An updated perspective on spiders as generalist predators in biological control

Abstract

The role of generalist predators in biological control remains controversial as they may not only reduce pest populations but also disrupt biocontrol exerted by other natural enemies. Here, we focus on spiders as a model group of generalist predators. They are among the most abundant and most diverse natural enemies in agroecosystems. We review their functional traits that influence food-web dynamics and pest suppression at organisational levels ranging from individuals to communities. At the individual and population levels, we focus on hunting strategy, body size, life stage, nutritional target, and personality (i.e., consistent inter-individual differences in behaviour). These functional traits determine the spider trophic niches. We also focus on the functional and numerical response to pest densities and on non-consumptive effects of spiders on pests. At the community level, we review multiple-predator effects and effect of alternative prey on pest suppression. Evidence for a key role of spiders in pest suppression is accumulating. Importantly, recent research has highlighted widespread non-consumptive effects and complex intraguild interactions of spiders. A better understanding of these effects is needed to optimize biocontrol services by spiders in agroecosystems.

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References

  1. Abrams PA, Cortez MH (2015) The many potential indirect interactions between predators that share competing prey. Ecol Monogr 85:625–641. https://doi.org/10.1890/14-2025.1

    Article  Google Scholar 

  2. Agustí N, Shayler SP, Harwood JD, Vaughan IP, Sunderland KD, Symondson WOC (2003) Collembola as alternative prey sustaining spiders in arable ecosystems: prey detection within predators using molecular markers. Mol Ecol 12:3467–3475. https://doi.org/10.1046/j.1365-294X.2003.02014.x

    CAS  Article  PubMed  Google Scholar 

  3. Amarasekare P (2008) Coexistence of intraguild predators and prey in resource-rich environments. Ecology 89:2786–2797. https://doi.org/10.1890/07-1508.1

    Article  PubMed  Google Scholar 

  4. Araújo MS, Bolnick DI, Layman CA (2011) The ecological causes of individual specialisation. Ecol Lett 14:948–958. https://doi.org/10.1111/j.1461-0248.2011.01662.x

    Article  PubMed  Google Scholar 

  5. Baba YG, Tanaka K (2016) Environmentally friendly farming and multi-scale environmental factors influence generalist predator community in rice paddy ecosystems of Japan. NIEAS Ser 6:171–179

    Google Scholar 

  6. Bartos M (2011) Partial dietary separation between coexisting cohorts of Yllenus arenarius (Araneae: Salticidae). J Arachnol 39:230–235. https://doi.org/10.1636/CP10-63.1

    Article  Google Scholar 

  7. Beleznai O, Tholt G, Tóth Z, Horváth V, Marczali Z, Samu F (2015) Cool headed individuals are better survivors: non-consumptive and consumptive effects of a generalist predator on a sap feeding insect. PLoS One 10:e0135954. https://doi.org/10.1371/journal.pone.0135954

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  8. Beleznai O, Dreyer J, Tóth Z, Samu F (2017) Natural enemies partially compensate for warming induced excess herbivory in an organic growth system. Sci Rep 7:7226. https://doi.org/10.1038/s41598-017-07509-w

    CAS  Article  Google Scholar 

  9. Bell JR, Wheater CP, Cullen WR (2001) The implications of grassland and heathland management for the conservation of spider communities: a review. J Zool 255:377–387. https://doi.org/10.1017/S0952836901001479

    Article  Google Scholar 

  10. Bell AM, Hankison SJ, Laskowski KL (2009) The repeatability of behaviour: a meta-analysis. Anim Behav 77:771–783. https://doi.org/10.1016/j.anbehav.2008.12.022

    Article  PubMed  PubMed Central  Google Scholar 

  11. Benamú MA, Lacava M, García LF, Santana M, Viera C (2017) Spiders Associated with Agroecosystems: Roles and Perspectives. In: Viera C, Gonzaga M (eds) Behaviour and ecology of spiders. Springer, Cham. https://doi.org/10.1007/978-3-319-65717-2_11

    Google Scholar 

  12. Binz H, Bucher R, Entling MH, Menzel F (2014) Knowing the risk: crickets distinguish between spider predators of different size and commonness. Ethology 120:99–110. https://doi.org/10.1111/eth.12183

    Article  Google Scholar 

  13. Birkhofer K, Wolters V (2012) The global relationship between climate net primary production and the diet of spiders. Glob Ecol Biogeogr 21:100–108. https://doi.org/10.1111/j.1466-8238.2011.00654.x

    Article  Google Scholar 

  14. Birkhofer K, Gavish-Regev E, Endlweber K, Lubin YD, von Berg K, Wise DH, Scheu S (2008a) Cursorial spiders retard initial aphid population growth at low densities in winter wheat. Bull Entomol Res 98:249–255. https://doi.org/10.1017/S0007485308006019

    CAS  Article  PubMed  Google Scholar 

  15. Birkhofer K, Wise DH, Scheu S (2008b) Subsidy from the detrital food web but not microhabitat complexity affects the role of generalist predators in an aboveground herbivore food web. Oikos 117:494–500. https://doi.org/10.1111/j.0030-1299.2008.16361.x

    Article  Google Scholar 

  16. Birkhofer K, Entling MH, Lubin Y (2013) Agroecology: trait composition spatial relationships trophic interactions. In: Penney D (ed) Spider Research in the 21st Century: Trends and Perspectives. SIRI Scientific Press, Manchester, pp 220–228

    Google Scholar 

  17. Birkhofer K, Fevrier V, Heinrich AE, Rink K, Smith HG (2018) The contribution of CAP greening measures to conservation biological control at two spatial scales. Agric Ecosyst Environ 255:84–94. https://doi.org/10.1016/j.agee.2017.12.026

    Article  Google Scholar 

  18. Bolnick DI, Amarasekare P, Araújo MS, Bürger R, Levine JM, Novak M, Rudolf VHW, Schreiber SJ, Urban MC, Vasseur DA (2011) Why intraspecific trait variation matters in community ecology. Trends Ecol Evol 26:183–192. https://doi.org/10.1016/j.tree.2011.01.009

    Article  PubMed  PubMed Central  Google Scholar 

  19. Bommarco R, Miranda F, Bžund H, Björkman C (2011) Insecticides suppress natural enemies and increase pest damage in cabbage. J Econ Entomol 104:782–791. https://doi.org/10.1603/EC10444

    CAS  Article  PubMed  Google Scholar 

  20. Bressendorff BB, Toft S (2011) Dome-shaped functional response induced by nutrient imbalance of the prey. Biol Lett 7:517–520. https://doi.org/10.1098/rsbl.2011.0103

    Article  PubMed  PubMed Central  Google Scholar 

  21. Bucher R, Binz H, Menzel F, Entling MH (2014a) Effects of spider chemotactile cues on arthropod behavior. J Insect Behav 27:567–580. https://doi.org/10.1007/s10905-014-9449-1

    Article  Google Scholar 

  22. Bucher R, Binz H, Menzel F, Entling MH (2014b) Spider cues stimulate feeding weight gain and survival of crickets. Ecol Entomol 39:667–673. https://doi.org/10.1111/een.12131

    Article  Google Scholar 

  23. Bucher R, Heinrich H, Entling MH (2015a) Plant choice herbivory and weight gain of wood crickets under the risk of predation. Entomol Exp Appl 155:148–153. https://doi.org/10.1111/eea.12291

    Article  Google Scholar 

  24. Bucher R, Menzel F, Entling MH (2015b) Risk of spider predation alters food web structure and reduces local herbivory in the field. Oecologia 178:571–577. https://doi.org/10.1007/s00442-015-3226-5

    Article  PubMed  Google Scholar 

  25. Cardoso P, Pekár S, Jocqué R, Coddington JA (2011) Global patterns of guild composition and functional diversity of spiders. PLoS One 6:e21710. https://doi.org/10.1371/journal.pone.0021710

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  26. Chapman EG, Schmidt JM, Welch KD, Harwood JD (2013) Molecular evidence for dietary selectivity and pest suppression potential in an epigeal spider community in winter wheat. Biol Control 65:72–86. https://doi.org/10.1016/j.biocontrol.2012.08.005

    CAS  Article  Google Scholar 

  27. Chen B, Wise DH (1999) Bottom-up limitation of predaceous arthropods in a detritus-based terrestrial food web. Ecology 80:761–772. https://doi.org/10.1890/0012-9658(1999)080%5b0761:BULOPA%5d2.0.CO;2

    Article  Google Scholar 

  28. Cronin JT, Haynes KJ, Dillemuth F (2004) Spider effects on planthopper mortality dispersal and spatial population dynamics. Ecology 85:2134–2143. https://doi.org/10.1890/03-0591

    Article  Google Scholar 

  29. Decae AE (1987) Dispersal: ballooning and other mechanisms. In: Nentwig W (ed) Ecophysiology of spiders. Springer-Verlag, Berlin, pp 357–370

    Google Scholar 

  30. Dell AI, Pawar S, Savage VM (2014) Temperature dependence of trophic interactions are driven by asymmetry of species responses and foraging strategy. J Anim Ecol 83:70–84. https://doi.org/10.1111/1365-2656.12081

    Article  PubMed  Google Scholar 

  31. Denno RF, Gratton C, Döbel H, Finke DL (2003) Predation risk affects relative strength of top-down and bottom-up impacts on insect herbivores. Ecology 84:1032–1044. https://doi.org/10.1890/0012-9658(2003)084%5b1032:PRARSO%5d2.0.CO;2

    Article  Google Scholar 

  32. Denno RF, Mitter MS, Langellotto GA, Gratton C, Finke DL (2004) Interactions between a hunting spider and a web-builder: consequences of intraguild predation and cannibalism for prey suppression. Ecol Entomol 29:566–577. https://doi.org/10.1111/j.0307-6946.2004.00628.x

    Article  Google Scholar 

  33. Fagan WF, Denno RF (2004) Stoichiometry of actual vs. potential predator–prey interactions: insights into nitrogen limitation for arthropod predators. Ecol Lett 7:876–883. https://doi.org/10.1111/j.1461-0248.2004.00641.x

    Article  Google Scholar 

  34. Finke DL, Denno RF (2006) Spatial refuge from intraguild predation: implications for prey suppression and trophic cascades. Oecologia 149:265–275. https://doi.org/10.1007/s00442-006-0443-y

    Article  PubMed  Google Scholar 

  35. Finke DL, Snyder WE (2008) Niche partitioning increases resource exploitation by diverse communities. Science 321:1488–1490. https://doi.org/10.1126/science.1160854

    CAS  Article  PubMed  Google Scholar 

  36. Foelix RF (2011) Biology of spiders. Oxford University Press, New York

    Google Scholar 

  37. Folz HC, Wilder SM, Persons MH, Rypstra AL (2006) Effects of predation risk on vertical habitat use and foraging of Pardosa milvina. Ethology 112:1152–1158. https://doi.org/10.1111/j.1439-0310.2006.01276.x

    Article  Google Scholar 

  38. Furlong MJ, Zu-Hua S, Yin-Quan L, Shi-Jian G, Yao-Bin L, Shu-Sheng L, Zalucki MP (2004) Experimental analysis of the influence of pest management practice on the efficacy of an endemic arthropod natural enemy complex of the diamondback moth. J Econ Entomol 97:1814–1827. https://doi.org/10.1603/0022-0493-97.6.1814

    Article  PubMed  Google Scholar 

  39. Gan W, Liu S, Yang X, Li D, Lei C (2015) Prey interception drives web invasion and spider size determines successful web takeover in nocturnal orb-web spiders. Biol Open 4:1326–1329. https://doi.org/10.1242/bio.012799

    Article  PubMed  PubMed Central  Google Scholar 

  40. Gavish-Regev E, Rotkopf R, Lubin Y, Coll M (2009) Consumption of aphids by spiders and the effect of additional prey: evidence from microcosm experiments. Biocontrol 54:341–350. https://doi.org/10.1007/s10526-008-9170-0

    Article  Google Scholar 

  41. Graf N, Bucher R, Schäfer RB, Entling MH (2017) Contrasting effects of aquatic subsidies on a terrestrial trophic cascade. Biol Lett 13:20170129. https://doi.org/10.1098/rsbl.2017.0129

    Article  PubMed  PubMed Central  Google Scholar 

  42. Griffin JN, Byrnes JE, Cardinale BJ (2013) Effects of predator richness on prey suppression: a meta-analysis. Ecology 94:2180–2187. https://doi.org/10.1890/13-0179.1

    Article  PubMed  Google Scholar 

  43. Halaj J, Wise DH (2002) Impact of a detrital subsidy on trophic cascades in a terrestrial grazing food web. Ecology 83:3141–3151. https://doi.org/10.1890/0012-9658(2002)083%5b3141:IOADSO%5d2.0.CO;2

    Article  Google Scholar 

  44. Hanley TC, La Pierre KJ (2015) Trophic ecology: bottom-up and top-down interactions across aquatic and terrestrial systems. Cambridge University Press, Cambridge

    Google Scholar 

  45. Hanna R, Zalom FG, Roltsch WJ (2003) Relative impact of spider predation and cover crop on population dynamics of Erythroneura variabilis in a raisin grape vineyard. Entomol Exp Appl 107:177–191. https://doi.org/10.1046/j.1570-7458.2003.00051.x

    Article  Google Scholar 

  46. Harwood JD, Sunderland KD, Symondson WOC (2003) Web-location by linyphiid spiders: prey-specific aggregation and foraging strategies. J Anim Ecol 72:745–756. https://doi.org/10.1046/j.1365-2656.2003.00746.x

    Article  Google Scholar 

  47. Harwood JD, Sunderland KD, Symondson WOC (2004) Prey selection by linyphiid spiders: molecular tracking of the effects of alternative prey on rates of aphid consumption in the field. Mol Ecol 13:3549–3560. https://doi.org/10.1111/j.1365-294X.2004.02331.x

    Article  PubMed  Google Scholar 

  48. Harwood JD, Sunderland KD, Symondson WOC (2005) Monoclonal antibodies reveal the potential of the tetragnathid spider Pachygnatha degeeri (Araneae: Tetragnathidae) as an aphid predator. Bull Entomol Res 95:161–167. https://doi.org/10.1079/BER2004346

    CAS  Article  PubMed  Google Scholar 

  49. Harwood JD, Bostrom MR, Hladilek EE, Wise DH, Obrycki JJ (2007) An order-specific monoclonal antibody to Diptera reveals the impact of alternative prey on spider feeding behavior in a complex food web. Biol Control 41:397–407. https://doi.org/10.1016/j.biocontrol.2007.02.008

    Article  Google Scholar 

  50. Hawlena D, Schmitz OJ (2010a) Physiological stress as a fundamental mechanism linking predation to ecosystem functioning. Am Nat 176:537–556. https://doi.org/10.1086/656495

    Article  PubMed  Google Scholar 

  51. Hawlena D, Schmitz OJ (2010b) Herbivore physiological response to predation risk and implications for ecosystem nutrient dynamics. PNAS 107:15503–15507. https://doi.org/10.1073/pnas.1009300107

    Article  PubMed  Google Scholar 

  52. Heong KL, Bleih S, Rubia EG (1991) Prey preference of the wolf spider Pardosa pseudoannulata (Boesenberg et Strand). Popul Ecol 33:179–186. https://doi.org/10.1007/BF02513547

    Article  Google Scholar 

  53. Herberstein ME (2011) Spider behaviour: flexibility and versatility. Cambridge University Press, Cambridge

    Google Scholar 

  54. Hodge MA (1999) The implications of intraguild predation for the role of spiders in biological control. J Arachnol 27:351–362

    Google Scholar 

  55. Holling CS (1965) The functional response of predators to prey density and its role in mimicry and population regulation. Mem Entomol Soc Can 97:5–60. https://doi.org/10.4039/entm9745fv

    Article  Google Scholar 

  56. Holt RD, Bonsall MB (2017) Apparent competition. Ann Rev Ecol Evol Syst 48:447–471. https://doi.org/10.1146/annurev-ecolsys-110316-022628

    Article  Google Scholar 

  57. Holt RD, Polis GA (1997) A theoretical framework for intraguild predation. Am Nat 149:745–764. https://doi.org/10.1086/286018

    Article  Google Scholar 

  58. Huey RB, Pianka ER (1981) Ecological consequences of foraging mode. Ecology 62:991–999. https://doi.org/10.2307/1936998

    Article  Google Scholar 

  59. Isaia M, Beikes S, Paschetta M, Sarvajayakesevalu S, Badino G (2010) Spiders as potential biological controllers in apple orchards infested by Cydia spp (Lepidoptera: Tortricidae). In: Nentwig W, Entling M, Kropf C (eds) Proceedings of the 24th European Congress of Arachnology, Bern, pp 25–29

  60. Janssen A, Sabelis MW, Magalhães S, Montserrat M, van der Hammen T (2007) Habitat structure affects intraguild predation. Ecology 88:713–2719. https://doi.org/10.1890/06-1408.1

    Article  Google Scholar 

  61. Jeschke JM, Kopp M, Tollrian R (2004) Consumer-food systems: why type I functional responses are exclusive to filter feeders. Biol Rev 79:337–349. https://doi.org/10.1017/S1464793103006286

    Article  PubMed  Google Scholar 

  62. Jonsson M, Kaartinen R, Straub CS (2017) Relationships between natural enemy diversity and biological control. Curr Opin Insect Sci 20:1–6. https://doi.org/10.1016/j.cois.2017.01.001

    Article  PubMed  Google Scholar 

  63. Jonsson T, Kaartinen R, Jonsson M, Bommarco R (2018) Predictive power of food web models based on body size decreases with trophic complexity. Ecol Lett 21:702–712. https://doi.org/10.1111/ele.12938

    Article  PubMed  Google Scholar 

  64. Klečka J, Boukal D (2013) Foraging and vulnerability traits modify predator–prey body mass allometry: freshwater macroinvertebrates as a case study. J Anim Ecol 82:1031–1041. https://doi.org/10.1111/1365-2656.12078

    Article  PubMed  Google Scholar 

  65. Knop E, Zünd J, Sanders D (2014) Interactive prey and predator diversity effects drive consumption rates. Oikos 123:1244–1249. https://doi.org/10.1111/oik.00926

    Article  Google Scholar 

  66. Kobayashi T, Takada M, Takagi S, Yoshioka A, Washitani I (2011) Spider predation on a mirid pest in Japanese rice fields. Basic Appl Ecol 12:532–539. https://doi.org/10.1016/j.baae.2011.07.007

    Article  Google Scholar 

  67. Korenko S, Pekár S (2010) Is there intraguild predation between winter-active spiders (Araneae) on apple tree bark? Biol Control 54:206–212. https://doi.org/10.1016/j.biocontrol.2010.05.008

    Article  Google Scholar 

  68. Korenko S, Pekar S, Honěk A (2010) Predation activity of two winter-active spiders (Araneae: Anyphaenidae Philodromidae). J Therm Biol 35:112–116. https://doi.org/10.1016/j.jtherbio.2009.12.004

    CAS  Article  PubMed  Google Scholar 

  69. Křivan V (2008) Prey–predator models. In: Jorgensen SE, Fath BD (eds) Encyclopedia of ecology. Elsevier, Amsterdam, pp 2929–2940

    Google Scholar 

  70. Kruse PD, Toft S, Sunderland KD (2008) Temperature and prey capture: opposite relationships in two predator taxa. Ecol Entomol 33:305–312. https://doi.org/10.1111/j.1365-2311.2007.00978.x

    Article  Google Scholar 

  71. Kuusk AK, Ekbom B (2010) Lycosid spiders and alternative food: feeding behavior and implications for biological control. Biol Control 55:20–26. https://doi.org/10.1016/j.biocontrol.2010.06.009

    Article  Google Scholar 

  72. Kuusk AK, Ekbom B (2012) Feeding habits of lycosids spiders in field habitats. J Pest Sci 85:253–260. https://doi.org/10.1007/s10340-012-0431-4

    Article  Google Scholar 

  73. Lang A (2003) Intraguild interference and biocontrol effects of generalist predators in a winter wheat field. Oecologia 134:144–153. https://doi.org/10.1007/s00442-002-1091-5

    Article  PubMed  Google Scholar 

  74. Laundré JW, Hernández L, Medina PL, Campanella A, López-Portillo J, González-Romero A, Grajales-Tam KM, Burke AM, Gronemeyer P, Browning DM (2014) The landscape of fear: the missing link to understand top-down and bottom-up controls of prey abundance? Ecology 95:1141–1152. https://doi.org/10.1890/13-1083.1

    Article  PubMed  Google Scholar 

  75. Lease HM, Wolf BO (2011) Lipid content of terrestrial arthropods in relation to body size phylogeny ontogeny and sex. Physiol Entomol 36:29–38. https://doi.org/10.1111/j.1365-3032.2010.00767.x

    CAS  Article  Google Scholar 

  76. Lefebvre M, Franck P, Olivares J, Ricard JM, Mandrin JF, Lavigne C (2017) Spider predation on rosy apple aphid in conventional organic and insecticide-free orchards and its impact on aphid populations. Biol Control 104:57–65. https://doi.org/10.1016/j.biocontrol.2016.10.009

    Article  Google Scholar 

  77. Lesne P, Trabalon M, Jeanson R (2016) Cannibalism in spiderlings is not only about starvation. Behav Ecol Sociobiol 70:1669–1678. https://doi.org/10.1007/s00265-016-2172-5

    Article  Google Scholar 

  78. Letourneau DK, Jedlicka JA, Bothwell SG, Moreno CR (2009) Effects of natural enemy biodiversity on the suppression of arthropod herbivores in terrestrial E ecosystems. Annu Rev Ecol Evol Syst 40:573–592. https://doi.org/10.1146/annurev.ecolsys.110308.120320

    Article  Google Scholar 

  79. Liu S, Li Z, Sui Y, Schaefer DA, Alele PO, Chen J, Yang X (2015) Spider foraging strategies dominate pest suppression in organic tea plantations. Biocontrol 60:839–847. https://doi.org/10.1007/s10526-015-9691-2

    CAS  Article  Google Scholar 

  80. Losey JE, Denno RF (1999) Factors facilitating synergistic predation: the central role of synchrony. Ecol Appl 9:378–386. https://doi.org/10.1890/1051-0761(1999)009%5b0378:FFSPTC%5d2.0.CO;2

    Article  Google Scholar 

  81. Madsen M, Terkildsen S, Toft S (2004) Microcosm studies on control of aphids by generalist arthropod predators: effects of alternative prey. Biocontrol 49:483–504. https://doi.org/10.1023/B:BICO.0000036442.70171.66

    Article  Google Scholar 

  82. Maloney D, Drummond FA, Alford R (2003) Spider predation in agroecosystems: can spiders effectively control pest populations? Technical Bulletin 190. University of Maine, Orono

    Google Scholar 

  83. Mansour F, Heimbach U (1993) Evaluation of Lycosid Micryphantid and Linyphiid spiders as predators of Rhopalosiphum padi (Hom: Aphididae) and their functional response to prey density-laboratory experiments. Biocontrol 38:79–87. https://doi.org/10.1007/BF02373142

    Article  Google Scholar 

  84. Marc P, Canard A, Ysnel F (1999) Spiders (Araneae) useful for pest limitation and bioindication. Agric Ecosyst Environ 74:229–273. https://doi.org/10.1016/S0167-8809(99)00038-9

    Article  Google Scholar 

  85. Markó V, Keresztes B (2014) Flowers for better pest control? Ground cover plants enhance apple orchard spiders (Araneae) but not necessarily their impact on pests. Biocontrol Sci Technol 24:574–596. https://doi.org/10.1080/09583157.2014.881981

    Article  Google Scholar 

  86. Matsumura M, Trafelet-Smith GM, Gratton C, Finke DL, Fagan WF, Denno RF (2004) Does intraguild predation enhance predator performance? A stoichiometric perspective. Ecology 85:2601–2615. https://doi.org/10.1890/03-0629

    Article  Google Scholar 

  87. Mayntz D, Toft S (2000) Effect of nutrient balance on tolerance to low quality prey in a wolf spider (Araneae: Lycosidae). Ekológia 19:153–158

    Google Scholar 

  88. Mayntz D, Toft S (2006) Nutritional value of cannibalism and the role of starvation and nutrient imbalance for cannibalistic tendencies in a generalist predator. J Anim Ecol 75:288–297. https://doi.org/10.1111/j.1365-2656.2006.01046.x

    Article  PubMed  Google Scholar 

  89. Mayntz D, Raubenheimer D, Salomon M, Toft S, Simpson SJ (2005) Nutrient-specific foraging in invertebrate predators. Science 307:111–113. https://doi.org/10.1126/science.1105493

    CAS  Article  PubMed  Google Scholar 

  90. Mestre L, Bonte D (2012) Food stress during juvenile and maternal development shapes natal and breeding dispersal in a spider. Behav Ecol 23:759–764. https://doi.org/10.1093/beheco/ars024

    Article  Google Scholar 

  91. Mestre L, Piñol J, Barrientos JA, Espadaler X, Brewitt K, Werner C, Platner C (2013) Trophic structure of the spider community of a Mediterranean citrus grove: a stable isotope analysis. Basic Appl Ecol 14:413–422. https://doi.org/10.1016/j.baae.2013.05.001

    Article  Google Scholar 

  92. Mestre L, Bucher R, Entling MH (2014) Trait-mediated effects between predators: ant chemical cues induce spider dispersal. J Zool 293:119–125. https://doi.org/10.1111/jzo.12127

    Article  Google Scholar 

  93. Michalko R, Košulič O (2016) Temperature-dependent effect of two neurotoxic insecticides on predatory potential of Philodromus spiders. J Pest Sci 89:517–527. https://doi.org/10.1007/s10340-015-0696-5

    Article  Google Scholar 

  94. Michalko R, Pekár S (2014) Is different degree of individual specialisation in three closely related spider species caused by different selection pressures? Basic Appl Ecol 15:496–506. https://doi.org/10.1016/j.baae.2014.08.003

    Article  Google Scholar 

  95. Michalko R, Pekár S (2015) The biocontrol potential of Philodromus (Araneae Philodromidae) spiders for the suppression of pome fruit orchard pests. Biol Control 82:13–20. https://doi.org/10.1016/j.biocontrol.2014.12.001

    Article  Google Scholar 

  96. Michalko R, Pekár S (2016) Different hunting strategies of generalist predators result in functional differences. Oecologia 181:1187–1197. https://doi.org/10.1007/s00442-016-3631-4

    Article  PubMed  Google Scholar 

  97. Michalko R, Pekár S (2017) The behavioral type of a top predator drives the short-term dynamic of intraguild predation. Am Nat 189:242–253. https://doi.org/10.1086/690501

    Article  PubMed  Google Scholar 

  98. Michalko R, Petráková L, Sentenská L, Pekár S (2017) The effect of habitat complexity and density-dependent non-consumptive interference on pest suppression by winter-active spiders. Agric Ecosyst Environ 242:26–33. https://doi.org/10.1016/j.agee.2017.03.025

    Article  Google Scholar 

  99. Miller JR, Ament JM, Schmitz OJ (2014) Fear on the move: predator hunting mode predicts variation in prey mortality and plasticity in prey spatial response. J Anim Ecol 83:214–222. https://doi.org/10.1111/1365-2656.12111

    Article  PubMed  Google Scholar 

  100. Morozov A, Petrovskii S (2013) Feeding on multiple sources: towards a universal parameterization of the functional response of a generalist predator allowing for switching. PloS One 8:e74586. https://doi.org/10.1371/journal.pone.0074586

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  101. Müller CB, Brodeur J (2002) Intraguild predation in biological control and conservation biology. Biol Control 25:216–223. https://doi.org/10.1016/S1049-9644(02)00102-0

    Article  Google Scholar 

  102. Murdoch WW, Kendall BE, Nisbet RM, Briggs CJ, McCauley E, Bolser R (2002) Single-species models for many-species food webs. Nature 417:541–543. https://doi.org/10.1038/417541a

    CAS  Article  PubMed  Google Scholar 

  103. Nentwig W, Wissel C (1986) A comparison of prey lengths among spiders. Oecologia 68:595–600. https://doi.org/10.1007/BF00378777

    Article  PubMed  Google Scholar 

  104. Nyffeler M, Benz G (1987) Spiders in natural pest control: a review. J Appl Entomol 103:321–339. https://doi.org/10.1111/j.1439-0418.1987.tb00992.x

    Article  Google Scholar 

  105. Nyffeler M, Birkhofer K (2017) An estimated 400–800 million tons of prey are annually killed by the global spider community. Sci Nat 104:30. https://doi.org/10.1007/s00114-017-1440-1

    CAS  Article  Google Scholar 

  106. Oelbermann K, Scheu S (2002) Effects of prey type and mixed diets on survival growth and development of a generalist predator Pardosa lugubris (Araneae: Lycosidae). Basic Appl Ecol 3:285–291. https://doi.org/10.1078/1439-1791-00094

    Article  Google Scholar 

  107. Oelbermann K, Scheu S (2009) Control of aphids on wheat by generalist predators: effects of predator density and the presence of alternative prey. Entomol Exp Appl 132:225–231. https://doi.org/10.1111/j.1570-7458.2009.00876.x

    Article  Google Scholar 

  108. Oelbermann K, Langel R, Scheu S (2008) Utilization of prey from the decomposer system by generalist predators of grassland. Oecologia 155:605–617. https://doi.org/10.1007/s00442-007-0927-4

    Article  PubMed  Google Scholar 

  109. Okuyama T (2007) Prey of two species of jumping spiders in the field. Appl Entomol Zool 42:663–668. https://doi.org/10.1303/aez.2007.663

    Article  Google Scholar 

  110. Pearman PB, Guisan A, Broennimann O, Randin CF (2008) Niche dynamics in space and time. Trends Ecol Evol 23:149–158. https://doi.org/10.1016/j.tree.2007.11.005

    Article  PubMed  Google Scholar 

  111. Pekár S (2012) Spiders (Araneae) in the pesticide world: an ecotoxicological review. Pest Manag Sci 68:1438–1446. https://doi.org/10.1002/ps.3397

    CAS  Article  PubMed  Google Scholar 

  112. Pekár S, Toft S (2015) Trophic specialisation in a predatory group: the case of prey-specialised spiders (Araneae). Biol Rev 90:744–761. https://doi.org/10.1111/brv.12133

    Article  PubMed  Google Scholar 

  113. Pekár S, Martišová M, Bilde T (2011) Intersexual trophic niche partitioning in an ant-eating spider (Araneae: Zodariidae). PLoS One 6:e14603. https://doi.org/10.1371/journal.pone.0014603

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  114. Pekár S, Coddington JA, Blackledge TA (2012) Evolution of stenophagy in spiders (Araneae): evidence based on the comparative analysis of spider diets. Evolution 66:776–806. https://doi.org/10.1111/j.1558-5646.2011.01471.x

    Article  PubMed  Google Scholar 

  115. Pekár S, Michalko R, Korenko S, Šedo O, Líznarová E, Sentenská L, Zdráhal Z (2013) Phenotypic integration in a series of trophic traits: tracing the evolution of myrmecophagy in spiders (Araneae). Zoology 116:27–35. https://doi.org/10.1016/j.zool.2012.05.006

    Article  PubMed  Google Scholar 

  116. Pekár S, Michalko R, Loverre P, Líznarová E, Černecká Ľ (2015) Biological control in winter: novel evidence for the importance of generalist predators. J Appl Ecol 52:270–279. https://doi.org/10.1111/1365-2664.12363

    Article  Google Scholar 

  117. Perkins MJ, Inger R, Bearhop S, Sanders D (2018) Multichannel feeding by spider functional groups is driven by feeding strategies and resource availability. Oikos 127:23–33. https://doi.org/10.1111/oik.04500

    Article  Google Scholar 

  118. Petcharad B, Košulič O, Michalko R (2018) Insecticides alter prey choice of potential biocontrol agent Philodromus cespitum (Araneae, Philodromidae). Chemosphere 202:491–497. https://doi.org/10.1016/j.chemosphere.2018.03.134

    CAS  Article  PubMed  Google Scholar 

  119. Petráková L, Michalko R, Loverre P, Sentenská L, Korenko S, Pekár S (2016) Intraguild predation among spiders and their effect on the pear psylla during winter. Agric Ecosyst Environ 233:67–74. https://doi.org/10.1016/j.agee.2016.08.008

    Article  Google Scholar 

  120. Picchi MS, Bocci G, Petacchi R, Entling MH (2016) Effects of local and landscape factors on spiders and olive fruit flies. Agric Ecosyst Environ 222:138–147. https://doi.org/10.1016/j.agee.2016.01.045

    Article  Google Scholar 

  121. Polis GA, Myers CA, Holt RD (1989) The ecology and evolution of intraguild predation: potential competitors that eat each other. Annu Rev Ecol Evol Syst 20:297–330. https://doi.org/10.1146/annurev.es.20.110189.001501

    Article  Google Scholar 

  122. Preisser EL, Bolnick DI (2008) The many faces of fear: comparing the pathways and impacts of nonconsumptive predator effects on prey populations. PLoS One 3:e2465. https://doi.org/10.1371/journal.pone.0002465

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  123. Pruitt JN, Riechert JE (2012) The ecological consequences of temperament in spiders. Curr Zool 58:589–596. https://doi.org/10.1093/czoolo/58.4.589

    Article  Google Scholar 

  124. 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 283:20161409. https://doi.org/10.1098/rspb.2016.1409

    Article  PubMed  Google Scholar 

  125. Rendon D, Whitehouse ME, Taylor PW (2016) Consumptive and non-consumptive effects of wolf spiders on cotton bollworms. Entomol Exp Appl 158:170–183. https://doi.org/10.1111/eea.12390

    CAS  Article  Google Scholar 

  126. Richardson ML, Hanks LM (2009) Partitioning of niches among four species of orb-weaving spiders in a grassland habitat. Environ Entomol 38:651–656. https://doi.org/10.1603/022.038.0316

    CAS  Article  PubMed  Google Scholar 

  127. Rickers S, Langel R, Scheu S (2006) Stable isotope analyses document intraguild predation in wolf spiders (Araneae: Lycosidae) and underline beneficial effects of alternative prey and microhabitat structure on intraguild prey survival. Oikos 114:471–478. https://doi.org/10.1111/j.2006.0030-1299.14421.x

    Article  Google Scholar 

  128. Riechert SE (1991) Prey abundance vs diet breadth in a spider test system. Evol Ecol 5:327–338. https://doi.org/10.1007/BF02214236

    Article  Google Scholar 

  129. Riechert SE (1999) The hows and whys of successful pest suppression by spiders: insights from case studies. J Arachnol 27:387–396

    Google Scholar 

  130. Riechert SE, Bishop L (1990) Prey control by an assemblage of generalist predators: spiders in garden test systems. Ecology 71:1441–1450. https://doi.org/10.2307/1938281

    Article  Google Scholar 

  131. Riechert SE, Harp JM (1987) Nutritional ecology of spiders. In: Rodriguez JG, Slansky F (eds) Nutritional ecology of insects mites and spiders. Wiley, New York, pp 645–672

    Google Scholar 

  132. Riechert SE, Hedrick AV (1993) A test for correlation among fitness-linked behavioural traits in the spider Agelenopsis aperta (Araneae Agelenidae). Anim Behav 46:669–675. https://doi.org/10.1006/anbe.1993.1243

    Article  Google Scholar 

  133. Riechert SE, Lockley T (1984) Spiders as biological control agents. Annu Rev Entomol 29:299–320. https://doi.org/10.1146/annurev.en.29.010184.001503

    Article  Google Scholar 

  134. Rosenheim JA, Harmon JP (2006) The influence of intraguild predation on the suppression of a shared prey population: an empirical reassessment. In: Boivin G, Brodeur J (eds) Trophic and guild in biological interactions control. Springer, Netherlands

    Google Scholar 

  135. Rosenheim JA, Kaya HK, Ehler LE, Marois JJ, Jaffee BA (1995) Intraguild predation among biological-control agents: theory and evidence. Biol Control 5:303–335. https://doi.org/10.1006/bcon.1995.1038

    Article  Google Scholar 

  136. Roubinet E, Birkhofer K, Malsher G, Staudacher K, Ekbom B, Traugott M, Jonsson M (2017) Diet of generalist predators reflects effects of cropping period and farming system on extra-and intraguild prey. Ecol Appl 27:1167–1177. https://doi.org/10.1002/eap.1510

    Article  PubMed  Google Scholar 

  137. Royauté R, Pruitt JN (2015) Varying predator personalities generates contrasting prey communities in an agroecosystem. Ecology 96:2902–2911. https://doi.org/10.1890/14-2424.1

    Article  PubMed  Google Scholar 

  138. Royauté R, Buddle CM, Vincent C (2014) Interpopulation variations in behavioral syndromes of a jumping spider from insecticide-treated and insecticide-free orchards. Ethology 120:127–139. https://doi.org/10.1111/eth.12185

    Article  Google Scholar 

  139. Rusch A, Birkhofer K, Bommarco R, Smith HG, Ekbom B (2015) Predator body sizes and habitat preferences predict predation rates in an agroecosystem. Basic Appl Ecol 16:250–259. https://doi.org/10.1016/j.baae.2015.02.003

    Article  Google Scholar 

  140. Ryabov AB, Morozov A, Blasius B (2015) Imperfect prey selectivity of predators promotes biodiversity and irregularity in food webs. Ecol Lett 18:1262–1269. https://doi.org/10.1111/ele.12521

    Article  PubMed  Google Scholar 

  141. Rypstra AL, Buddle CM (2013) Spider silk reduces insect herbivory. Biol Lett 9:20120948. https://doi.org/10.1098/rsbl.2012.0948

    Article  PubMed  PubMed Central  Google Scholar 

  142. Rypstra AL, Samu F (2005) Size dependent intraguild predation and cannibalism in coexisting wolf spiders (Araneae Lycosidae). J Arachnol 33:390–397. https://doi.org/10.1636/CT05-10.1

    Article  Google Scholar 

  143. Rypstra AL, Carter PE, Balfour RA, Marshall SD (1999) Architectural features of agricultural habitats and their impact on the spider inhabitants. J Arachnol 27:371–377

    Google Scholar 

  144. Samu F (1993) Wolf spider feeding strategies: optimality of prey consumption in Pardosa hortensis. Oecologia 94:139–145. https://doi.org/10.1007/BF00317315

    CAS  Article  PubMed  Google Scholar 

  145. Samu F, Bíró Z (1993) Functional response multiple feeding and wasteful killing in a wolf spider (Araneae: Lycosidae). Eur J Entomol 90:471–476

    Google Scholar 

  146. Samu F, Sunderland KD, Szinetár C (1999) Scale-dependent dispersal and distribution patterns of spiders in agricultutural systems: a review. J Arachnol 27:325–332

    Google Scholar 

  147. Samu F, Beleznai O, Tholt G (2013) A potential spider natural enemy against virus vector leafhoppers in agricultural mosaic landscapes–Corroborating ecological and behavioral evidence. Biol Control 67:390–396. https://doi.org/10.1016/j.biocontrol.2013.08.016

    Article  Google Scholar 

  148. Sanders D, Vogel E, Knop E (2015) Individual and species-specific traits explain niche size and functional role in spiders as generalist predators. J Anim Ecol 84:134–142. https://doi.org/10.1111/1365-2656.12271

    Article  PubMed  Google Scholar 

  149. Schellhorn NA, Bianchi FJJA, Hsu CL (2014) Movement of entomophagous arthropods in agricultural landscapes: links to pest suppression. Annu Rev Entomol 59:559–581. https://doi.org/10.1146/annurev-ento-011613-161952

    CAS  Article  PubMed  Google Scholar 

  150. Schmidt JM, Rypstra AL (2010) Opportunistic predator prefers habitat complexity that exposes prey while reducing cannibalism and intraguild encounters. Oecologia 164:899–910. https://doi.org/10.1007/s00442-010-1785-z

    Article  PubMed  Google Scholar 

  151. Schmidt MH, Lauer A, Purtauf T, Thies C, Schaefer M, Tscharntke T (2003) Relative importance of predators and parasitoids for cereal aphid control. Proc R Soc Lond B 270:1905–1909. https://doi.org/10.1098/rspb.2003.2469

    Article  Google Scholar 

  152. Schmidt MH, Thewes U, Thies C, Tscharntke T (2004) Aphid suppression by natural enemies in mulched cereals. Entomol Exp Appl 113:87–93. https://doi.org/10.1111/j.0013-8703.2004.00205.x

    Article  Google Scholar 

  153. Schmidt JM, Harwood JD, Rypstra AL (2012a) Foraging activity of a dominant epigeal predator: molecular evidence for the effect of prey density on consumption. Oikos 121:1715–1724. https://doi.org/10.1111/j.1600-0706.2011.20366.x

    Article  Google Scholar 

  154. Schmidt JM, Sebastian P, Wilder SM, Rypstra AL (2012b) The nutritional content of prey affects the foraging of a generalist arthropod predator. PLoS One 7:e49223. https://doi.org/10.1371/journal.pone.0049223

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  155. Schmidt JM, Crist TO, Wrinn K, Rypstra AL (2014) Predator interference alters foraging behavior of a generalist predatory arthropod. Oecologia 175:501–508. https://doi.org/10.1007/s00442-014-2922-x

    Article  PubMed  Google Scholar 

  156. Schmidt-Entling MH, Siegenthaler E (2009) Herbivore release through cascading risk effects. Biol Lett 5:773–776. https://doi.org/10.1098/rsbl.2009.0436

    Article  PubMed  PubMed Central  Google Scholar 

  157. Schmitz OJ (2005) Behavior of predators and prey and links with population-level processes. In: Barbosa P, Castellanos I (eds) Ecology of predator–prey interactions. Oxford University Press, Oxford

    Google Scholar 

  158. Schmitz OJ (2007) Predator diversity and trophic interactions. Ecology 88:2415–2426. https://doi.org/10.1890/06-0937.1

    Article  PubMed  Google Scholar 

  159. Schmitz OJ (2010) Resolving Ecosystem Complexity. Princeton University Press, Princeton

    Google Scholar 

  160. Schmitz OJ, Beckerman AP, O’Brien KM (1997) Behaviorally mediated trophic cascades: effects of predation risk on food web interactions. Ecology 78:1388–1399. https://doi.org/10.1890/0012-9658(1997)078%5b1388:BMTCEO%5d2.0.CO;2

    Article  Google Scholar 

  161. Schneider FD, Scheu S, Brose U (2012) Body mass constraints on feeding rates determine the consequences of predator loss. Ecol Lett 15:436–443. https://doi.org/10.1111/j.1461-0248.2012.01750.x

    Article  PubMed  Google Scholar 

  162. Settle WH, Ariawan H, Astuti ET, Cahyana W, Hakim AL, Hindayana D, Lestari AS (1996) Managing tropical rice pests through conservation of generalist natural enemies and alternative prey. Ecology 77:1975–1988. https://doi.org/10.2307/2265694

    Article  Google Scholar 

  163. Sih A, Englund G, Wooster D (1998) Emergent impacts of multiple predators on prey. Trends Ecol Evol 13:350–355. https://doi.org/10.1016/S0169-5347(98)01437-2

    CAS  Article  PubMed  Google Scholar 

  164. Sinclair ARE, Pech RP, Dickman CR, Hik D, Mahon P, Newsome AE (1998) Predicting effects of predation on conservation of endangered prey. Conserv Biol 12:564–575. https://doi.org/10.1111/j.1523-1739.1998.97030.x

    Article  Google Scholar 

  165. Sitvarin MI, Rypstra AL (2014) The importance of intraguild predation in predicting emergent multiple predator effects. Ecology 95:2936–2945. https://doi.org/10.1890/13-2347.1

    Article  Google Scholar 

  166. Snyder WE, Ives AR (2003) Interactions between specialist and generalist natural enemies: parasitoids, predators, and pea aphid biocontrol. Ecology 84:91–107. https://doi.org/10.1890/0012-9658(2003)084%5b0091:IBSAGN%5d2.0.CO;2

    Article  Google Scholar 

  167. Snyder WE, Chang GC, Prasad RP (2005) Conservation biological control. In: Barbosa P, Castellanos I (eds) Ecology of predator–prey interactions. Oxford University Press, Oxford

    Google Scholar 

  168. Solomon ME (1949) The natural control of animal populations. J Anim Ecol 18:1–35. https://doi.org/10.2307/1578

    Article  Google Scholar 

  169. Stephens DW, Brown JS, Ydenberg RC (2007) Foraging: behavior and ecology. University of Chicago Press, Chicago

    Google Scholar 

  170. Sunderland K (1999) Mechanisms underlying the effects of spiders on pest populations. J Arachnol 27:308–316

    Google Scholar 

  171. 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 24:1205–1210. https://doi.org/10.1093/beheco/art052

    Article  PubMed  PubMed Central  Google Scholar 

  172. Symondson WOC, Sunderland KD, Greenstone MH (2002) Can generalist predators be effective biocontrol agents? Annu Rev Entomol 47:561–594. https://doi.org/10.1146/annurev.ento.47.091201.145240

    CAS  Article  PubMed  Google Scholar 

  173. Takada MB, Kobayashi T, Yoshioka A, Takagi S, Washitani I (2013) Facilitation of ground-dwelling wolf spider predation on mirid bugs by horizontal webs built by Tetragnatha spiders in organic paddy fields. J Arachnol 41:31–35. https://doi.org/10.1636/P12-30.1

    Article  Google Scholar 

  174. Toft S (1995) Value of the aphid Rhopalosiphum padi as food for cereal spiders. J Appl Ecol 32:552–560. https://doi.org/10.2307/2404652

    Article  Google Scholar 

  175. Toft S (1999) Prey choice and spider fitness. J Arachnol 27:301–307

    Google Scholar 

  176. Toft S (2005) The quality of aphids as food for generalist predators: implications for natural control of aphids. Eur J Entomol 102:371

    Article  Google Scholar 

  177. Toft S (2013) Nutritional aspects of spider feeding. In: Nentwig W (ed) Spider ecophysiology. Springer-Verlag, Berlin

    Google Scholar 

  178. Toft S, Wise DH (1999a) Behavioral and ecophysiological responses of a generalist predator to single- and mixed-species diets of different quality. Oecologia 119:198–207. https://doi.org/10.1007/s004420050777

    Article  PubMed  Google Scholar 

  179. Toft S, Wise DH (1999b) Growth development and survival of a generalist predator fed single- and mixed-species diets of different quality. Oecologia 119:191–197. https://doi.org/10.1007/s004420050776

    Article  PubMed  Google Scholar 

  180. Traugott M, Bell JR, Raso L, Sint D, Symondson WOC (2012) Generalist predators disrupt parasitoid aphid control by direct and coincidental intraguild predation. Bull Entomol Res 102:239–247. https://doi.org/10.1017/S0007485311000551

    CAS  Article  PubMed  Google Scholar 

  181. Tscharntke T, Karp DS, Chaplin-Kramer R et al (2016) When natural habitat fails to enhance biological pest control-five hypotheses. Biol Conserv 204:449–458. https://doi.org/10.1016/j.biocon.2016.10.001

    Article  Google Scholar 

  182. Tsutsui MH, Tanaka K, Baba YG, Miyashita T (2016) Spatio-temporal dynamics of generalist predators (Tetragnatha spider) in environmentally friendly paddy fields. Appl Entomol Zool 51:631–640. https://doi.org/10.1007/s13355-016-0440-5

    Article  Google Scholar 

  183. Tsutsui MH, Kobayashi K, Miyashita T (2018) Temporal trends in arthropod abundances after the transition to organic farming in paddy fields. PLoS One 13:e0190946. https://doi.org/10.1371/journal.pone.0190946

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  184. Tylianakis JM, Romo CM (2010) Natural enemy diversity and biological control: making sense of the context-dependency. Basic Appl Ecol 11:657–668. https://doi.org/10.1016/j.baae.2010.08.005

    Article  Google Scholar 

  185. von Berg K, Thies C, Tscharntke T, Scheu S (2009) Cereal aphid control by generalist predators in presence of belowground alternative prey: complementary predation as affected by prey density. Pedobiologia 53:41–48. https://doi.org/10.1016/j.pedobi.2009.03.001

    Article  Google Scholar 

  186. Vucic-Pestic O, Birkhofer K, Rall BC, Scheu S, Brose U (2010) Habitat structure and prey aggregation determine the functional response in a soil predator–prey interaction. Pedobiologia 53:307–312. https://doi.org/10.1016/j.pedobi.2010.02.003

    Article  Google Scholar 

  187. Walker SE, Rypstra AL (2003) Hungry spiders aren’t afraid of the big bad wolf spider. J Arachnol 31:425–427. https://doi.org/10.1636/S02-63

    Article  Google Scholar 

  188. Welch KD, Whitney TD, Harwood JD (2016) Non-pest prey do not disrupt aphid predation by a web-building spider. Bull Entomol Res 106:91–98. https://doi.org/10.1017/S0007485315000875

    CAS  Article  PubMed  Google Scholar 

  189. Werner EE, Peacor SD (2003) A review of trait-mediated indirect interactions in ecological communities. Ecology 84:1083–1100. https://doi.org/10.1890/0012-9658(2003)084%5b1083:AROTII%5d2.0.CO;2

    Article  Google Scholar 

  190. Whitehouse MEA, Mansfield S, Barnett MC, Broughton K (2011) From lynx spiders to cotton: behaviorally mediated predator effects over four trophic levels. Aus Ecol 36:687–697. https://doi.org/10.1111/j.1442-9993.2010.02204.x

    Article  Google Scholar 

  191. Wilder SM (2011) Spider nutrition: an integrated perspective. Adv Insect Physiol 40:87–136

    Article  Google Scholar 

  192. Wilder SM, Norris M, Lee RW, Raubenheimer D, Simpson SJ (2013) Arthropod food webs become increasingly lipid-limited at higher trophic levels. Ecol Lett 16:895–902. https://doi.org/10.1111/ele.12116

    Article  PubMed  Google Scholar 

  193. Wise DH (1993) Spiders in ecological webs. Cambridge University Press, Cambridge

    Google Scholar 

  194. Wise DH (2006) Cannibalism food limitation intraspecific competition and the regulation of spider populations. Annu Rev Entomol 51:441–465. https://doi.org/10.1146/annurev.ento.51.110104.150947

    CAS  Article  PubMed  Google Scholar 

  195. Yamanoi T, Miyashita T (2005) Foraging strategy of nocturnal orb-web spiders (Araneidae: Neoscona) with special reference to the possibility of beetle specialization by N punctigera. Acta Arachnol 54:13–19. https://doi.org/10.2476/asjaa.54.13

    Article  Google Scholar 

  196. Yang Y, Chen X, Shao Z, Zhou P, Porter D, Knight DP, Vollrath F (2005) Toughness of spider silk at high and low temperatures. Adv Mater 17:84–88. https://doi.org/10.1002/adma.200400344

    CAS  Article  Google Scholar 

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Acknowledgements

We are grateful to Riccardo Bommarco and several members of his lab for their comments that greatly improved the manuscript. We also thank the handling editor for his helpful comments. This study was supported by the Specific University Research Fund of the Faculty of Forestry and Wood Technology, Mendel University in Brno (Reg. No. LDF_PSV_2017004).

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RM conceived the idea. RM, ME, SP wrote the manuscript.

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Correspondence to Radek Michalko.

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Michalko, R., Pekár, S. & Entling, M.H. An updated perspective on spiders as generalist predators in biological control. Oecologia 189, 21–36 (2019). https://doi.org/10.1007/s00442-018-4313-1

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Keywords

  • Araneae
  • Agroecosystem
  • Food-web
  • Functional trait
  • Niche
  • Pest