Personality variation in two predator species does not impact prey species survival or plant damage in staged mesocosms

  • James L. L. Lichtenstein
  • Henry K. Rice
  • Jonathan N. Pruitt
Original Article

Abstract

Mounting evidence suggests that consistent individual differences in behavior, better known as animal personality, can shape aspects of population and community ecology. Yet, the potential for animal personality to affect more complex and non-linear food webs, like those seen in nature, remains understudied. Here, we explore the degree to which the aggregate behaviors of two predator species simultaneously interact to alter prey survival rates and the presence and magnitude of trophic cascades. We set up mesocosms in an old-field habitat containing four different insect prey species and either two Phidippus clarus (Salticidae), two Platycryptus undatus (Salticidae), or one of each predator. Prior to initiating each mesocosm, we assayed the activity level and boldness of each individual predator and included these metrics in our models predicting prey survival and plant damage. We then compared the number of surviving prey and plant damage under each of these conditions and tested for associations between each of these response variables and predator behavior. We found no significant effect of predator community composition or predators’ behavior on prey survival or plant damage. These results suggest that the effects of predator personality on prey survival may be subtle or absent in complex species interaction modules.

Significance statement

Although much research suggests that animal personality can influence broader scale ecological phenomena, the ability of animal personality to alter complex species interaction modules remains unresolved. We tested whether pairs of predators of different personality types differentially impacted prey survival rates and plant damage in a tritrophic system, and whether these effects varied based on predator community composition. We recovered no evidence that predator personality types influenced prey survival or plant damage regardless of the predator composition considered. These results suggest that the effects of personality may be absent or undetectable in more complex, realistic ecological settings. The majority of laboratory-based personality studies published to date evaluate only dyadic species interactions in simplified environments. Our findings therefore raise concerns that such studies are prone to overestimate the effects of animal personality.

Keywords

Indirect effects Personality Salticidae Temperament Trophic cascades 

Notes

Acknowledgements

We thank the University of Pittsburgh and the Pymatuning Laboratory of Ecology for providing space and materials for our studies. Finally, we would like to thank two anonymous reviewers whose comments were helpful in improving the quality of this paper.

Funding information

This study received financial support from the Pape and McKinley grants from the University of Pittsburgh’s Pymatuning Laboratory of Ecology.

References

  1. Belgrad BA, Griffen BD (2016) Predator–prey interactions mediated by prey personality and predator hunting mode. In: Proc R Soc B. The Royal Society, pp 20160408Google Scholar
  2. Bell AM, Sih A (2007) Exposure to predation generates personality in threespined sticklebacks (Gasterosteus aculeatus). Ecol Lett 10:828–834CrossRefPubMedGoogle Scholar
  3. Bell AM, Hankison SJ, Laskowski KL (2009) The repeatability of behaviour: a meta-analysis. Animal Behaviour 77(4):771-783Google Scholar
  4. Brown C, Jones F, Braithwaite V (2005) In situ examination of boldness–shyness traits in the tropical poeciliid, Brachyraphis episcopi. Anim Behav 70:1003–1009CrossRefGoogle Scholar
  5. Byrnes J, Stachowicz JJ, Hultgren KM, Randall Hughes A, Olyarnik SV, Thornber CS (2006) Predator diversity strengthens trophic cascades in kelp forests by modifying herbivore behaviour. Ecol Lett 9:61–71PubMedGoogle Scholar
  6. Carpenter SR, Kitchell JF, Hodgson JR (1985) Cascading trophic interactions and lake productivity. Bioscience 35:634–639CrossRefGoogle Scholar
  7. Carter AJ, Marshall HH, Heinsohn R, Cowlishaw G (2012) How not to measure boldness: novel object and antipredator responses are not the same in wild baboons. Anim Behav 84:603–609CrossRefGoogle Scholar
  8. Carter AJ, Feeney WE, Marshall HH, Cowlishaw G, Heinsohn R (2013) Animal personality: what are behavioural ecologists measuring? Biol Rev 88:465–475CrossRefPubMedGoogle Scholar
  9. Dingemanse NJ, Dochtermann NA (2013) Quantifying individual variation in behaviour: mixed-effect modelling approaches. J Anim Ecol 82:39–54CrossRefPubMedGoogle Scholar
  10. Dingemanse NJ, Dochtermann NA, Nakagawa S (2012) Defining behavioural syndromes and the role of “syndrome” deviation in understanding their evolution. Behav Ecol Sociobiol 66:1543–1548CrossRefGoogle Scholar
  11. DiRienzo N, Pruitt JN, Hedrick AV (2012) Juvenile exposure to acoustic sexual signals from conspecifics alters growth trajectory and an adult personality trait. Anim Behav 84:861–868CrossRefGoogle Scholar
  12. DiRienzo N, Pruitt JN, Hedrick AV (2013) The combined behavioural tendencies of predator and prey mediate the outcome of their interaction. Anim Behav 86:317–322CrossRefGoogle Scholar
  13. Enders F (1975) The influence of hunting manner on prey size, particularly in spiders with long attack distances (Araneidae, Linyphiidae, and Salticidae). Am Nat 109:737–763CrossRefGoogle Scholar
  14. Finke DL, Denno RF (2004) Predator diversity dampens trophic cascades. Nature 429:407–410CrossRefPubMedGoogle Scholar
  15. Finke DL, Denno RF (2005) Predator diversity and the functioning of ecosystems: the role of intraguild predation in dampening trophic cascades. Ecol Lett 8:1299–1306CrossRefGoogle Scholar
  16. Giverns R (1978) Dimorphic foraging strategies of a salticid spider (Phidippus audax). Ecology 59:309–321CrossRefGoogle Scholar
  17. Gosling SD (2001) From mice to men: what can we learn about personality from animal research? Psychol Bull 127:45–86CrossRefPubMedGoogle Scholar
  18. Griffen BD, Toscano BJ, Gatto J (2012) The role of individual behavior type in mediating indirect interactions. Ecology 93:1935–1943CrossRefPubMedGoogle Scholar
  19. Grinsted L, Pruitt JN, Settepani V, Bilde T (2013) Individual personalities shape task differentiation in a social spider. Proc R Soc Lond B Biol Sci 280:20131407CrossRefGoogle Scholar
  20. Hairston NG, Smith FE, Slobodkin LB (1960) Community structure, population control, and competition. American naturalist:421–425Google Scholar
  21. Hammerstein P, Riechert SE (1988) Payoffs and strategies in territorial contests: ESS analyses of two ecotypes of the spider Agelenopsis aperta. Evol Ecol 2:115–138CrossRefGoogle Scholar
  22. Hawley J, Simpson SJ, Wilder SM (2014) Effects of prey macronutrient content on body composition and nutrient intake in a web-building spider. PLoS One 9:e99165CrossRefPubMedPubMedCentralGoogle Scholar
  23. Herberstein ME (2011) Spider behaviour: flexibility and versatility. Cambridge University PressGoogle Scholar
  24. Hixon MA, Beets JP (1993) Predation, prey refuges, and the structure of coral-reef fish assemblages. Ecol Monogr 63:77–101CrossRefGoogle Scholar
  25. Hlivko JT, Rypstra AL (2003) Spiders reduce herbivory: nonlethal effects of spiders on the consumption of soybean leaves by beetle pests. Ann Entomol Soc Am 96:914–919CrossRefGoogle Scholar
  26. Hoefler CD, Jakob EM (2006) Jumping spiders in space movements patterns, nest site fidelity, and the use of beacons. Anim Behav 71:109–116CrossRefGoogle Scholar
  27. Hoefler CD, Taylor M, Jakob EM (2002) Chemosensory response to prey cues in Phidippus audax (Araneae, Salticidae) and Pardosa milvina (Araneae, Lycosidae). J Arachnol 30:155–158CrossRefGoogle Scholar
  28. Hoefler CD, Chen A, Jakob EM (2006) The potential of a jumping spider, Phidippus clarus, as a biocontrol agent. J Econ Entomol 99:432–436CrossRefPubMedGoogle Scholar
  29. Jackson R, Blest A (1982) The biology of Portia fimbriata, a web-building jumping spider (Araneae, Salticidae) from Queensland: utilization of webs and predatory versatility. J Zool 196:255–293CrossRefGoogle Scholar
  30. Johnson JC, Sih A (2007) Fear, food, sex and parental care: a syndrome of boldness in the fishing spider,< i> Dolomedes triton</i>. Anim Behav 74:1131–1138CrossRefGoogle Scholar
  31. Keiser CN, Pruitt JN (2013) Spider aggressiveness determines the bidirectional consequences of host–inquiline interactions. Behav Ecol :art096Google Scholar
  32. Keiser CN, Slyder JB, Carson WP, Pruitt JN (2015) Individual differences in predators but not producers mediate the magnitude of a trophic cascade. Arthropod Plant Interact 9:225–232CrossRefGoogle Scholar
  33. Lichtenstein JL, Pruitt JN, Modlmeier AP (2015) Intraspecific variation in collective behaviors drives interspecific contests in acorn ants. Behav Ecol :arv188Google Scholar
  34. Lucas É, Coderre D, Brodeur J (1998) Intraguild predation among aphid predators: characterization and influence of extraguild prey density. Ecology 79:1084–1092CrossRefGoogle Scholar
  35. Maupin JL, Riechert SE (2001) Superfluous killing in spiders: a consequence of adaptation to food-limited environments? Behav Ecol 12:569–576CrossRefGoogle Scholar
  36. McGhee KE, Pintor LM, Bell AM (2013) Reciprocal behavioral plasticity and behavioral types during predator-prey interactions. Am Nat 182:704–717CrossRefPubMedPubMedCentralGoogle Scholar
  37. Menge BA (1995) Indirect effects in marine rocky intertidal interaction webs: patterns and importance. Ecol Monogr 65:21–74CrossRefGoogle Scholar
  38. Modlmeier AP, Keiser CN, Wright CM, Lichtenstein JL, Pruitt JN (2015) Integrating animal personality into insect population and community ecology. Curr Opin Insect SciGoogle Scholar
  39. Moran MD, Rooney TP, Hurd L (1996) Top-down cascade from a bitrophic predator in an old-field community. Ecology 77:2219–2227CrossRefGoogle Scholar
  40. Niemelä PT, Lattenkamp EZ, Dingemanse NJ (2015) Personality-related survival and sampling bias in wild cricket nymphs. Behav Ecol 26:936–946CrossRefGoogle Scholar
  41. Persons MH, Walker SE, Rypstra AL (2002) Fitness costs and benefits of antipredator behavior mediated by chemotactile cues in the wolf spider Pardosa milvina (Araneae: Lycosidae). Behav Ecol 13:386–392CrossRefGoogle Scholar
  42. Pruitt JN, Ferrari MC (2011) Intraspecific trait variants determine the nature of interspecific interactions in a habitat-forming species. Ecology 92:1902–1908CrossRefPubMedGoogle Scholar
  43. Pruitt JN, Keiser CN (2014) The personality types of key catalytic individuals shape colonies’ collective behaviour and success. Anim Behav 93:87–95CrossRefGoogle Scholar
  44. Pruitt JN, Riechert SE, Jones TC (2008) Behavioural syndromes and their fitness consequences in a socially polymorphic spider, Anelosimus studiosus. Anim Behav 76:871–879CrossRefGoogle Scholar
  45. Pruitt JN, Stachowicz JJ, Sih A (2012) Behavioral types of predator and prey jointly determine prey survival: potential implications for the maintenance of within-species behavioral variation. Am Nat 179:217–227CrossRefPubMedGoogle Scholar
  46. Riechert SE, Hedrick AV (1993) A test for correlations among fitness-linked behavioural traits in the spider Agelenopsis aperta (Araneae, Agelenidae). Anim Behav 46:669–675CrossRefGoogle Scholar
  47. Rosenheim JA, Wilhoit LR, Armer CA (1993) Influence of intraguild predation among generalist insect predators on the suppression of an herbivore population. Oecologia 96:439–449CrossRefPubMedGoogle Scholar
  48. Rothley KD, Schmitz OJ, Cohon JL (1997) Foraging to balance conflicting demands: novel insights from grasshoppers under predation risk. Behav Ecol 8:551–559CrossRefGoogle Scholar
  49. Royauté R, Pruitt JN (2015) Varying predator personalities generates contrasting prey communities in an agroecosystem. Ecology 96:2902–2911CrossRefPubMedGoogle Scholar
  50. Schmidt J, Harwood J, Rypstra A (2012) Foraging activity of a dominant epigeal predator: molecular evidence for the effect of prey density on consumption. Oikos 121:1715–1724CrossRefGoogle Scholar
  51. Schmitz OJ (1998) Direct and indirect effects of predation and predation risk in old-field interaction webs. Am Nat 151:327–342PubMedGoogle Scholar
  52. Schmitz OJ (2008) Effects of predator hunting mode on grassland ecosystem function. Science 319:952–954CrossRefPubMedGoogle Scholar
  53. Schmitz OJ, Krivan V, Ovadia O (2004) Trophic cascades: the primacy of trait-mediated indirect interactions. Ecol Lett 7:153–163CrossRefGoogle Scholar
  54. Sih A, Englund G, Wooster D (1998) Emergent impacts of multiple predators on prey. Trends Ecol Evol 13:350–355CrossRefPubMedGoogle Scholar
  55. Sih A, Bell A, Johnson JC (2004) Behavioral syndromes: an ecological and evolutionary overview. Trends Ecol Evol 19:372–378CrossRefPubMedGoogle Scholar
  56. Sih A, Cote J, Evans M, Fogarty S, Pruitt J (2012) Ecological implications of behavioural syndromes. Ecol Lett 15:278–289CrossRefPubMedGoogle Scholar
  57. Simpson SJ, Clissold FJ, Lihoreau M, Ponton F, Wilder SM, Raubenheimer D (2015) Recent advances in the integrative nutrition of arthropods. Annu Rev Entomol 60:293–311CrossRefPubMedGoogle Scholar
  58. Skow CD, Jakob EM (2006) Jumping siders attend to context during learned avoidance of aposematic prey. Behav Ecol 17:34–40CrossRefGoogle Scholar
  59. Snyder WE, Wise DH (2000) Antipredator behavior of spotted cucumber beetles (Coleoptera: Chrysomelidae) in response to predators that pose varying risks. Environ Entomol 29:35–42CrossRefGoogle Scholar
  60. Soluk DA (1993) Multiple predator effects: predicting combined functional response of stream fish and invertebrate predators. Ecology :219–225Google Scholar
  61. Strauss SY (1991) Indirect effects in community ecology: their definition, study and importance. Trends Ecol Evol 6:206–210CrossRefPubMedGoogle Scholar
  62. Sweeney K, Gadd RD, Hess ZL, McDermott DR, MacDonald L, Cotter P, Armagost F, Chen JZ, Berning AW, DiRienzo N (2013) Assessing the effects of rearing environment, natural selection, and developmental stage on the emergence of a behavioral syndrome. Ethology 119:436–447CrossRefGoogle Scholar
  63. Taylor LA, Amin Z, Maiar EB, Byrnes KJ, Morehouse NI (2015) Flexible color learning in an invertebrate predator: Habronattus jumpong spiders can learn to preder or avoid red during foraging. Behav Ecol 27:520–529CrossRefGoogle Scholar
  64. Toscano BJ, Griffen BD (2014) Trait-mediated functional responses: predator behavioural type mediates prey consumption. J Anim Ecol 83:1469–1477CrossRefPubMedGoogle Scholar
  65. Toscano BJ, Gownaris NJ, Heerhartz SM, Monaco CJ (2016) Personality, foraging behavior and specialization: integrating behavioral and food web ecology at the individual level. Oecologia:1–15Google Scholar
  66. Webster M, Ward A, Hart P (2009) Individual boldness affects interspecific interactions in sticklebacks. Behav Ecol Sociobiol 63:511–520CrossRefGoogle Scholar
  67. Wolf M, Weissing FJ (2012) Animal personalities: consequences for ecology and evolution. Trends Ecol Evol 27:452–461CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • James L. L. Lichtenstein
    • 1
  • Henry K. Rice
    • 2
  • Jonathan N. Pruitt
    • 1
  1. 1.Department of Ecology, Evolution and Marine BiologyUC Santa BarbaraSanta BarbaraUSA
  2. 2.Department of Biological SciencesUniversity of PittsburghPittsburghUSA

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