University of Nebraska - Lincoln DigitalCommons@University of Nebraska - Lincoln Faculty Publications: Department of Entomology Entomology, Department of 4-2020 Effect of Temperature on Plant Resistance to Arthropod Pests James R. Nechols Kansas State University, [email protected] Ashley R. Hough Kansas State University David C. Margolies Kansas State University, [email protected] John R. Ruberson University of Nebraska-Lincoln, [email protected] Brian P. McCornack Kansas State University, [email protected] See next page for additional authors Follow this and additional works at: https://digitalcommons.unl.edu/entomologyfacpub Part of the Entomology Commons Nechols, James R.; Hough, Ashley R.; Margolies, David C.; Ruberson, John R.; McCornack, Brian P.; Sandercock, Brett K.; and Murray, Leigh, "Effect of Temperature on Plant Resistance to Arthropod Pests" (2020). Faculty Publications: Department of Entomology. 853. https://digitalcommons.unl.edu/entomologyfacpub/853 This Article is brought to you for free and open access by the Entomology, Department of at DigitalCommons@University of Nebraska - Lincoln. It has been accepted for inclusion in Faculty Publications: Department of Entomology by an authorized administrator of DigitalCommons@University of Nebraska - Lincoln. Authors James R. Nechols, Ashley R. Hough, David C. Margolies, John R. Ruberson, Brian P. McCornack, Brett K. Sandercock, and Leigh Murray This article is available at DigitalCommons@University of Nebraska - Lincoln: https://digitalcommons.unl.edu/ entomologyfacpub/853 digitalcommons.unl.edu Effect of Temperature on Plant Resistance to Arthropod Pests James R. Nechols,1 Ashley R. Hough,1 David C. Margolies,1 John R. Ruberson,2 Brian P. McCornack,1 Brett K. Sandercock,3 and Leigh Murray4 1 Department of Entomology, Kansas State University, 2 Department of Entomology, University of Nebraska, 1603 Old Claflin Place, Manhattan, KS 66506 3 Department of Terrestrial Ecology, Norwegian Institute for Nature Research, 103 Entomology Hall, Lincoln, NE 68583 4 Department of Statistics, Kansas State University, 101 Dickens Hall, P.O. Box 5685 Torgarden, 7485 Trondheim, Norway Corresponding1116 Mid-Campus author —Drive J. R. Nechols,North, Manhattan, email [email protected] KS 66506 Abstract - bivorous arthropods, and it plays a key role in regulating the growth and development ofTemperature their host plants.has a strong In addition, influence temperature on the development, affects the survival, production and offecundity plant second of her- ary chemicals as well as structural characteristics used for defense against herbivores. Thus, temperature has potentially important implications for host plant resistance. Be- cause temperature directly impacts arthropod pests, both positively and negatively, dis- tinguishing direct effects from indirect effects mediated through host plants poses a challenge for researchers and practitioners. A more comprehensive understanding of Published in Environmental Entomology doi: 10.1093/ee/nvaa033 Copyright © 2020 by the authors. Published 49:3 by (2020), Oxford pp University 537–545 Press on behalf of Entomological Society of America. Used by permission. Submitted 6 December 2019; accepted 16 March 2020; published 13 April 2020. 1 Environmental Entomology 49 (2020) 2 Nechols et al. in would lead to better predictions of pest populations, and more effective use of plant resistancehow temperature as a management affects plant tactic. resistance Therefore, specifically, the goals and of arthropodthis paper pestsare to in 1) general, review and update knowledge about temperature effects on plant resistance, 2) evaluate al- ternative experimental approaches for separating direct from plant-mediated indirect and 3) offer recommendations for future research. effects of temperature on pests, including benefits and limitations of each approach, Keywords: temperature-induced effects host plant resistance, insect–plant interactions, plant-mediated effects, Temperature is an important environmental driver in the evolutionary ecology of plants and animals, and it plays a key role in shaping the life affects poikilotherms directly by setting upper and lower limits for de- velopmenthistories of andpoikilothermic survival, and organisms by regulating (Precht population et al. 1973a). growth Temperature through - - temperature-dependent processes. It also mediates plant–arthropod in teractions via direct effects on plants (Vegis 1973) and arthropods (Pre thatcht et impact al. 1973b), insect and herbivores indirectly include by influencing phytochemicals host plant produced quality for(Pisek de- fenseet al. 1973, by plants, Basra availability 2001). Temperature-induced of nutrients such as changessugars and in plantamino quality acids, and McClure 1983, Ishaaya 1986, Zhu-Salzman et al. 2008, Shuman and Baldwinand undigestible 2016). or impenetrable plant structures (Went 1953, Denno Host plant resistance is a pest management tactic that exploits nat- ural plant defenses, traditionally, through breeding programs designed antixenosisto augment (nonpreference)—physical traits that confer resistance and/or to pests chemical (Painter traits 1951, that causeBeck pests1965, to Smith avoid 2006). plants, Plants 2) antibiosis defend—plant themselves characteristics by three mechanisms: that negatively 1) tolerance—adaptations that allow plants to withstand or compensate for tissue damage or loss that would be del- affect pest fitness, and 3) - ent throughout a plant’s life cycle (constitutive resistance), or it may be elicitedeterious in to response susceptible to environmental plants (Painter stimuli 1951). such Resistance as feeding may by be insects pres (induced resistance) (Koch et al. 2016). An accumulating body of evidence indicates that a change in temper- ature elicits changes in plants that alter the expression of resistance to Environmental Entomology 49 (2020) 3 Nechols et al. in Thindwa and Teetes 1994, Chen et al. 2014, Hough 2016, Hough et al. insect pests. In some cases temperature enhances resistance (Sosa 1979,- 2017); in others it weakens it (Cartwright et al. 1946, Hackerott and Har- tersvey 1959,et al. 1991,McMurtry Harvey 1962, et al. Isaak 1994, et Richardsonal. 1963, Kindler 2011, and Chen Staples et al. 2014,1970, ChirumamillaWood and Starks et al.1972, 2014). Johnson And etin al.a few 1980, cases, Salim temperature and Saxena appears1991, Wal to have no effect on plant resistance (Dahms and Painter 1940, Jackai and Inang 1992, Randolph et al. 2008). may be related to a temperature-induced change in the expression of Altered fitness or population growth in an herbivorous insect pest also result from direct temperature effects. Distinguishing direct from plant resistance. However, a change in fitness or population growth can- ing accurate predictions of pest populations and associated crop dam- indirect temperature effects can be difficult, but it is essential for mak - tifyage. plantTo adequately and pest understandresponses underthe role different of temperature temperatures, in the expression including of plant resistance, more research is needed to characterize and quan paper has three aims: to 1) expand and update knowledge about tem- peraturethe thermally effects variable on plant conditions resistance that and occur associated in the field. pest Therefore, responses, our 2) compare different experimental approaches for elucidating tempera- ture effects on plant resistance, including ways to distinguish them from direct effects on arthropod pests, and 3) identify knowledge gaps and make recommendations for future research. Temperature Effects on Plant Resistance Currently, 26 experimental studies have investigated temperature to de- (Table 1). Of these, 21 studies, representing eight pest species— most oftermine them ifaphids—in it influences three the insectexpression orders of plantand four resistance families, to provideinsect pests ev- - idence that temperature modifies the level of plant resistance. In five- ingsother were studies, inconclusive temperature because either it was did not possibleappear to to influence distinguish plant direct re effectssistance of (Dahms temperature and Painter on pests 1940, from Randolphindirect effects et al. on2008), plant or resistance the find Environmental Entomology 49 (2020) 4 Nechols et al. in Table 1. Insect taxa for which temperature-induced changes in host plant resistance have been investigated Order Family Species Source Hemiptera Aphididae Schizaphis graminum Rondani HarveyWood and et al.Starks (1994) (1972) Greenbug ThindwaSchweissing and and Teetes Wilde (1994) (1979) Aphis glycines Matsumura Richardson (2011) Soybean aphid Chirumamilla et al. (2014) Hough (2016) Therioaphis maculata Hough et al. (2017) Spotted alfalfa aphid McMurtry (1962) (Buckton) IsaakHackerott et al. and (1963) Harvey (1959) Schalk et al. (1969) Acyrthosiphon pisum (Harris) KindlerDahms and and Painter Staples (1940)(1970)a Pea aphid Isaak et al. (1963) Aulacorthum solani (Kaltenbach) Walters et al. (1991) Foxglove aphid Diuraphis noxia Mordvilko Randolph et al. (2008)a Russian wheat aphid Cicadellidae Empoasca fabae (Harris) Casteel et al. (2006)a Delphacidae PotatoSogatella Leafhopper furcifera (Horváth) Salim and Saxena (1991) Whitebacked planthopper Coreidae Clavigralla tomentosicollis (Stål) Jackai and Inang 1992a Brown cowpea coreid bug Coleoptera Curculionidae Hypera postica Gyllenhal Johnson et al. (1980) Alfalfa weevil Diptera Cecidomyiidae Mayetiola destructor (Say) Cartwright et al. (1946) a Hessian