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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
Decae AE (1987) Dispersal: ballooning and other mechanisms. In: Nentwig W (ed) Ecophysiology of spiders. Springer-Verlag, Berlin, pp 357–370
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
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
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
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
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
Finke DL, Snyder WE (2008) Niche partitioning increases resource exploitation by diverse communities. Science 321:1488–1490. https://doi.org/10.1126/science.1160854
Foelix RF (2011) Biology of spiders. Oxford University Press, New York
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
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
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
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
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
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
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
Hanley TC, La Pierre KJ (2015) Trophic ecology: bottom-up and top-down interactions across aquatic and terrestrial systems. Cambridge University Press, Cambridge
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
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
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
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
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
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
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
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
Herberstein ME (2011) Spider behaviour: flexibility and versatility. Cambridge University Press, Cambridge
Hodge MA (1999) The implications of intraguild predation for the role of spiders in biological control. J Arachnol 27:351–362
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
Holt RD, Bonsall MB (2017) Apparent competition. Ann Rev Ecol Evol Syst 48:447–471. https://doi.org/10.1146/annurev-ecolsys-110316-022628
Holt RD, Polis GA (1997) A theoretical framework for intraguild predation. Am Nat 149:745–764. https://doi.org/10.1086/286018
Huey RB, Pianka ER (1981) Ecological consequences of foraging mode. Ecology 62:991–999. https://doi.org/10.2307/1936998
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
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
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
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
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
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
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
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
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
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
Křivan V (2008) Prey–predator models. In: Jorgensen SE, Fath BD (eds) Encyclopedia of ecology. Elsevier, Amsterdam, pp 2929–2940
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
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
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
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
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
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
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
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
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
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
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
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
Maloney D, Drummond FA, Alford R (2003) Spider predation in agroecosystems: can spiders effectively control pest populations? Technical Bulletin 190. University of Maine, Orono
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
Nentwig W, Wissel C (1986) A comparison of prey lengths among spiders. Oecologia 68:595–600. https://doi.org/10.1007/BF00378777
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
Riechert SE (1991) Prey abundance vs diet breadth in a spider test system. Evol Ecol 5:327–338. https://doi.org/10.1007/BF02214236
Riechert SE (1999) The hows and whys of successful pest suppression by spiders: insights from case studies. J Arachnol 27:387–396
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
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
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
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
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
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
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
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
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
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
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
Rypstra AL, Buddle CM (2013) Spider silk reduces insect herbivory. Biol Lett 9:20120948. https://doi.org/10.1098/rsbl.2012.0948
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
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
Samu F (1993) Wolf spider feeding strategies: optimality of prey consumption in Pardosa hortensis. Oecologia 94:139–145. https://doi.org/10.1007/BF00317315
Samu F, Bíró Z (1993) Functional response multiple feeding and wasteful killing in a wolf spider (Araneae: Lycosidae). Eur J Entomol 90:471–476
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
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
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
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
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
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
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
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
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
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
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
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
Schmitz OJ (2007) Predator diversity and trophic interactions. Ecology 88:2415–2426. https://doi.org/10.1890/06-0937.1
Schmitz OJ (2010) Resolving Ecosystem Complexity. Princeton University Press, Princeton
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
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
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
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
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
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
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
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
Solomon ME (1949) The natural control of animal populations. J Anim Ecol 18:1–35. https://doi.org/10.2307/1578
Stephens DW, Brown JS, Ydenberg RC (2007) Foraging: behavior and ecology. University of Chicago Press, Chicago
Sunderland K (1999) Mechanisms underlying the effects of spiders on pest populations. J Arachnol 27:308–316
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
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
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
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
Toft S (1999) Prey choice and spider fitness. J Arachnol 27:301–307
Toft S (2005) The quality of aphids as food for generalist predators: implications for natural control of aphids. Eur J Entomol 102:371
Toft S (2013) Nutritional aspects of spider feeding. In: Nentwig W (ed) Spider ecophysiology. Springer-Verlag, Berlin
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
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
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
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
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
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
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
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
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
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
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
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
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
Wilder SM (2011) Spider nutrition: an integrated perspective. Adv Insect Physiol 40:87–136
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
Wise DH (1993) Spiders in ecological webs. Cambridge University Press, Cambridge
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
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
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
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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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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DOI: https://doi.org/10.1007/s00442-018-4313-1