University of Kentucky UKnowledge Entomology Faculty Publications Entomology 8-4-2017 Natural Enemies Partially Compensate for Warming Induced Excess Herbivory in an Organic Growth System Orsolya Beleznai Hungarian Academy of Sciences, Hungary Jamin Dreyer University of Kentucky, [email protected] Zoltán Tóth Hungarian Academy of Sciences, Hungary Ferenc Samu Hungarian Academy of Sciences, Hungary Right click to open a feedback form in a new tab to let us know how this document benefits oy u. Follow this and additional works at: https://uknowledge.uky.edu/entomology_facpub Part of the Animal Sciences Commons, Ecology and Evolutionary Biology Commons, and the Entomology Commons Repository Citation Beleznai, Orsolya; Dreyer, Jamin; Tóth, Zoltán; and Samu, Ferenc, "Natural Enemies Partially Compensate for Warming Induced Excess Herbivory in an Organic Growth System" (2017). Entomology Faculty Publications. 124. https://uknowledge.uky.edu/entomology_facpub/124 This Article is brought to you for free and open access by the Entomology at UKnowledge. It has been accepted for inclusion in Entomology Faculty Publications by an authorized administrator of UKnowledge. For more information, please contact [email protected]. Natural Enemies Partially Compensate for Warming Induced Excess Herbivory in an Organic Growth System Notes/Citation Information Published in Scientific Reports, v. 7, article 7266, p. 1-9. © The Author(s) 2017 This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/. Digital Object Identifier (DOI) https://doi.org/10.1038/s41598-017-07509-w This article is available at UKnowledge: https://uknowledge.uky.edu/entomology_facpub/124 www.nature.com/scientificreports OPEN Natural enemies partially compensate for warming induced excess herbivory in an organic Received: 31 March 2017 Accepted: 29 June 2017 growth system Published: xx xx xxxx Orsolya Beleznai1, Jamin Dreyer2, Zoltán Tóth3 & Ferenc Samu1 Predators can limit prey abundance and/or levels of activity. The magnitudes of these efects are contingent on predator and prey traits that may change with environmental conditions. Aberrant thermal regimes could disrupt pest suppression through asymmetric efects, e.g. heat-sensitive predator vs. heat-tolerant prey. To explore potential efects of warming on suppressing pests and controlling herbivory in a vegetable crop, we performed laboratory experiments exposing an important pest species to two spider predator species at diferent temperatures. Heat tolerance was characterised by the critical thermal maxima parameter (CTM50) of the cucumber beetle (Diabrotica undecimpunctata), wolf spider (Tigrosa helluo), and nursery web spider (Pisaurina mira). Cucumber beetles and wolf spiders were equally heat tolerant (CTM50 > 40 °C), but nursery web spiders had limited heat tolerance (CTM50 = 34 °C). Inside mesocosms, beetle feeding increased with temperature, wolf spiders were always efective predators, nursery web spiders were less lethal at high temperature (38 °C). Neither spider species reduced herbivory at ambient temperature (22 °C), however, at warm temperature both species reduced herbivory with evidence of a dominant non-consumptive efect. Our experiments highlight the contingent nature of predator-prey interactions and suggest that non- consumptive efects should not be ignored when assessing the impact of temperature change. Predators can negatively impact prey populations either by directly consuming prey individuals or through non-consumptive efects (NCEs) that trigger costly anti-predator reaction in prey1. Te wide ranging behavioural responses of prey to the presence or cues of predators may result in decreased feeding2, lower quality diet3, 4 or physiological stress5. Predator efects have the potential to cascade through ecological systems, afecting produc- tivity and ecosystem functioning at the lower levels of the food web6 and shaping ecological interactions spatially7. Elements at both sides of this interaction, predator activity, performance and the success or failure of the prey’s anti-predator behaviour are contingent on environmental factors. Tese efects gain economic importance in the natural enemy – pest context, especially in the view of global climate change. With climate change both mean summer temperatures and temperature variability are projected to increase8. Tis results in the more frequent occurrence of climate extremes, such as heatwaves9, which may have particularly large impact on ecological systems10. Studies in natural ecosystems11, 12 suggest that the outcome of predator-prey interactions can be especially temperature sensitive, because diferences in temperature tolerance of the interact- ing species can magnify the response13. In agroecosystems natural enemy – pest interactions are in the focus of biological control research since any shif in the efciency of biological control processes has paramount economic importance. Not only expected elevated temperatures arising from global climate change, but also high temper- atures caused by some agricultural practices, such as greenhouse growing14, plastic mulch and foil covers15, 16 make it necessary to study how diferent interactions may change under altered thermal conditions. Research has been done on how plant-herbivore interactions are afected by rising temperatures, reviewed by Bale et al.17. 1Department of Zoology, Plant Protection Institute, Centre for Agricultural Research, Hungarian Academy of Sciences, Budapest, Nagykovácsi út 26-30, H-1029, Hungary. 2Department of Entomology, University of Kentucky, S-225 Ag Science Center N Lexington, Kentucky, 40506-0091, USA. 3Lendület Evolutionary Ecology Research Group, Plant Protection Institute, Centre for Agricultural Research, Hungarian Academy of Sciences, Budapest, Herman Ottó út 15, H-1022, Hungary. Correspondence and requests for materials should be addressed to O.B. (email: beleznai. [email protected]) SCIENTIFIC REPORTS | 7: 7266 | DOI:10.1038/s41598-017-07509-w 1 www.nature.com/scientificreports/ More recently, studies have addressed the question of how herbivore – natural enemy interactions might respond to climate change18, 19, but we still need more studies to understand complex, multitrophic and non-consumptive efects of rising temperatures20, 21. Te present study examines how a ‘crop - herbivore pest – generalist predators’ system responds to temperature changes. Te tritrophic system of ‘organically grown cucumber crop –cucumber beetle – two species of spider natu- ral enemies’ is a highly relevant model system for studying the temperature sensitivity of trophic interactions. Despite the importance of cucurbit crops, organic farmers largely avoid growing them because feeding damage by insect pests and spread of pathogens can account for as much as 80% loss in the marketable product22. One of the major pests is the spotted cucumber beetle, Diabrotica undecimpunctata howardi (Barber, 1947). Both organic and conventional growers rank the cucumber beetle/bacterial wilt complex as one of the most important and least controllable threat to cucumber crop23. Current organic management options include using polypropylene fabric row covers to keep out pests, and organic insecticides combined with proper planting dates24. Row covers applied in this practice highly increase crop temperature. Natural enemies, including spiders, have been shown to be important in organic cucurbit systems because early in the season they were able to reduce the densities of striped cucumber beetles and cause fruit production to increase25, 26. As a result of the NCE of wolf spiders, cucumber beetles were shown to modify their behaviour, including a reduced feeding activity on plants, which resulted in nearly 50% reduction in feeding damage27, 28. Since spiders are efective predators and biological control agents, some aspects of the temperature dependence of their direct efect and NCE on prey have already received some attention in the literature. In Barton’s29 study of grassland ecosystems, warming had no direct efect on herbivores, but it did decrease spider activity which caused a reduced predation risk for herbivores. Lubin and Henschel30 also demonstrated that in spiders high daytime temperatures may restrict the time available for foraging. At the same time, higher temperatures can increase herbivore activity, translating to a greater amount of host plant consumption17. Te interaction of spider and herbivore thermal responses is exemplifed in an old feld case study where grasshoppers could reduce predator encounters by becoming more active during the hottest parts of the day when spiders reduced their activity to avoid thermal stress31. Te outcome of such interactions depends on the individual thermal tolerances of the con-