Hostname: page-component-586b7cd67f-t8hqh Total loading time: 0 Render date: 2024-11-27T00:59:01.215Z Has data issue: false hasContentIssue false
  • English
  • Français

Super-predation and intraguild interactions in a multi-predator-one-prey system alter the abundance and behaviour of green peach aphid (Hemiptera: Aphididae)

Published online by Cambridge University Press:  13 March 2020

Mouhammad Shadi Khudr Open the ORCID record for Mouhammad Shadi Khudr [Opens in a new window] ,
Lea Fliegner ,
Oksana Y. Buzhdygan  and
Susanne Wurst
Mouhammad Shadi Khudr*
Affiliation:
Faculty of Biology, Medicine and Health, The University of Manchester, Michael Smith Building, M13 9PT, Manchester, United Kingdom
Lea Fliegner
Affiliation:
Institute of Biology, Freie Universität Berlin, Altensteinstraße 34, 14195Berlin, Germany
Oksana Y. Buzhdygan
Affiliation:
Institute of Biology, Freie Universität Berlin, Altensteinstraße 34, 14195Berlin, Germany Department of Ecology and Biomonitoring, Chernivtsi National University, 58012Chernivtsi, Ukraine
Susanne Wurst
Affiliation:
Institute of Biology, Freie Universität Berlin, Altensteinstraße 34, 14195Berlin, Germany
*
*Corresponding author. Email: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

The dynamics of interactions amongst natural enemies are central to the investigation of insect pest ecology. Ternary and quaternary interactions between parasitoids and predators in the presence of entomophagous organisms are yet to be comprehensively explored. We investigated the performance of a clone of green peach aphid (Myzus persicae (Sulzer); Hemiptera: Aphididae), raised on savoy cabbage (Brassica oleracea Linnaeus; Brassicaceae), under all possible combinations of: I) the parasitoid Aphidius colemani Viereck (Hymenoptera: Braconidae); II) the predator Chrysoperla carnea (Stephens) (Neuroptera: Chrysopidae); III) the predator Adalia bipunctata (Linnaeus) (Coleoptera: Coccinellidae); and IV) the spider Parasteatoda tepidariorum (Koch) (Araneae: Theridiidae). We demonstrate a considerably differential green peach aphid abundance, polyphenism, and fine-scale spatial distribution in response to the combination, number, and identity of the present enemy species and their interactions. Surprisingly, certain combinations led to thriving green peach aphid populations due to interference between enemies; whereas, other combinations resulted in tangible collective suppression of the population. At the frontier of agroecology and entomology, we provide fresh insights on the effects of conflict and synergy between natural enemies sharing a pest of a cash crop as prey, highlighting the consequences of the presence of a novel synanthropic spider, as a top predator, on pest regulation.

Type
Research Papers
Information
The Canadian Entomologist , Volume 152 , Issue 2 , April 2020 , pp. 200 - 223
Copyright
© 2020 Entomological Society of Canada

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Footnotes

Subject editor: Christopher Cutler

References

Belgrad, B. and Griffen, B. 2016. Predator–prey interactions mediated by prey personality and predator hunting mode. Proceedings of the Royal Society B: Biological Sciences, 283: article 20160408, 1–8. http://doi.org/10.1098/rspb.2016.0408.CrossRefGoogle ScholarPubMed
Bell, A., Rader, R., Peck, S., and Sih, A. 2009. The positive effects of negative interactions: can avoidance of competitors or predators increase resource sampling by prey? Theoretical Population Biology, 76: 52–58. https://doi.org/10.1016/j.tpb.2009.03.008.CrossRefGoogle ScholarPubMed
Benelli, G., Messing, R., Wright, M., Giunti, G., Kavallieratos, N., and Canale, A. 2014. Cues triggering mating and host-seeking behavior in the aphid parasitoid Aphidius colemani (Hymenoptera: Braconidae: Aphidiinae): Implications for biological control. Journal of Economic Entomology, 107: 2005–2022. https://doi.org/10.1603/EC14291.CrossRefGoogle ScholarPubMed
Benjamin, S. and Zschokke, S. 2003. Webs of theridiid spiders: construction, structure and evolution. Biological Journal of the Linnean Society, 78: 293–305. https://doi.org/10.1046/j.1095-8312.2003.00110.x.CrossRefGoogle Scholar
Bilu, E. and Coll, M. 2009. Parasitized aphids are inferior prey for a coccinellid predator: implications for intraguild predation. Environmental Entomology, 3: 153–158. https://doi.org/10.1603/022.038.0119.CrossRefGoogle Scholar
Brahma, S., Sharma, D., Kundu, M., Saha, N., Saha, G., and Aditya, G. 2015. Intraguild predation in Heteroptera: effects of density and predator identity on Dipteran prey. Neotropical Entomology, 44: 374–384. http://doi.org/10.1007/s13744-015-0286-5.CrossRefGoogle ScholarPubMed
Breene, R., Dean, D., Nyffeler, M., and Edwards, G. 1993. Biology, predation ecology, and significance of spiders in Texas cotton ecosystems with a key to species. Texas Agriculture Experiment Station, College Station, Texas, United States of America. Available from https://conservation.unibas.ch/team/nyffeler/pdf/breene1993tab.pdf [accessed 19 January 2020].Google Scholar
Brodeur, J. and Rosenheim, J. 2000. Intraguild interactions in aphid parasitoids. Entomologia Experimentalis et Applicata, 97: 93–108. http://doi.org/10.1046/j.1570-7458.2000.00720.x.CrossRefGoogle Scholar
Buchanan, A., Hermann, S., Lund, M., and Szendrei, Z. 2017. A meta-analysis of non-consumptive predator effects in arthropods: the influence of organismal and environmental characteristics. Oikos, 126: 1233–1240. http://doi.org/10.1111/oik.04384.CrossRefGoogle Scholar
Cardinale, B., Harvey, C., Gross, K., and Ives, A. 2003. Biodiversity and biocontrol: emergent impacts of a multi-enemy assemblage on pest suppression and crop yield in an agroecosystem. Ecology Letters, 6: 857–865. http://doi.org/10.1046/j.1461-0248.2003.00508.x.CrossRefGoogle Scholar
Crawley, M. 2007. The R Book. John Wiley & Sons, New York, New York, United States of America.CrossRefGoogle Scholar
Crumrine, P. and Crowley, P. 2003. Partitioning components of risk reduction in a dragonfly–fish intraguild predation system. Ecology, 84: 1588–1597. https://doi.org/10.1890/00129658(2003)084[1588:PCORRI]2.0.CO;2.CrossRefGoogle Scholar
Davenport, J. and Chalcraft, D. 2013. Nonconsumptive effects in a multiple predator system reduce the foraging efficiency of a keystone predator. Ecology and Evolution, 3: 3063–3072. http://doi.org/10.1002/ece3.691.CrossRefGoogle Scholar
Dawkins, R. and Krebs, J. 1979. Arms races between and within species. Proceedings of the Royal Society B: Biological Sciences, 205: 489–511. https://doi.org/10.1098/rspb.1979.0081.Google ScholarPubMed
Dent, D. 2000. Insect pest management. Centre for Agriculture and Bioscience International, Wallingford, United Kingdom.CrossRefGoogle Scholar
Dinter, A. 2002. Microcosm studies on intraguild predation between female erigonid spiders and lacewing larvae and influence of single versus multiple predators on cereal aphids. Journal of Applied Entomology, 126: 249–257. http://doi.org/10.1046/j.1439-0418.2002.00638.x.CrossRefGoogle Scholar
Ferguson, K. and Stiling, P. 1996. Non-additive effects of multiple natural enemies on aphid populations. Oecologia, 108: 375–379. http://doi.org/10.1007/bf00334664.CrossRefGoogle ScholarPubMed
Fiedler, R. 2000. Parasteatoda tepidariorum, Animal diversity web [online]. Available from https://animaldiversity.org/accounts/Parasteatoda_tepidariorum [accessed 19 January 2020].Google Scholar
Fodrie, F., Kenworthy, M., and Powers, S. 2008. Unintended facilitation between marine consumers generates enhanced mortality for their shared prey. Ecology, 89: 3268–3274. https://doi.org/10.1890/07-1679.1.CrossRefGoogle ScholarPubMed
Fox, J. and Weisberg, S. 2011. An R companion to applied regression (second edition). Sage Puplications, Los Angeles, California, United States of America.Google Scholar
Greer, L. 2000. Greenhouse IPM: sustainable aphid control [online]. Appropriate Technology Transfer for Rural Areas (ATTRA), pest management technical note. Available from http://www.carolinafarmstewards.org/wp-content/uploads/2012/12/7-ATTRA-GH-Aphid.pdf [accessed 21 January 2020].Google Scholar
Griffen, B. and Byers, J. 2006. Intraguild predation reduces redundancy of predator species in multiple predator assemblage. Journal of Animal Ecology, 75: 959–966. https://doi.org/10.1111/j.1365-2656.2006.01115.x.CrossRefGoogle ScholarPubMed
Hajer, J. and Hrubá, L. 2006. Wrap attack of the spider Achaearanea tepidariorum (Araneae: Theridiidae) by preying on mealybugs Planococcus citri (Homoptera: Pseudococcidae). Journal of Ethology, 25: 9–20. http://doi.org/10.1007/s10164-006-0198-2.CrossRefGoogle Scholar
Harvell, C. 1990. The ecology and evolution of inducible defenses. The Quarterly Review of Biology, 65: 323–340. https://doi.org/10.1086/416841.CrossRefGoogle ScholarPubMed
Hénaut, Y., Machkour-M’rabet, S., and Lachaud, J. 2013. The role of learning in risk-avoidance strategies during spider–ant interactions. Animal Cognition, 17: 185–195. http://doi.org/10.1007/s10071-013-0651-x.CrossRefGoogle ScholarPubMed
Henry, L., Bannerman, J., Gillespie, D., and Roitberg, B. 2010. Predator identity and the nature and strength of food web interactions. Journal of Animal Ecology, 79: 1164–1171. http://doi.org/10.1111/j.1365-2656.2010.01723.x.CrossRefGoogle ScholarPubMed
Hermann, S. and Landis, D. 2017. Scaling up our understanding of non-consumptive effects in insect systems. Current Opinion in Insect Science, 20: 54–60. http://doi.org/10.1016/j.cois.2017.03.010.CrossRefGoogle ScholarPubMed
Hieber, C., Wilcox, S., Boyle, J., and Uetz, G. 2002. The spider and fly revisited: ploy-counterploy behavior in a unique predator-prey system. Behavioral Ecology and Sociobiology, 53: 51–60. http://doi.org/10.1007/s00265-002-0547-2.CrossRefGoogle Scholar
Hlivko, J. and Rypstra, A. 2003. Spiders reduce herbivory: nonlethal effects of spiders on the consumption of soybean leaves by beetle pests. Annals of the Entomological Society of America, 96: 914–919. https://doi.org/10.1603/00138746(2003)096[0914:SRHNEO]2.0.CO;2.CrossRefGoogle Scholar
Hodge, M. 1999. The implications of intraguild predation for the role of spiders in biological control. Journal of Arachnology, 27: 351–362.Google Scholar
Holt, R. and Polis, G. 1997. A theoretical framework for intraguild predation. The American Naturalist, 149: 745–764. http://doi.org/10.1086/286018.CrossRefGoogle Scholar
Hothorn, T., Bretz, F., and Westfall, P. 2008. Simultaneous inference in general parametric models. Biometrical Journal, 50: 346–363. https://doi.org/10.1002/bimj.200810425.CrossRefGoogle ScholarPubMed
Irwin, E., Kampmeier, G., and Weisser, W. 2007. Aphid movement: process and consequences. In Aphids as crop pests. Edited by van Emden, H. and Harrington, R.. Centre for Agriculture and Bioscience International, Wallingford, United Kingdom. Pp. 153–186.CrossRefGoogle Scholar
Janssen, A., Pallini, A., Venzon, M., and Sabelis, M. 1998. Review behaviour and indirect interactions in food webs of plant-inhabiting arthropods. Experimental and Applied Acarology, 22: 497–521. https://doi.org/10.1023/A:1006089924336.CrossRefGoogle Scholar
Jervis, M., Copland, M., and Harvey, J. 2005. The life cycle. In Insect as natural enemies: a practical perspective. Edited by Jervis, M.. Springer, Dordrecht, The Netherlands. Pp. 73–165.CrossRefGoogle Scholar
Khudr, M.S., Buzhdygan, O., Petermann, J., and Wurst, S. 2017. Fear of predation alters clone-specific performance in phloem-feeding prey. Scientific Reports, 7: article 7695, 1–10. https://doi.org/10.1038/s41598-017-07723-6.CrossRefGoogle ScholarPubMed
Khudr, M.S., Oldekop, J., Shuker, D., and Preziosi, R. 2013. Parasitoid wasps influence where aphids die via an interspecific indirect genetic effect. Biology Letters, 9: article 20121151, 1–4. https://doi.org/10.1098/rsbl.2012.1151.CrossRefGoogle ScholarPubMed
Kowles, K.A. 2015. Spatial and temporal dynamics of predator-prey interactions in winter wheat. Ph.D. dissertation. University of Kentucky, Lexington, Kentucky, United States of America. Available from http://uknowledge.uky.edu/entomology_etds/20 [accessed 21 January 2020].Google Scholar
Krause, J. and Ruxton, G. 2002. Living in groups. University Press Oxford, Oxford, United Kingdom.Google Scholar
Lang, A. 2003. Intraguild interference and biocontrol effects of generalist predators in a winter wheat field. Oecologia, 134: 144–153. http://doi.org/10.1007/s00442-002-1091-5.CrossRefGoogle Scholar
Lapchin, L. and Guillemaud, T. 2005. Asymmetry in host and parasitoid diffuse coevolution: when the red queen has to keep a finger in more than one pie. Frontiers in Zoology, 2: article 4, 1–5. http://doi.org/10.1186/1742-9994-2-4.CrossRefGoogle Scholar
Le Bourlot, V., Tully, T., and Claessen, D. 2014. Interference versus exploitative competition in the regulation of size-structured populations. The American Naturalist, 184: 609–623. https://doi.org/10.1086/678083.CrossRefGoogle ScholarPubMed
Lima, S. 1998. Nonlethal effects in the ecology of predator-prey interactions. Bioscience, 48: 25–34. http://doi.org/10.2307/1313225.CrossRefGoogle Scholar
Losey, J. and Denno, R. 1998. Positive predator-predator interactions: enhanced predation rates and synergistic suppression of aphid populations. Ecology, 79: 2143–2152. http://doi.org/10.2307/176717.Google Scholar
Lucas, E. 2005. Intraguild predation among aphidophagous predators. European Journal of Entomology, 102: 351–364. http://doi.org/10.14411/eje.2005.052.CrossRefGoogle Scholar
Lucas, E., Coderre, D., and Brodeur, J. 1997. Instar-specific defense of Coleomegilla maculata lengi (Col.: Coccinellidae): influence on attack success of the intraguild predator Chrysoperla rufilabris (Neur.: Chrysopidae). Entomophaga, 42: 3–12. https://doi.org/10.1007/BF02769874.CrossRefGoogle Scholar
Lucas, E., Coderre, D., and Brodeur, J. 1998. Intraguild predation among aphid predators: characterization and influence of extraguild prey density. Ecology, 79: 1084–1092. http://doi.org/10.2307/176603.CrossRefGoogle Scholar
Maloney, D., Drummond, F., and Alford, R. 2003. Spider predation in agro ecosystems: can spiders effectively control pest population? Maine Agricultural and Forest Experiments Station Technical Bulletin, 190: 1–32. Available from https://digitalcommons.library.umaine.edu/aes_techbulletin/18 [accessed 19 January 2020].Google Scholar
McAllister, M. and Roitberg, B. 1987. Adaptive suicidal behaviour in pea aphids. Nature, 328: 797–799. http://doi.org/10.1038/328797b0.CrossRefGoogle Scholar
McAllister, M., Roitberg, B., and Weldon, K. 1990. Adaptive suicide in pea aphids: decisions are cost sensitive. Animal Behaviour, 40: 167–175. http://doi.org/10.1016/s0003-3472(05)80676-1.CrossRefGoogle Scholar
McGregor, A., Hilbrant, M., Pechmann, M., Schwager, E., Prpic, N., and Damen, W. 2008. Cupiennius salei and Achaearanea tepidariorum: spider models for investigating evolution and development. Bioessays, 30: 487–498. http://doi.org/10.1002/bies.20744.CrossRefGoogle ScholarPubMed
Miller, J., Ament, J., and Schmitz, O. 2013. Fear on the move: predator hunting mode predicts variation in prey mortality and plasticity in prey spatial response. Journal of Animal Ecology, 83: 214–222. http://doi.org/10.1111/1365-2656.12111.CrossRefGoogle ScholarPubMed
Müller, C.B., Williams, I.S., and Hardie, J. 2001. The role of nutrition, crowding and interspecific interactions in the development of winged aphids. Ecological Entomology, 26: 330–340. http://doi.org/10.1046/j.1365-2311.2001.00321.x.CrossRefGoogle Scholar
Muratori, F., Rouyar, A., and Hance, T. 2014. Clonal variation in aggregation and defensive behavior in pea aphids. Behavioral Ecology, 25: 901–908. http://doi.org/10.1093/beheco/aru064.CrossRefGoogle Scholar
Nedvěd, O., Fois, X., Ungerová, D., and Kalushkov, P. 2013. Alien vs. predator – the native lacewing Chrysoperla carnea is the superior intraguild predator in trials against the invasive ladybird Harmonia axyridis. Bulletin of Insectology, 66: 73–78.Google Scholar
Nelson, E. and Rosenheim, J. 2006. Encounters between aphids and their predators: the relative frequencies of disturbance and consumption. Entomologia Experimentalis et Applicata, 118: 211–219. http://doi.org/10.1111/j.1570-7458.2006.00378.x.CrossRefGoogle Scholar
Nilsson, E., Hertonsson, P., Stenberg, M., Bodersen, J., Olsson, K., Stenroth, P., et al. 2006. Facilitation and interference among three predators affect their consumption of a stream-dwelling mayfly. Freshwater Biology, 51: 1507–1514. http://doi.org/10.1111/j.1365-2427.2006.01581.x.CrossRefGoogle Scholar
Nyffeler, M. 1982. Field studies on the ecological role of the spiders as insect predators in agroecosystems (abandoned grassland, meadows, and cereal fields). Ph.D. dissertation. Swiss Federal Institute of Technology, Zurich, Switzerland. Available from https://conservation.unibas.ch/team/nyffeler/pdf/nyffeler1982phd.pdf.Google Scholar
Nyffeler, M. and Benz, G. 1982. Kleptoparasitismus von juvenilen Kreuzspinnen und Skorpionsfliegen in den Netzen adulter Spinnen. Revue Suisse de Zoologie, 87: 907–918. Available from https://conservation.unibas.ch/team/nyffeler/pdf/nyffeler1980rsz.pdf [accessed 21 January 2020].CrossRefGoogle Scholar
Nyffeler, M. and Birkhofer, K. 2017. An estimated 400–800 million tons of prey are annually killed by the global spider community. The Science of Nature, 104: 30. https://doi.org/10.1007/s00114-017-1440-1.CrossRefGoogle ScholarPubMed
Nyffeler, M. and Sunderland, K. 2003. Composition, abundance and pest control potential of spider communities in agroecosystems: a comparison of European and US studies. Agriculture, Ecosystems & Environment, 95: 579–612. http://doi.org/10.1016/s0167-8809(02)00181-0.CrossRefGoogle Scholar
O’Hara, R. and Kotze, D. 2010. Do not log-transform count data. Methods in Ecology and Evolution, 1: 118–122. https://doi.org/10.1111/j.2041-210X.2010.00021.x.CrossRefGoogle Scholar
Omkar. 2016. Ecofriendly pest management for food security. Academic Press, London, United Kingdom.Google Scholar
Pennisi, E. 2017. Spider genes put a new spin on arachnids’ potent venoms, stunning silks, and surprising history [online]. Available from https://www.sciencemag.org/news/2017/10/spider-genes-put-new-spin-arachnids-potent-venoms-stunning-silks-and-surprising-history [accessed 21 January 2020].CrossRefGoogle Scholar
Polis, G. and Holt, R. 1992. Intraguild predation: the dynamics of complex trophic interactions. Trends in Ecology & Evolution, 7: 151–154. https://doi.org/10.1016/0169-5347(92)90208-S.CrossRefGoogle ScholarPubMed
Polis, G., Myers, C., and Holt, R. 1989. The ecology and evolution of intraguild predation: potential competitors that eat each other. Annual Review of Ecology, Evolution, and Systematics, 20: 297–330. http://doi.org/10.1146/annurev.es.20.110189.001501.CrossRefGoogle Scholar
Purandare, R., Tenhumberg, B., and Brisson, A. 2014. Comparison of the wing polyphenic response of pea aphids (Acyrthosiphon pisum) to crowding and predator cues. Ecological Entomology, 39: 263–266. http://doi.org/10.1111/een.12080.CrossRefGoogle ScholarPubMed
R Development Core Team. 2016. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Available from www.R-project.org [accessed 19 January 2020]Google Scholar
Rosenheim, J., Kaya, H., Ehler, L., Marois, J., and Jaffee, B. 1995. Intraguild predation among biological-control agents: theory and evidence. Biological Control, 5: 303–335. http://doi.org/10.1006/bcon.1995.1038.CrossRefGoogle Scholar
Rosenheim, J. and Wilhoit, L. 1993. Predators that eat other predators disrupt cotton aphid control. California Agriculture, 47: 7–9.Google Scholar
Rosenheim, J., Wilhoit, L., and Armer, C. 1993. Influence of intraguild predation among generalist insect predators on the suppression of an herbivore population. Oecologia, 96: 439–449. http://doi.org/10.1007/bf00317517.CrossRefGoogle ScholarPubMed
RStudio Team. 2017. RStudio: integrated development for R. RStudio, Boston, Massachusetts, United States of America. Available from http://www.rstudio.com [accessed 21 January 2020].Google Scholar
Rusch, A., Birkhofer, K., Bommarco, R., Smith, H., and Ekbom, B. 2015. Predator body sizes and habitat preferences predict predation rates in an agroecosystem. Basic and Applied Ecology, 16: 250–259. https://doi.org/10.1016/j.baae.2015.02.003.CrossRefGoogle Scholar
Samu, F. and Szinetár, C. 2002. On the nature of agrobiont spiders. Journal of Arachnology, 30: 389–402. http://doi.org/10.1636/0161-8202(2002)030[0389:otnoas]2.0.co;2.CrossRefGoogle Scholar
Şengonca, Ç. and Frings, B. 1985. Interference and competitive behaviour of the aphid predators, Chrysoperla carnea and Coccinella septempunctata in the laboratory. Entomophaga, 30: 245–251. http://doi.org/10.1007/bf02372225.CrossRefGoogle Scholar
Sih, A., Englund, G., and Wooster, D. 1998. Emergent impacts of multiple predators on prey. Trends in Ecology & Evolution, 13: 350–355. http://doi.org/10.1016/s0169-5347(98)01437-2.CrossRefGoogle ScholarPubMed
Snyder, W. and Ives, A. 2008. Behavior influences whether intra-guild predation disrupts herbivore suppression by parasitoids. In Behavioural ecology of insect parasitoids: from theoretical approaches to field applications (first edition). Edited by Wajnberg, E., Bernstein, C., and Van Alphen, J.. Blackwell, Oxford, United Kingdom. Pp. 71–91.CrossRefGoogle Scholar
Snyder, W. and Wise, D. 2001. Contrasting trophic cascades generated by a community of generalist predators. Ecology, 82: 1571–1583. https://doi.org/10.1890/00129658(2001)082[1571:CTCGBA]2.0.CO;2.CrossRefGoogle Scholar
Sokol-Hessner, L. and Schmitz, O. 2002. Aggregate effects of multiple predator species on a shared prey. Ecology, 83: 2367–2372. http://doi.org/10.2307/3071797.CrossRefGoogle Scholar
Sunderland, K., Crook, N., Stacey, D., and Fuller, B. 1987. A study of feeding by polyphagous predators on cereal aphids using ELISA and gut dissection. The Journal of Applied Ecology, 24: 907–933. http://doi.org/10.2307/2403989.CrossRefGoogle Scholar
Sunderland, K., Fraser, A., and Dixon, A.F.G. 1986. Field and laboratory studies on money spiders (Linyphiidae) as predators of cereal aphids. Journal of Applied Ecology, 23: 433–447. http://doi.org/10.2307/2404027.CrossRefGoogle Scholar
Symondson, W., Sunderland, K., and Greenstone, M. 2002. Can generalist predators be effective biocontrol agents? Annual Review of Entomology, 47: 561–594. http://doi.org/10.1146/annurev.ento.47.091201.145240.CrossRefGoogle ScholarPubMed
Szentkirályi, F. 2001. Ecology and habitat relationships. In Lacewings in the crop environment. Edited by McEwen, P.K., New, T.R., and Whittington, A.E.. Cambridge University Press, Cambridge, United Kingdom. Pp. 82–115.CrossRefGoogle Scholar
Tholt, G., Kis, A., Medzihradszky, A., Szita, É., Tóth, Z., Havelda, Z., and Samu, F. 2018. Could vectors’ fear of predators reduce the spread of plant diseases? Scientific Reports, 8: article 8705, 1–10. http://doi.org/10.1038/s41598-018-27103-y.CrossRefGoogle ScholarPubMed
Traugott, M., Bell, J., Raso, L., Sint, D., and Symondson, W. 2011. Generalist predators disrupt parasitoid aphid control by direct and coincidental intraguild predation. Bulletin of Entomological Research, 102: 239–247. http://doi.org/10.1017/s0007485311000551.CrossRefGoogle ScholarPubMed
Turchin, P. and Kareiva, P. 1989. Aggregation in Aphis varians: an effective strategy for reducing predation risk. Ecology, 70: 1008–1016. http://doi.org/10.2307/1941369.CrossRefGoogle Scholar
Uetz, G., Boyle, J., Hieber, C., and Wilcox, R. 2002. Antipredator benefits of group living in colonial web-building spiders: the ‘early warning’ effect. Animal Behaviour, 63: 445–452. http://doi.org/10.1006/anbe.2001.1918.CrossRefGoogle Scholar
Uma, D. and Weiss, M. 2012. Flee or fight: ontogenetic changes in the behavior of cobweb spiders in encounters with spider-hunting wasps. Environmental Entomology, 41: 1474–1480. http://doi.org/10.1603/en12126.CrossRefGoogle ScholarPubMed
Urban, M. 2008. The evolution of prey body size reaction norms in diverse communities. Journal of Animal Ecology, 77: 346–355. http://doi.org/10.1111/j.1365-2656.2007.01337.x.CrossRefGoogle ScholarPubMed
Vance-Chalcraft, H., Rosenheim, J., Vonesh, J., Osenberg, C., and Sih, A. 2007. The influence of intraguild predation on prey suppression and prey release: a meta-analysis. Ecology, 88: 2689–2696. http://doi.org/10.1890/06-1869.1.CrossRefGoogle ScholarPubMed
Vance-Chalcraft, H. and Soluk, D. 2005. Multiple predator effects result in risk reduction for prey across multiple prey densities. Oecologia, 144: 472–480. http://doi.org/10.1007/s00442-005-0077-5.CrossRefGoogle ScholarPubMed
Van Emden, H., Eastop, V., Hughes, R., and Way, M. 1969. The ecology of Myzus persicae. Annual Review of Entomology, 14: 197–270. http://doi.org/10.1146/annurev.en.14.010169.001213.CrossRefGoogle Scholar
Van Emden, H. and Harrington, R. 2007. Aphids as crop pests. Centre for Agriculture and Bioscience International, Wallingford, United Kingdom.CrossRefGoogle Scholar
Venables, W. and Ripley, B. 2002. Modern applied statistics with S (fourth edition). Springer, New York, New York, United States of America.CrossRefGoogle Scholar
Ver Hoef, J. and Boveng, P. 2007. Quasi-poisson vs. negative binomial regression: how should we model overdispersed count data? Ecology, 88, 2766–2772. https://doi.org/10.1890/07-0043.1.CrossRefGoogle ScholarPubMed
Villagra, C., Ramírez, C., and Niemeyer, H. 2002. Antipredator responses of aphids to parasitoids change as a function of aphid physiological state. Animal Behaviour, 64: 677–683. http://doi.org/10.1006/anbe.2002.4015.CrossRefGoogle Scholar
Vulinec, K. 1990. Collective security: aggregation by insects as a defense. In Insect defenses: adaptive mechanisms and strategies of prey and predators. Edited by Evans, D. and Schmidt, J.. State University of New York Press, Albany, New York, United States of America. Pp. 251–288.Google Scholar
Wente, R. 2014. Effects of intraguild cues of ground-dwelling and foliage-dwelling spiders on lady beetle oviposition and aphid suppression. Kaleidoscope, 11: article 88. Available from https://uknowledge.uky.edu/kaleidoscope/vol11/iss1/88 [accessed 19 January 2020].Google Scholar
Whitman, D. and Agrawal, A. 2009. What is phenotypic plasticity and why is it important?In Phenotypic plasticity of insects: mechanisms and consequences. Editied by Whitman, D.W. and Ananthakrishnan, T.N.. Science Publishers, Enfield, New Hampshire, United States of America. Pp. 1–63.CrossRefGoogle Scholar
Woodward, G., Ebenman, B., Emmerson, M., Montoya, J., Olesen, J., Valido, A., and Warren, P. 2005. Body size in ecological networks. Trends in Ecology & Evolution, 20: 402–409. https://doi.org/10.1016/j.tree.2005.04.005.CrossRefGoogle ScholarPubMed
Woodward, G. and Hildrew, A. 2002. Body-size determinants of niche overlap and intraguild predation within a complex food web. Journal of Animal Ecology, 71: 1063–1074. https://doi.org/10.1046/j.1365-2656.2002.00669.x.CrossRefGoogle Scholar
World Spider Catalog. 2016. World spider catalog, version 17.5 [online]. Available from http://wsc.nmbe.ch [accessed 19 January 2020].Google Scholar
Yasuda, H. and Kimura, T. 2001. Interspecific interactions in a tri-trophic arthropod system: effects of a spider on the survival of larvae of three predatory ladybirds in relation to aphids. Entomologia Experimentalis et Applicata, 98: 17–25. http://doi.org/10.1046/j.1570-7458.2001.00752.x.CrossRefGoogle Scholar
Young, S. 2017. A systematic review of the literature reveals trends and gaps in integrated pest management studies conducted in the United States. Pest Management Science, 73: 1553–1558. https://doi.org/10.1002/ps.4574.CrossRefGoogle ScholarPubMed
Yvon-Durocher, G., Reiss, J., Blanchard, J., Ebenman, B., Perkins, D., Reuman, D., et al. 2011. Across ecosystem comparisons of size structure: methods, approaches and prospects. Oikos, 120: 550–563. https://doi.org/10.1111/j.1600-0706.2010.18863.x.CrossRefGoogle Scholar
Zeileis, A., Kleiber, C., and Jackman, S. 2008. Regression models for count data in R. Journal of Statistical Software, 27 (8): 1–25. https://doi.org/10.18637/jss.v027.i08.CrossRefGoogle Scholar
Zevenbergen, J., Schneider, N., and Blackledge, T. 2008. Fine dining or fortress? Functional shifts in spider web architecture by the western black widow Latrodectus hesperus. Animal Behaviour, 76: 823–829. http://doi.org/10.1016/j.anbehav.2008.05.008.CrossRefGoogle Scholar
Supplementary material: File

Khudr et al. supplementary material

Khudr et al. supplementary material

Download Khudr et al. supplementary material(File)
File 1.3 MB