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Oecologia

, Volume 178, Issue 4, pp 1093–1103 | Cite as

Foraging syndromes and trait variation in antlions along a climatic gradient

  • Yehonatan Alcalay
  • Inon Scharf
  • Ofer Ovadia
Behavioral ecology - Original research

Abstract

Behavioral syndromes arise when individual behavior is correlated over time and/or across environmental contexts, often resulting in inter-population behavioral differences. Three main hypotheses have been suggested to explain the evolution of behavioral syndromes. The constraint hypothesis suggests that behaviors originate from a shared mechanism with a strong genetic or physiological basis. In contrast, according to the adaptive hypothesis, behavioral syndromes depend on specific selective pressures in each environment, and thus should evolve when specific behavioral combinations are advantageous. Finally, behavioral syndromes can also arise owing to neutral stochastic processes. We tested here for variation in the foraging syndromes of pit-building antlions originating from different populations along a climatic gradient. Although inter-population variation existed in some traits, foraging syndromes were similar across populations, supporting the constraint hypothesis. These findings suggest that stabilizing selection, acting on the foraging behavior of antlions during their larval phase, outweighs local selection pressures, resulting in “constraint syndromes.” We also explored behavioral repeatability of foraging-related traits within and among habitats (natural, novel and disturbed habitats), and detected different levels of repeatability: pit diameter was more repeatable than response time to prey, followed by prey exploitation efficiency. Behavioral repeatability of the same trait differed according to context, suggesting that repeatability is a trait in itself and should not be considered identical even when studying the same behavioral trait.

Keywords

Behavioral syndrome Climate gradient Natural selection Repeatability Trap-building predators 

Notes

Acknowledgments

The research leading to this manuscript was partially funded by a start-up grant of the US-Israel Binational Science Foundation no. 2013086 to I. S.

Supplementary material

442_2015_3284_MOESM1_ESM.docx (19 kb)
Supplementary material 1 (DOCX 18 kb)

References

  1. Abràmoff MD, Magalhães PJ, Ram SJ (2004) Image processing with ImageJ. J Biophotonics 11:36–43Google Scholar
  2. Abramsky Z (1988) The role of habitat and productivity in structuring desert rodent communities. Oikos 52:107–114CrossRefGoogle Scholar
  3. Alcalay Y, Barkae ED, Ovadia O, Scharf I (2014a) Consequences of the instar stage for behaviour in a pit-building antlion. Behav Process 103:105–111CrossRefGoogle Scholar
  4. Alcalay Y, Ovadia O, Scharf I (2014b) Behavioral repeatability and personality in pit-building antlion larvae under differing environmental contexts. Behav Ecol Sociobiol 68:1985–1993CrossRefGoogle Scholar
  5. Armbruster W, Schwaegerle K (1996) Causes of covariation of phenotypic traits among populations. J Evol Biol 9:261–276CrossRefGoogle Scholar
  6. Arnett AE, Gotelli NJ (1999a) Bergmann’s rule in the ant lion Myrmeleon immaculatus DeGeer (Neuroptera: Myrmeleontidae): geographic variation in body size and heterozygosity. J Biogeogr 26:275–283CrossRefGoogle Scholar
  7. Arnett AE, Gotelli NJ (1999b) Geographic variation in life-history traits of the ant lion, Myrmeleon immaculatus: evolutionary implications of Bergmann’s rule. Evolution 53:1180–1188CrossRefGoogle Scholar
  8. Arnett AE, Gotelli NJ (2001) Pit-building decisions of larval ant lions: effects of larval age, temperature, food, and population source. J Insect Behav 14:89–97CrossRefGoogle Scholar
  9. Atkinson D (1994) Temperature and organism size—a biological law for ectotherms? Adv Ecol Res 25:1–58CrossRefGoogle Scholar
  10. Barkae ED, Scharf I, Subach A, Ovadia O (2010) The involvement of sand disturbance, cannibalism and intra-guild predation in competitive interactions among pit-building antlion larvae. Zoology 113:308–315PubMedCrossRefGoogle Scholar
  11. Barkae ED, Scharf I, Abramsky Z, Ovadia O (2012) Jack of all trades, master of all: a positive association between habitat niche breadth and foraging performance in pit-building antlion larvae. PLoS One 7:e33506PubMedCentralPubMedCrossRefGoogle Scholar
  12. Bell AM (2005) Behavioural differences between individuals and two populations of stickleback (Gasterosteus aculeatus). J Evol Biol 18:464–473PubMedCrossRefGoogle Scholar
  13. Bell AM (2007) Future directions in behavioural syndromes research. Proc R Soc B Lond B Biol Sci 274:755–761CrossRefGoogle Scholar
  14. Bell AM, Sih A (2007) Exposure to predation generates personality in three spined sticklebacks (Gasterosteus aculeatus). Ecol Lett 10:828–834PubMedCrossRefGoogle Scholar
  15. Bengston S, Dornhaus A (2014) Be meek or be bold? A colony-level behavioural syndrome in ants. Proc R Soc Lond B Biol Sci 281:20140518CrossRefGoogle Scholar
  16. Blanckenhorn W, Demont M (2004) Bergmann and converse Bergmann latitudinal clines in arthropods: two ends of a continuum? Integr Comp Biol 44:413–424PubMedCrossRefGoogle Scholar
  17. Brown JS (1988) Patch use as an indicator of habitat preference, predation risk, and competition. Behav Ecol Sociobiol 22:37–47CrossRefGoogle Scholar
  18. Brown C, Laland KN (2003) Social learning in fishes: a review. Fish Fish 4:280–288CrossRefGoogle Scholar
  19. Castellano S, Cuatto B, Rinella R, Rosso A, Giacoma C (2002) The advertisement call of the European treefrogs (Hyla arborea): a multilevel study of variation. Ethology 108:75–89CrossRefGoogle Scholar
  20. Chown SL, Gaston KJ (1999) Exploring links between physiology and ecology at macro-scales: the role of respiratory metabolism in insects. Biol Rev Camb Philos Soc 74:87–120CrossRefGoogle Scholar
  21. Dall SRX, Bell AM, Bolnick DI, Ratnieks FL (2012) An evolutionary ecology of individual differences. Ecol Lett 15:1189–1198PubMedCentralPubMedCrossRefGoogle Scholar
  22. Dall’Olmo G, Karnieli A (2002) Monitoring phenological cycles of desert ecosystems using NDVI and LST data derived from NOAA-AVHRR imagery. Int J Remote Sens 23:4055–4071CrossRefGoogle Scholar
  23. Danin A (1978) Plant species diversity and plant succession in a sandy area in the Northern Negev. Flora 167:409–422Google Scholar
  24. Devetak D, Novak T, Janžekovič F (2012) Effect of substrate density on behaviour of antlion larvae (Neuroptera: Myrmeleontidae). Acta Oecol 43:1–7CrossRefGoogle Scholar
  25. Dingemanse NJ, Wolf M (2010) Recent models for adaptive personality differences: a review. Philos Trans R Soc Lond B Biol Sci 365:3947–3958PubMedCentralPubMedCrossRefGoogle Scholar
  26. Dingemanse NJ, Both C, Drent PJ, Tinbergen JM (2004) Fitness consequences of avian personalities in a fluctuating environment. Proc R Soc Lond B Biol Sci 271:847–852CrossRefGoogle Scholar
  27. Dingemanse NJ, Wright J, Kazem AJ, Thomas DK, Hickling R, Dawnay N (2007) Behavioural syndromes differ predictably between 12 populations of three-spined stickleback. J Anim Ecol 76:1128–1138PubMedCrossRefGoogle Scholar
  28. Dochtermann NA, Jenkins SH (2007) Behavioural syndromes in Merriam’s kangaroo rats (Dipodomys merriami): a test of competing hypotheses. Proc R Soc Lond B Biol Sci 274:2343–2349CrossRefGoogle Scholar
  29. Dochtermann NA, Jenkins SH, Swartz MJ, Hargett AC (2012) The roles of competition and environmental heterogeneity in the maintenance of behavioral variation and covariation. Ecology 93:1330–1339PubMedCrossRefGoogle Scholar
  30. Duckworth RA (2006) Behavioral correlations across breeding contexts provide a mechanism for a cost of aggression. Behav Ecol 17:1011–1019CrossRefGoogle Scholar
  31. Dupont-Prinet A, Chatain B, Grima L, Vandeputte M, Claireaux G, McKenzie D (2010) Physiological mechanisms underlying a trade-off between growth rate and tolerance of feed deprivation in the European sea bass (Dicentrarchus labrax). J Exp Biol 213:1143–1152PubMedCrossRefGoogle Scholar
  32. Eltz T (1997) Foraging in the ant-lion Myrmeleon mobilis Hagen 1888 (Neuroptera: Myrmeleontidae): behavioral flexibility of a sit-and-wait predator. J Insect Behav 10:1–11CrossRefGoogle Scholar
  33. Endler JA, Houde AE (1995) Geographic variation in female preferences for male traits in Poecilia reticulata. Evolution 49:456–468CrossRefGoogle Scholar
  34. Falissard B (2012) psy: Various procedures used in psychometry. R package version 1.1. http://CRAN.R-project.org/package=psy
  35. Farji-Brener AG (2003) Microhabitat selection by antlion larvae, Myrmeleon crudelis: effect of soil particle size on pit-trap design and prey capture. J Insect Behav 16:783–796CrossRefGoogle Scholar
  36. Farji-Brener AG, Carvajal D, Gei MG, Olano J, Sanchez JD (2008) Direct and indirect effects of soil structure on the density of an antlion larva in a tropical dry forest. Ecol Entomol 33:183–188CrossRefGoogle Scholar
  37. Foster SA (1999) The geography of behaviour: an evolutionary perspective. Trends Ecol Evol 14:190–195PubMedCrossRefGoogle Scholar
  38. Foster SA, Endler JA (1999) Thoughts on geographic variation in behavior. In: Foster SA, Endler JA (eds) Geographic variation in behavior. Oxford University Press, New YorkGoogle Scholar
  39. Goldreich Y (2003) The climate of Israel: observation, research, and application. Kluwer Academic/Plenum, New YorkCrossRefGoogle Scholar
  40. Gosling SD (2001) From mice to men: what can we learn about personality from animal research? Psychol Bull 127:45–86PubMedCrossRefGoogle Scholar
  41. Gotelli NJ (1993) Ant lion zones: causes of high-density predator aggregations. Ecology 74:226–237CrossRefGoogle Scholar
  42. Guerra PA, Pollack GS (2007) A life history trade-off between flight ability and reproductive behavior in male field crickets (Gryllus texensis). J Insect Behav 20:377–387CrossRefGoogle Scholar
  43. Hayes JP, Jenkins SH (1997) Individual variation in mammals. J Mamm 78:274–293CrossRefGoogle Scholar
  44. Herczeg G, Gonda A, Merilä J (2009) Predation mediated population divergence in complex behaviour of nine-spined stickleback (Pungitius pungitius). J Evol Biol 22:544–552PubMedCrossRefGoogle Scholar
  45. Hoffmann AA, Merilä J (1999) Heritable variation and evolution under favourable and unfavourable conditions. Trends Ecol Evol 14:96–101PubMedCrossRefGoogle Scholar
  46. Karan D, Parkash R (1998) Desiccation tolerance and starvation resistance exhibit opposite latitudinal clines in Indian geographical populations of Drosophila kikkawai. Ecol Entomol 23:391–396CrossRefGoogle Scholar
  47. Klokočovnik V, Devetak D, Orlačnik M (2012) Behavioral plasticity and variation in pit construction of antlion larvae in substrates with different particle sizes. Ethology 118:1102–1110CrossRefGoogle Scholar
  48. Lucas JR (1982) The biophysics of pit construction by antlion larvae (Myrmeleon, Neuroptera). Anim Behav 30:651–664CrossRefGoogle Scholar
  49. Lucas JR (1985a) Partial prey consumption by antlion larvae. Anim Behav 33:945–958CrossRefGoogle Scholar
  50. Lucas JR (1985b) Metabolic rates and pit-construction costs of two antlion species. J Anim Ecol 54:295–309CrossRefGoogle Scholar
  51. Ofer J (2000) Let’s go to the ant. A field guide to the ants of Israel (in Hebrew). Yuval Ofer, JerusalemGoogle Scholar
  52. Parsons SM, Joern A (2014) Life history traits associated with body size covary along a latitudinal gradient in a generalist grasshopper. Oecologia 174:379–391PubMedCrossRefGoogle Scholar
  53. Price T, Langen T (1992) Evolution of correlated characters. Trends Ecol Evol 7:307–310PubMedCrossRefGoogle Scholar
  54. Pruitt JN, Riechert SE, Iturralde G, Vega M, Fitzpatrick BM, Aviles L (2010) Population differences in behaviour are explained by shared within-population trait correlations. J Evol Biol 23:748–756PubMedCrossRefGoogle Scholar
  55. Quinn JL, Cresswell W (2005) Personality, anti-predation behaviour and behavioural plasticity in the chaffinch Fringilla coelebs. Behaviour 142:1377–1402CrossRefGoogle Scholar
  56. R Core Team (2014) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. http://www.R-project.org/
  57. Réale D, Reader SM, Sol D, McDougall PT, Dingemanse NJ (2007) Integrating animal temperament within ecology and evolution. Biol Rev 82:291–318PubMedCrossRefGoogle Scholar
  58. Refsnider JM, Milne-Zelman C, Warner DA, Janzen FJ (2014) Population sex ratios under differing local climates in a reptile with environmental sex determination. Evol Ecol 28:977–989CrossRefGoogle Scholar
  59. Roff DA (2002) Life history evolution. Sinauer, SunderlandGoogle Scholar
  60. Rosenzweig MR, Bennett EL (1996) Psychobiology of plasticity: effects of training and experience on brain and behavior. Behav Brain Res 78:57–65PubMedCrossRefGoogle Scholar
  61. Rotkopf R, Ovadia O (2014) Examining growth rate and starvation endurance in pit-building antlions from Mediterranean and desert regions. Ecol Entomol 39:94–100CrossRefGoogle Scholar
  62. Rotkopf R, Alcalay Y, Bar-Hanin E, Barkae ED, Ovadia O (2013) Slow growth improves compensation ability: examining growth rate and starvation endurance in pit-building antlions from semi-arid and hyper-arid regions. Evol Ecol 27:1129–1144CrossRefGoogle Scholar
  63. Scharf I, Ovadia O (2006) Factors influencing site abandonment and site selection in a sit-and-wait predator: a review of pit-building antlion larvae. J Insect Behav 19:197–218CrossRefGoogle Scholar
  64. Scharf I, Filin I, Golan M, Buchshtav M, Subach A, Ovadia O (2008) A comparison between desert and Mediterranean antlion populations: differences in life history and morphology. J Evol Biol 21:162–172PubMedGoogle Scholar
  65. Scharf I, Filin I, Ben-Yehoshua D, Ovadia O (2009a) Phenotypic plasticity and variation in morphological and life-history traits of antlion adults across a climatic gradient. Zoology 112:139–150PubMedCrossRefGoogle Scholar
  66. Scharf I, Filin I, Ovadia O (2009b) A trade-off between growth and starvation endurance in a pit-building antlion. Oecologia 160:453–460PubMedCrossRefGoogle Scholar
  67. Scharf I, Golan B, Ovadia O (2009c) The effect of sand depth, feeding regime, density, and body mass on the foraging behaviour of a pit-building antlion. Ecol Entomol 34:26–33CrossRefGoogle Scholar
  68. Scharf I, Barkae ED, Ovadia O (2010) Response of pit-building antlions to repeated unsuccessful encounters with prey. Anim Behav 79:153–158CrossRefGoogle Scholar
  69. Scharf I, Lubin Y, Ovadia O (2011) Foraging decisions and behavioural flexibility in trap-building predators: a review. Biol Rev 86:626–639PubMedCrossRefGoogle Scholar
  70. Sih A, Bell AM, Johnson JC, Ziemba RE (2004) Behavioral syndromes: an integrative overview. Q Rev Biol 79:241–277PubMedCrossRefGoogle Scholar
  71. Simon D (1988) Ant-lions (Neuroptera: Myrmeleontidae) of the coastal plain: systematical, ecological, and zoogeographical aspects with emphasis on the coexistence of a species guild of the unstable dunes. Ph.D. thesis, Tel-Aviv University, IsraelGoogle Scholar
  72. Smith MJ, Hunter D (2005) Temporal and geographic variation in the advertisement call of the booroolong frog (Litoria booroolongensis: Anura: Hylidae). Ethology 111:1103–1115CrossRefGoogle Scholar
  73. Sogavker U (2004) The relationship between productivity and ant-species richness at regional and local scales. M.Sc. thesis, Ben-Gurion University of the Negev, IsraelGoogle Scholar
  74. Stillwell RC (2010) Are latitudinal clines in body size adaptive? Oikos 119:1387–1390CrossRefGoogle Scholar
  75. Tabachnick B, Fidell L (2007) Using multivariate statistics, 5th edn. Pearson, BostonGoogle Scholar
  76. Whitlock MC, Phillips PC, Fowler K (2002) Persistence of changes in the genetic covariance matrix after a bottleneck. Evolution 56:1968–1975PubMedCrossRefGoogle Scholar
  77. Wilson DS (1998) Adaptive individual differences within single populations. Philos Trans R Soc Lond B Biol Sci 353:199–205PubMedCentralCrossRefGoogle Scholar
  78. Wilson AD, Whattam EM, Bennett R, Visanuvimol L, Lauzon C, Bertram SM (2010) Behavioral correlations across activity, mating, exploration, aggression, and antipredator contexts in the European house cricket, Acheta domesticus. Behav Ecol Sociobiol 64:703–715CrossRefGoogle Scholar
  79. Wolf M, Weissing FJ (2010) An explanatory framework for adaptive personality differences. Philos Trans R Soc Lond B Biol Sci 365:3959–3968PubMedCentralPubMedCrossRefGoogle Scholar
  80. Zar JH (1999) Biostatistical analysis, 4th edn. Prentice Hall, New JerseyGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  1. 1.Department of Life Sciences, Faculty of Natural SciencesBen-Gurion University of the NegevBeer-ShevaIsrael
  2. 2.Department of Zoology, Faculty of Life SciencesTel Aviv UniversityTel AvivIsrael

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