Abstract
Geographic range has long been noted to be associated with many organismic and ecological traits such as body size and species richness. However, much less is known about whether and how ecological variation across latitudinal gradients reflects behavioral variation. Ant colonies may also show behavioral variation, and Temnothorax rugatulus show a colony-level behavioral syndrome that seems to reflect risk tolerance across their North American range. While it is presumed that this pattern is the result of adaptation to local environmental conditions, which ecological factors are driving this variation are unknown. Here, we test if colony risk tolerance is affected by competition, predation, resource availability, or environmental stress at each site. Our results show that increased competition, specifically for nest sites, as well as increased spatial clustering of colonies predicts higher risk tolerance. Additionally, the spatial clustering of colonies influences the structure of the risk-taking syndrome, i.e., which colony-level behaviors are correlated and how strongly. This emphasizes the need for understanding large-scale geographic variation in behavior, as it may explain how ecological factors drive the evolution and maintenance of intraspecific behavioral variation across populations.
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References
Anderson CA (2001) Heat and violence. Curr Dir Psychol Sci 10:33–38. doi:10.1111/1467-8721.00109
Anderson DR, Burnham KP (2002) Avoiding pitfalls when using information-theoretic methods. J Wildl Manag 66:912–918. doi:10.2307/3803155
Angilletta MJ Jr, Wilson RS, Navas CA, James RS (2003) Tradeoffs and the evolution of thermal reaction norms. Trends Ecol Evol 18:234–240. doi:10.1016/S0169-5347(03)00087-9
Ashton KG (2004) Sensitivity of intraspecific latitudinal clines of body size for tetrapods to sampling, latitude and body size. Integr Comp Biol 44:403–412. doi:10.1093/icb/44.6.403
Ashton KG, Feldman CR (2003) Bergmann’s rule in nonavian reptiles: turtles follow it, lizards and snakes reverse it. Evolution 57:1151–1163
Bell AM, Stamps JA (2004) Development of behavioural differences between individuals and populations of sticklebacks, Gasterosteus aculeatus. Anim Behav 68:1339–1348. doi:10.1016/j.anbehav.2004.05.007
Bengston SE, Dornhaus A (2013) Colony size does not predict foraging distance in the ant Temnothorax rugatulus: a puzzle for standard scaling models. Insect Soc 60:93–96. doi:10.1007/s00040-012-0272-4
Bengston SE, Dornhaus A (2014) Be meek or be bold? A colony-level behavioural syndrome in ants. Proc R Soc B Biol Sci 281:20140518. doi:10.1098/rspb.2014.0518
Bengston SE, Jandt JM (2014) The development of collective personality: the ontogenetic drivers of behavioral variation across groups. Behav Evol Ecol 2:81. doi:10.3389/fevo.2014.00081
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. doi:10.1016/j.anbehav.2014.04.022
Biro PA, Stamps JA (2008) Are animal personality traits linked to life-history productivity? Trends Ecol Evol 23:361–368. doi:10.1016/j.tree.2008.04.003
Biro PA, Abrahams MV, Post JR, Parkinson EA (2004) Predators select against high growth rates and risk–taking behaviour in domestic trout populations. Proc R Soc Lond B Biol Sci 271:2233–2237. doi:10.1098/rspb.2004.2861
Blanckenhorn WU, Fairbairn DJ (1995) Life history adaptation along a latitudinal cline in the water strider Aquarius remigis (Heteroptera: Gerridae). J Evol Biol 8:21–41. doi:10.1046/j.1420-9101.1995.8010021.x
Blumstein DT (2006) Developing an evolutionary ecology of fear: how life history and natural history traits affect disturbance tolerance in birds. Anim Behav 71:389–399. doi:10.1016/j.anbehav.2005.05.010
Bryant MJ, Grant JWA (1995) Resource defence, monopolization and variation of fitness in groups of female Japanese medaka depend on the synchrony of food arrival. Anim Behav 49:1469–1479. doi:10.1016/0003-3472(95)90068-3
Burnham KP, Anderson DR, Huyvaert KP (2010) AIC model selection and multimodel inference in behavioral ecology: some background, observations, and comparisons. Behav Ecol Sociobiol 65:23–35. doi:10.1007/s00265-010-1029-6
Cao TT, Dornhaus A (2012) Ants use pheromone markings in emigrations to move closer to food-rich areas. Insect Soc 59:87–92. doi:10.1007/s00040-011-0192-8
Chapuisat M, Goudet J, Keller L (1997) Microsatellites reveal high population viscosity and limited dispersal in the ant formica paralugubris. Evolution 51:475–482. doi:10.2307/2411120
Clark PJ, Evans FC (1954) Distance to nearest neighbor as a measure of spatial relationships in populations. Ecology 35:445–453. doi:10.2307/1931034
Conover DO (1992) Seasonality and the scheduling of life history at different latitudes. J Fish Biol 41:161–178. doi:10.1111/j.1095-8649.1992.tb03876.x
Conover DO, Schultz ET (1995) Phenotypic similarity and the evolutionary significance of countergradient variation. Trends Ecol Evol 10:248–252. doi:10.1016/S0169-5347(00)89081-3
Costa R, Peixoto AA, Barbujani G, Kyriacou CP (1992) A latitudinal cline in a drosophila clock gene. Proc R Soc Lond B Biol Sci 250:43–49. doi:10.1098/rspb.1992.0128
Cousyn C, Meester LD, Colbourne JK et al (2001) Rapid, local adaptation of zooplankton behavior to changes in predation pressure in the absence of neutral genetic changes. Proc Natl Acad Sci 98:6256–6260. doi:10.1073/pnas.111606798
Croy MI, Hughes RN (1991) Effects of food supply, hunger, danger and competition on choice of foraging location by the fifteen-spined stickleback, Spinachia spinachia L. Anim Behav 42:131–139. doi:10.1016/S0003-3472(05)80613-X
Derksen S, Keselman HJ (1992) Backward, forward and stepwise automated subset selection algorithms: Frequency of obtaining authentic and noise variables. Br J Math Stat Psychol 45:265–282. doi:10.1111/j.2044-8317.1992.tb00992.x
Dingemanse NJ, Kazem AJN, Réale D, Wright J (2010) Behavioural reaction norms: animal personality meets individual plasticity. Trends Ecol Evol 25:81–89. doi:10.1016/j.tree.2009.07.013
Dornhaus A, Chittka L (2004) Why do honey bees dance? Behav Ecol Sociobiol 55:395–401. doi:10.1007/s00265-003-0726-9
Dornhaus A, Holley J-A, Pook VG et al (2008) Why do not all workers work? Colony size and workload during emigrations in the ant Temnothorax albipennis. Behav Ecol Sociobiol 63:43–51. doi:10.1007/s00265-008-0634-0
Dornhaus A, Holley J-A, Franks NR (2009) Larger colonies do not have more specialized workers in the ant Temnothorax albipennis. Behav Ecol. doi:10.1093/beheco/arp070
Fisher J (1954) Evolution and bird sociality. Evol Process 71–83
Fisher BL (1999) Improving inventory efficiency: a case study of leaf-litter ant diversity of Madagascar. Ecol Appl 9:714–731. doi:10.1890/1051-0761(1999)009[0714:IIEACS]2.0.CO;2
Foitzik S, Heinze J (1998) Nest site limitation and colony takeover in the ant Leptothorax nylanderi. Behav Ecol 9:367–375. doi:10.1093/beheco/9.4.367
Goldberg JL, Grant JWA, Lefebvre L (2001) Effects of the temporal predictability and spatial clumping of food on the intensity of competitive aggression in the Zenaida dove. Behav Ecol 12:490–495. doi:10.1093/beheco/12.4.490
Gordon DM (2013) The rewards of restraint in the collective regulation of foraging by harvester ant colonies. Nature 498:91–93. doi:10.1038/nature12137
Grand TC, Dill LM (1999) The effect of group size on the foraging behaviour of juvenile coho salmon: reduction of predation risk or increased competition? Anim Behav 58:443–451. doi:10.1006/anbe.1999.1174
Grant JWA, Guha RT (1993) Spatial clumping of food increases its monopolization and defense by convict cichlids, Cichlasoma nigrofasciatum. Behav Ecol 4:293–296. doi:10.1093/beheco/4.4.293
Guttman L (1954) Some necessary conditions for common-factor analysis. Psychometrika 19:149–161. doi:10.1007/BF02289162
Holway DA (1998) Factors governing rate of invasion: a natural experiment using Argentine ants. Oecologia 115:206–212. doi:10.1007/s004420050509
Hood WG, Tschinkel WR (1990) Desiccation resistance in arboreal and terrestrial ants. Physiol Entomol 15:23–35. doi:10.1111/j.1365-3032.1990.tb00489.x
Inger R, Bearhop S, Robinson JA, Ruxton G (2006) Prey choice affects the trade-off balance between predation and starvation in an avian herbivore. Anim Behav 71:1335–1341. doi:10.1016/j.anbehav.2005.08.015
Jackson DA (1993) Stopping rules in principal components analysis: a comparison of heuristical and statistical approaches. Ecology 74:2204–2214. doi:10.2307/1939574
Jandt JM, Bengston S, Pinter-Wollman N et al (2014) Behavioural syndromes and social insects: personality at multiple levels. Biol Rev 89:48–67. doi:10.1111/brv.12042
Jongepier E, Kleeberg I, Job S, Foitzik S (2014) Collective defence portfolios of ant hosts shift with social parasite pressure. Proc R Soc B Biol Sci 281:20140225. doi:10.1098/rspb.2014.0225
Kaspari M, Vargo EL (1995) Colony size as a buffer against seasonality: Bergmann’s rule in social insects. Am Nat 145:610–632
Kaspari M, Ward PS, Yuan M (2004) Energy gradients and the geographic distribution of local ant diversity. Oecologia 140:407–413. doi:10.1007/s00442-004-1607-2
Kelley OJ, Hunter AS, Haise HR, Hobbs CH (1946) Comparison of methods of measuring soil moisture under field conditions
Lima SL (1998) Stress and decision-making under the risk of predation: recent developments from behavioral, reproductive, and ecological perspectives. Advances in the study of behavior: stress and behavior. Academic Press
McGlone J, Stansbury W, Tribble L (1987) Effects of heat and social stressors and within-pen weight variation on young pig performance and agonistic behavior. J Anim Sci 65:456–462
Modlmeier AP, Foitzik S (2011) Productivity increases with variation in aggression among group members in Temnothorax ants. Behav Ecol 22:1026–1032. doi:10.1093/beheco/arr086
Mundry R (2010) Issues in information theory-based statistical inference—a commentary from a frequentist’s perspective. Behav Ecol Sociobiol 65:57–68. doi:10.1007/s00265-010-1040-y
Pamminger T, Modlmeier AP, Suette S et al (2012) Raiders from the sky: slavemaker founding queens select for aggressive host colonies. Biol Lett. doi:10.1098/rsbl.2012.0499
Partridge LW, Partridge KA, Franks NR (1997) Field survey of a monogynous leptothoracine ant (Hymenoptera, Formicidae) evidence of seasonal polydomy ? Insect Soc 44:75–83. doi:10.1007/s000400050031
Pinter-Wollman N, Gordon DM, Holmes S (2012) Nest site and weather affect the personality of harvester ant colonies. Behav Ecol. doi:10.1093/beheco/ars066
Relyea RA (2001) Morphological and behavioral plasticity of larval anurans in response to different predators. Ecology 82:523–540. doi:10.1890/0012-9658(2001)082[0523:MABPOL]2.0.CO;2
Riechert SE, Jones TC (2008) Phenotypic variation in the social behaviour of the spider Anelosimus studiosus along a latitudinal gradient. Anim Behav 75:1893–1902. doi:10.1016/j.anbehav.2007.10.033
Rueppell O, Kirkman RW (2005) Extraordinary starvation resistance in Temnothorax rugatulus (Hymenoptera, Formicidae) colonies: demography and adaptive behavior. Insect Soc 52:282–290. doi:10.1007/s00040-005-0804-2
Rüppell O, Heinze J, Hölldobler B (1998) Size-dimorphism in the queens of the North American ant Leptothorax rugatulus (Emery). Insect Soc 45:67–77. doi:10.1007/s000400050069
Rüppell O, Strätz M, Baier B, Heinze J (2003) Mitochondrial markers in the ant Leptothorax rugatulus reveal the population genetic consequences of female philopatry at different hierarchical levels. Mol Ecol 12:795–801. doi:10.1046/j.1365-294X.2003.01769.x
Sasaki T, Pratt SC (2013) Ants learn to rely on more informative attributes during decision-making. Biol Lett 9:20130667. doi:10.1098/rsbl.2013.0667
Sawyer LA, Sandrelli F, Pasetto C et al (2006) The period gene thr-Gly polymorphism in Australian and African drosophila melanogaster populations: implications for selection. Genetics 174:465–480. doi:10.1534/genetics.106.058792
Scheiner SM (1993) Genetics and evolution of phenotypic plasticity. Annu Rev Ecol Syst 24:35–68
Schumacher B (2002) Methods for the determination of total organic carbon (TOC) in soils and sediments
Sih A, Bell A, Johnson JC (2004) Behavioral syndromes: an ecological and evolutionary overview. Trends Ecol Evol 19:372–378. doi:10.1016/j.tree.2004.04.009
Stachowicz JJ, Hay ME (2000) Geographic variation in camouflage specialization by a decorator crab. Am Nat 156:59–71. doi:10.1086/an.2000.156.issue-1
Tran MV, O’Grady M, Colborn J et al (2014) Aggression and food resource competition between sympatric hermit crab species. PLoS ONE 9:e91823. doi:10.1371/journal.pone.0091823
West-Eberhard MJ (1989) Phenotypic plasticity and the origins of diversity. Annu Rev Ecol Syst 20:249–278
Acknowledgments
We would like to thank the Dornhaus lab, Stephen Pratt and two anonymous reviewers for helpful feedback on the manuscript, Daniel Charbonneau for advice and feedback on the data analysis, Min Shin and Hoan Nguyen for their development of the optic flow algorithm, as well as NSF (grants no. IOS-1045239 and DBI-1262292 to AD).
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Communicated by W. O. H. Hughes
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Supplemental Figure 1
All of the models tested in the stepwise model selection process and the associated AIC value of each model. The final model selected resulted in the percentage of nest sites occupied and the clustering index as the predictive variables with an AIC score of -146.9. (JPEG 60 kb)
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Bengston, S.E., Dornhaus, A. Latitudinal variation in behaviors linked to risk tolerance is driven by nest-site competition and spatial distribution in the ant Temnothorax rugatulus . Behav Ecol Sociobiol 69, 1265–1274 (2015). https://doi.org/10.1007/s00265-015-1939-4
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DOI: https://doi.org/10.1007/s00265-015-1939-4