerM, BolkerB. lme4: Linear mixed effects models using S4 classes. 2012. R package version. 0.999375-42.
41.
BolkerBM, BrooksME, ClarkCJ, GeangeSW, PoulsenJR, StevensMHH, et al.Generalized linear mixed models: A practical guide for ecology and evolution. Trends Ecol Evol, 2009; 24:127–135.
PolverinoG, RubertoT, StaaksG, MehnerT. Tank size alters mean behaviours and individual rank orders in personality traits of fish depending on their life stage. Anim Behav, 2016; 115:127–135.
46.
NakagawaS, SchielzethH. Repeatability for Gaussian and non-Gaussian data: A practical guide for biologists. Biol Rev, 2010; 85:935–956.
DowlingLM, GodinJ-GJ. Refuge use in a killifish: Influence of body size and nutritional state. Can J Zool, 2002; 80:782–788.
49.
HerczegG, GondaA, KuparinenA, MeriläJ. Contrasting growth strategies of pond versus marine populations of nine-spined stickleback (Pungitius pungitius): A combined effect of predation and competition?. Evol Ecol, 2012; 26:109–122.
50.
BrownC, BurgessF, BraithwaiteVA. Heritable and experiential effects on boldness in a tropical poeciliid. Behav Ecol Sociobiol, 2007; 62:237–243.
51.
HillJ, GrossmanGD. An energetic model of microhabitat use for rainbow trout and rosyside dace. Ecology, 1993; 74:685–698.
52.
KillenSS, GlazierDS, RezendeEL, ClarkTD, AtkinsonD, WillenerAST, et al.Ecological influences and morphological correlates of resting and maximal metabolic rates across teleost fish species. Am Nat, 2016; 187:592–606.
53.
MartinsEP, BhatA. Population-level personalities in zebrafish: Aggression-boldness across but not within populations. Behav Ecol, 2014; 25:368–373.
54.
WhiteleyAR, BhatA, MartinsEP, MaydenRL, ArunachalamM, Uusi-HeikkiläSet al.Population genomics of wild and laboratory zebrafish (Danio rerio). Mol Ecol, 2011; 20:4259–4276.
55.
MagurranAE, SeghersBH. Sexual conflict as a consequence of ecology: Evidence from guppy, Poecilia reticulata, populations in Trinidad. Proc R Soc B Biol Sci, 1994; 255:31–36.
56.
WolfM, van DoornGS, LeimarO, WeissingFJ. Life-history trade-offs favour the evolution of animal personalities. Nature, 2007; 447:581–584.
57.
KingAJ, FürtbauerI, MamuneasD, JamesC, ManicaA. Sex-differences and temporal consistency in stickleback fish boldness. PLoS One, 2013; 8:31–36.
58.
KrauseJ, LoaderSP, McDermottJ, RuxtonGD. Refuge use by fish as a function of body length-related metabolic expenditure and predation risks. Proc R Soc B Biol Sci, 1998; 265:2373–2379.
59.
SkalskiGT, GilliamJF. Feeding under predation hazard: Testing models of adaptive behavior with stream fish. Am Nat, 2002; 160:158–172.
60.
SihA, BellA, JohnsonJC. Behavioral syndromes: An ecological and evolutionary overview. Trends Ecol Evol, 2004; 19:372–378.
61.
WilsonDS, ColemanK, ClarkAB, BiedermanL. Shy-bold continuum in pumpkinseed sunfish (Lepomis gibbosus): An ecological study of a psychological trait. J Comp Psychol, 1993; 107:250–260.
62.
GotthardK, NylinS. Adaptive plasticity and plasticity as an adaptation: A selective review of plasticity in animal morphology and life history. Oikos, 1995; 74:3–17.
63.
FalconerDS, MackayTF, FrankhamR. Introduction to quantitative genetics (4th edn). Trends in Genetics, 1996; 12:280.
64.
PitcherTJ, ParrishJK: Functions of shoaling behaviour in teleosts. In: Behaviour of Teleost Fishes. PitcherTJ (ed), pp. 363–439, Springer, Dordrecht, 1993.
65.
DingemanseNJ, WolfM. Between-individual differences in behavioural plasticity within populations: Causes and consequences. Anim Behav, 2013; 85:1031–1039.
66.
WangT, HungCCY, RandallDJ. The comparative physiology of food deprivation: From feast to famine. Annu Rev Physiol, 2006; 68:223–251.
67.
KillenSS, MarrasS, McKenzieDJ. Fuel, fasting, fear: Routine metabolic rate and food deprivation exert synergistic effects on risk-taking in individual juvenile European sea bass. J Anim Ecol, 2011; 80:1024–1033.
Supplementary Material
Please find the following supplemental material available below.
For Open Access articles published under a Creative Commons License, all supplemental material carries the same license as the article it is associated with.
For non-Open Access articles published, all supplemental material carries a non-exclusive license, and permission requests for re-use of supplemental material or any part of supplemental material shall be sent directly to the copyright owner as specified in the copyright notice associated with the article.
