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Oecologia

pp 1–12 | Cite as

Habitat structure changes the relationships between predator behavior, prey behavior, and prey survival rates

  • James L. L. LichtensteinEmail author
  • Karis A. Daniel
  • Joanna B. Wong
  • Colin M. Wright
  • Grant Navid Doering
  • Raul Costa-Pereira
  • Jonathan N. Pruitt
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Abstract

The individual behavioral traits of predators and prey sometimes determine the outcome of their interactions. Here, we examine whether changes to habitat complexity alter the effects of predator and prey behavior on their survival rates. Specifically, we test whether behavioral traits (activity level, boldness, and perch height) measured in predators and prey or multivariate behavioral volumes best predict the survival rates of both trophic levels in staged mesocosms with contrasting structural complexity. Behavioral volumes and hypervolumes are a composite group-level behavioral diversity metric built from the individual-level behavioral traits we measured in predators and prey. We stocked mesocosms with a host plant and groups of cannibalistic predators (n = 5 mantises/mesocosm) and their prey (n = 15 katydids/mesocosm), and mesocosms varied in the presence/absence of additional non-living climbing structures. We found that mantis survival rates were unrelated to any behavioral metric considered here, but were higher in structurally complex mesocosms. Unexpectedly, katydids were more likely to survive when mantis groups occupied larger behavioral volumes, indicating that more behaviorally diverse predator groups are less lethal. Katydid mortality was also increased when both predators and prey exhibited higher average perch heights, but this effect was increased by the addition of supplemental structure. This is consistent with the expectation that structural complexity increases the effect of intraspecific behavioral variation on prey survival rates. Collectively, these results convey that the effects of predator and prey behavior on prey survival could depend highly on the environment in which they are evaluated.

Keywords

Hypervolumes Temperament Behavioral syndromes Mantidae Tettigoniidae 

Notes

Acknowledgements

Funding for this research was provided by the University of California (Santa Barbara), National Science Foundation grant awards to JNP (1352705 and 1455895), and a National Institutes of Health grant awarded to JNP (R01GM115509). We also thank the Pymatuning Laboratory of Ecology of the University of Pittsburgh for hosting our research. Particularly we thank Dr. Cori Richards-Zawacki and Chris Davis for helping navigate the process of working at a research institution not affiliated with our own.

Author contribution statement

JLLL designed the experiment, collected data, and wrote the manuscript. KAD and JBW contributed to data collection and writing. GND calculated behavioral volumes and contributed to writing. RCP performed path analyses and contributed to writing. CMW and JNP helped with experimental design and writing. All authors approved the manuscript in its current form.

Supplementary material

442_2019_4344_MOESM1_ESM.docx (85 kb)
Supplementary material 1 (docx 85 kb)

References

  1. Akaike H (1987) Factor analysis and AIC. Psychometrika 52:317–332Google Scholar
  2. Amarasinghe M, Balasubramaniam S (1992) Structural properties of two types of mangrove stands on the northwestern coast of Sri Lanka. Ecol Mangrove Relat Ecosyst 247:17–27Google Scholar
  3. Attrill MJ, Strong JA, Rowden AA (2000) Are macroinvertebrate communities influenced by seagrass structural complexity? Ecography 23:114–121Google Scholar
  4. Ballew NG, Mittelbach GG, Scribner KT (2017) Fitness consequences of boldness in juvenile and adult largemouth bass. Am Nat 189:396–406Google Scholar
  5. Boyer N, Réale D, Marmet J, Pisanu B, Chapuis JL (2010) Personality, space use and tick load in an introduced population of Siberian chipmunks Tamias sibiricus. J Anim Ecol 79:538–547Google Scholar
  6. Burnham KP, Anderson DR (2003) Model selection and multimodel inference: a practical information-theoretic approach. Springer, BerlinGoogle Scholar
  7. Chang CC, Teo HY, Norma-Rashid Y, Li D (2017) Predator personality and prey behavioural predictability jointly determine foraging performance. Scie Rep 7:40734Google Scholar
  8. Connell JH (1970) A predator–prey system in the marine intertidal region. I. Balanus glandula and several predatory species of Thais. Ecol Monogr 40:49–78Google Scholar
  9. Cook W, Streams F (1984) Fish predation on Notonecta (Hemiptera): relationship between prey risk and habitat utilization. Oecologia 64:177–183Google Scholar
  10. Crowder LB, Cooper WE (1982) Habitat structural complexity and the interaction between bluegills and their prey. Ecology 63:1802–1813Google Scholar
  11. Cushing JM, Saleem M (1982) A predator prey model with age structure. J Math Biol 14:231–250Google Scholar
  12. Dall SR, Houston AI, McNamara JM (2004) The behavioural ecology of personality: consistent individual differences from an adaptive perspective. Ecol Lett 7:734–739Google Scholar
  13. Diehl S (1992) Fish predation and benthic community structure: the role of omnivory and habitat complexity. Ecology 73:1646–1661Google Scholar
  14. Dingemanse NJ, Both C, Drent PJ, van Oers K, van Noordwijk AJ (2002) Repeatability and heritability of exploratory behaviour in great tits from the wild. Anim Behav 64:929–938Google Scholar
  15. DiRienzo N, Pruitt JN, Hedrick AV (2013) The combined behavioural tendencies of predator and prey mediate the outcome of their interaction. Anim Behav 86:317–322Google Scholar
  16. Eldakar OT, Dlugos MJ, Wilcox RS, Wilson DS (2009) Aggressive mating as a tragedy of the commons in the water strider Aquarius remigis. Behav Ecol Sociobiol 64:25Google Scholar
  17. Finke DL, Snyder WE (2008) Niche partitioning increases resource exploitation by diverse communities. Science 321:1488–1490Google Scholar
  18. Fisher DN, David M, Tregenza T, Rodríguez-Muñoz R (2015) Dynamics of among-individual behavioral variation over adult lifespan in a wild insect. Behav Ecol 26:975–985Google Scholar
  19. Griffen BD, Toscano BJ, Gatto J (2012) The role of individual behavior type in mediating indirect interactions. Ecology 93:1935–1943Google Scholar
  20. Hedrick AV, Kortet R (2012) Sex differences in the repeatability of boldness over metamorphosis. Behav Ecol Sociobiol 66:407–412Google Scholar
  21. Hironori Y, Katsuhiro S (1997) Cannibalism and interspecific predation in two predatory ladybirds in relation to prey abundance in the field. Biocontrol 42:153–163Google Scholar
  22. Hulthén K, Chapman BB, Nilsson PA, Hollander J, Brönmark C (2014) Express yourself: bold individuals induce enhanced morphological defences. Proc R Soc Lond B Biol Sci 281:20132703Google Scholar
  23. Hurd L, Eisenberg R (1984a) Experimental density manipulations of the predator Tenodera sinensis (Orthoptera: Mantidae) in an old-field community. II. The influence of mantids on arthropod community structure. J Anim Ecol 53:955–967Google Scholar
  24. Hurd L, Eisenberg RM (1984b) Experimental density manipulations of the predator Tenodera sinensis (Orthoptera: Mantidae) in an old-field community. I. Mortality, development and dispersal of juvenile mantids. J Anim Ecol 53:269–281Google Scholar
  25. Hurd L, Eisenberg RM (1990) Arthropod community responses to manipulation of a bitrophic predator guild. Ecology 71:2107–2114Google Scholar
  26. Jakob EM, Marshall SD, Uetz GW (1996) Estimating fitness: a comparison of body condition indices. Oikos 77:61–67Google Scholar
  27. Jones C, DiRienzo N (2018) Behavioral variation post-invasion: resemblance in some, but not all, behavioral patterns among invasive and native praying mantids. Behav Process 153:92–99Google Scholar
  28. 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 9:225–232Google Scholar
  29. Keiser CN, Ingley SJ, Toscano BJ, Scharf I, Pruitt JN (2017) Habitat complexity dampens selection on prey activity level. Ethology 124:25–32Google Scholar
  30. Kurvers RH et al (2009) Personality differences explain leadership in barnacle geese. Anim Behav 78:447–453Google Scholar
  31. Lichtenstein JL, Chism GT, Kamath A, Pruitt JN (2017a) Intraindividual behavioral variability predicts foraging outcome in a beach-dwelling jumping spider. Sci Rep 7:18063Google Scholar
  32. Lichtenstein JL, Wright CM, McEwen B, Pinter-Wollman N, Pruitt JN (2017b) The multidimensional behavioural hypervolumes of two interacting species predict their space use and survival. Anim Behav 132:129–136Google Scholar
  33. Lichtenstein JL, Rice HK, Pruitt JN (2018) Personality variation in two predator species does not impact prey species survival or plant damage in staged mesocosms. Behav Ecol Sociobiol 72:70Google Scholar
  34. McDonnell MJ, Stiles EW (1983) The structural complexity of old field vegetation and the recruitment of bird-dispersed plant species. Oecologia 56:109–116Google Scholar
  35. McElhinny C, Gibbons P, Brack C, Bauhus J (2005) Forest and woodland stand structural complexity: its definition and measurement. For Ecol Manag 218:1–24Google Scholar
  36. McGhee KE, Pintor LM, Suhr EL, Bell AM (2012) Maternal exposure to predation risk decreases offspring antipredator behaviour and survival in threespined stickleback. Funct Ecol 26:932–940Google Scholar
  37. Moran V (1980) Interactions between phytophagous insects and their Opuntia hosts. Ecol Entomol 5:153–164Google Scholar
  38. Moran MD, Hurd L (1997) A trophic cascade in a diverse arthropod community caused by a generalist arthropod predator. Oecologia 113:126–132Google Scholar
  39. Moran MD, Rooney TP, Hurd L (1996) Top-down cascade from a bitrophic predator in an old-field community. Ecology 77:2219–2227Google Scholar
  40. Müller T, Müller C (2015) Behavioural phenotypes over the lifetime of a holometabolous insect. Front Zool 12:S8Google Scholar
  41. Nakagawa S, Schielzeth H (2013) A general and simple method for obtaining R2 from generalized linear mixed-effects models. Methods Ecol Evol 4:133–142Google Scholar
  42. Niemelä PT, Vainikka A, Hedrick AV, Kortet R (2012) Integrating behaviour with life history: boldness of the field cricket, Gryllus integer, during ontogeny. Funct Ecol 26:450–456Google Scholar
  43. Pearish S, Hostert L, Bell AM (2013) Behavioral type—environment correlations in the field: a study of three-spined stickleback. Behav Ecol Sociobiol 67:765–774Google Scholar
  44. Polis GA, Myers CA, Holt RD (1989) The ecology and evolution of intraguild predation: potential competitors that eat each other. Annu Rev Ecol Syst 20:297–330Google Scholar
  45. Preisser EL, Orrock JL, Schmitz OJ (2007) Predator hunting mode and habitat domain alter nonconsumptive effects in predator–prey interactions. Ecology 88:2744–2751Google Scholar
  46. Prete FR, Hurd LE, Wells PH (1999) The praying mantids. JHU Press, BaltimoreGoogle Scholar
  47. Pruitt JN, Ferrari MC (2011) Intraspecific trait variants determine the nature of interspecific interactions in a habitat-forming species. Ecology 92:1902–1908Google Scholar
  48. Pruitt JN, Bolnick DI, Sih A, DiRienzo N, Pinter-Wollman N (2016) Behavioural hypervolumes of spider communities predict community performance and disbandment. Proc R Soc B 283:20161409Google Scholar
  49. Pruitt JN et al (2017) Behavioral hypervolumes of predator groups and predator-predator interactions shape prey survival rates and selection on prey behavior. Am Nat 189:254–266Google Scholar
  50. Qin J, Fast AW (1996) Size and feed dependent cannibalism with juvenile snakehead Channa striatus. Aquaculture 144:313–320Google Scholar
  51. Rosseel Y (2012) Lavaan: an R package for structural equation modeling and more. Version 0.5–12 (BETA). J Stat Softw 48:1–36Google Scholar
  52. Royauté R, Pruitt JN (2015) Varying predator personalities generates contrasting prey communities in an agroecosystem. Ecology 96:2902–2911Google Scholar
  53. Schmitz OJ (2007) Predator diversity and trophic interactions. Ecology 88:2415–2426Google Scholar
  54. Sih A, Watters JV (2005) The mix matters: behavioural types and group dynamics in water striders. Behaviour 142:1417–1431Google Scholar
  55. Sih A, Englund G, Wooster D (1998) Emergent impacts of multiple predators on prey. Trends Ecol Evol 13:350–355Google Scholar
  56. Sih A, Kats LB, Maurer EF (2003) Behavioural correlations across situations and the evolution of antipredator behaviour in a sunfish–salamander system. Anim Behav 65:29–44Google Scholar
  57. Sih A, Bell A, Johnson JC (2004) Behavioral syndromes: an ecological and evolutionary overview. Trends Ecol Evol 19:372–378Google Scholar
  58. Sih A, Cote J, Evans M, Fogarty S, Pruitt J (2012) Ecological implications of behavioural syndromes. Ecol Lett 15:278–289Google Scholar
  59. Smith BR, Blumstein DT (2008) Fitness consequences of personality: a meta-analysis. Behav Ecol 19:448–455Google Scholar
  60. Soluk DA (1993) Multiple predator effects: predicting combined functional response of stream fish and invertebrate predators. Ecology 74:219–225Google Scholar
  61. Southwood TR, Brown V, Reader P (1979) The relationships of plant and insect diversities in succession. Biol J Lin Soc 12:327–348Google Scholar
  62. Spiegel O, Leu ST, Sih A, Godfrey SS, Bull CM (2015) When the going gets tough: behavioural type-dependent space use in the sleepy lizard changes as the season dries. Proc R Soc B 282:20151768Google Scholar
  63. Sugihara G, May RM (1990) Applications of fractals in ecology. Trends Ecol Evol 5:79–86Google Scholar
  64. Sweeney K, Cusack B, Armagost F, O’Brien T, Keiser CN, Pruitt JN (2013) Predator and prey activity levels jointly influence the outcome of long-term foraging bouts. Behav Ecol 24:1205–1210Google Scholar
  65. Thompson D (1975) Towards a predator-prey model incorporating age structure: the effects of predator and prey size on the predation of Daphnia magna by Ischnura elegans. J Anim Ecol 44:907–916Google Scholar
  66. Toscano BJ, Griffen BD (2014) Trait-mediated functional responses: predator behavioural type mediates prey consumption. J Anim Ecol 83:1469–1477Google Scholar
  67. 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 182:1–15Google Scholar
  68. Uetz G (1991) Habitat structure and spider foraging. Habitat structure. Springer, Berlin, pp 325–348Google Scholar
  69. Vince S, Valiela I, Backus N, Teal J (1976) Predation by the salt marsh killifish Fundulus heteroclitus (L.) in relation to prey size and habitat structure: consequences for prey distribution and abundance. J Exp Mar Biol Ecol 23:255–266Google Scholar
  70. Wilson AD, McLaughlin RL (2007) Behavioural syndromes in brook charr, Salvelinus fontinalis: prey-search in the field corresponds with space use in novel laboratory situations. Anim Behav 74:689–698Google Scholar
  71. 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 107:250Google Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Department of Ecology, Evolution, and Marine BiologyUniversity of California Santa BarbaraSanta BarbaraUSA
  2. 2.Department of BiologyWilson CollegeChambersburgUSA
  3. 3.Department of BiologyDalhousie UniversityHalifaxCanada
  4. 4.Department of EcologySão Paolo State UniversitySão PaoloBrazil

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