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Yang-Et-Al-2015 BIOLOGICAL AND MICROBIAL CONTROL Functional Response, Prey Stage Preference, and Mutual Interference of the Tamarixia triozae (Hymenoptera: Eulophidae) on Tomato and Bell Pepper 1 XIANG-BING YANG, MANUEL CAMPOS-FIGUEROA, ADRIAN SILVA, AND DONALD C. HENNE Texas A&M AgriLife Research and Extension Center, Texas A&M University System, Weslaco, TX 78596 USA. J. Econ. Entomol. 108(2): 414–424 (2015); DOI: 10.1093/jee/tou048 ABSTRACT The potato psyllid, Bactericera cockerelli (sˇulc), has been detrimental to potato, tomato, and other solanaceous crop production in many countries. Management of B. cockerelli is dominated by frequent insecticide applications, but other approaches need consideration, including biological control. The sole arrhenotokous ectoparasitoid of nymphal potato psyllids is Tamarixia triozae (Burks) (Hyme- noptera: Eulophidae). Here, laboratory evaluations of host stage preference, parasitoid mutual interfer- Downloaded from ence, and functional response of T. triozae were conducted with varying host B. cockerelli nymphal stages and densities on both tomato and bell pepper plant leaves. Significant differences in prey stage prefer- ences were found on both host plants. In a no-choice host stage test, significantly greater parasitism of fourth- and fifth-instar B. cockerelli nymphs occurred, and no parasitism of first or second instars was found. Similar preferences were found in a host stage choice test. Effect of mutual interference on per capita female parasitism was significant when confining two or three simultaneously ovipositing female http://jee.oxfordjournals.org/ T. triozae adults on a given host density versus solitary females. The per capita search efficiency (s)of female T. triozae was significantly and negatively correlated with T. triozae density. The functional response of T. triozae to nymphal B. cockerelli was a Type III form on both host plants. In addition, host plant type did not exert a significant bottom-up effect on either parasitism or functional response of female T. triozae. The feasibility of using bell pepper as a potential banker plant for T. triozae augmentation is also discussed. KEY WORDS Tamarixia triozae, functional response, searching efficiency, mutual interference, parasitism by guest on October 3, 2016 Introduction transmission (Butler et al. 2011). Therefore, biological control of B. cockerelli by natural enemies and its com- The potato psyllid, Bactericera cockerelli (sˇulc), is a patibility with insecticide programs needs more atten- damaging insect pest of potato, tomato, and other culti- tion. Previous studies of the potential for effective vated solanaceous crops in the United States, Mexico, biological control of B. cockerelli arelimited.Biological Central America, and New Zealand (Munyaneza et al. control has been used successfully in pest management 2007; Hansen et al. 2008; Liefting et al. 2008; Munya- programs for decades (van Lenteren and Woets 1988; neza and Henne 2012). Potato psyllids damage plants Bailey et al. 2009), and incorporating beneficial preda- by direct feeding and, more importantly, by transmit- tors and parasitoids in integrated pest management ting the bacterial pathogen ‘Candidatus Liberibacter programs have helped reduce reliance on chemical solanacearum (syn. psyllaurous)’ to solanaceous plants control. and causing zebra chip disease of potato (Hansen et al. Tamarixia triozae (Burks) (Hymenoptera: Eulophidae) 2008; Liefting et al. 2008). In the United States, mil- is the only known arrhenotokous ectoparasitoid of nym- lions of dollars in potato production losses have been phal B. cockerelli. Described previously as Tetrastichus reported, with severely affected potato farms being sp. and Tetrastichus triozae, T. triozae is the current ac- devastated by zebra chip disease, particularly in Texas cepted name (Romney 1939; Burks 1943). In the United (Goolsby et al. 2007). Currently, frequent insecticide States and Mexico, T. triozae occur naturally in fields applications to control B. cockerelli remain the optimal and greenhouses (Lomeli-Flores and Bueno 2002; Bravo management option because of the need for immediate and Lopez 2007). Previous field studies of T. triozae efficacy to control bacterialiferous adults (Goolsby used brief scouting in potato and tomato fields, and high et al. 2007; Gharalari et al. 2009; Yang et al. 2010). parasitoid pupal mortality (38–100%) and low parasitism However, B. cockerelli are becoming resistant to some rates (<20%) were present owing to factors such as fun- insecticides, leading to increased Liberibacter gal diseases and predation (Johnson 1971;Yangand Henne unpublished data). Otherwise, no comprehensive studies of T. triozae host–parasitoid interactions have been reported, particularly functional responses, host 1 Corresponding author, e-mail: [email protected]. stage preferences, or parasitoid mutual interference. VC The Authors 2015. Published by Oxford University Press on behalf of Entomological Society of America. All rights reserved. For Permissions, please email: [email protected] April 2015 YANG ET AL.: FUNCTIONAL RESPONSE,PREY STAGE PREFERENCE, AND MUTUAL INTERFERENCE 415 Functional responses elucidate the relationship be- the Texas A&M AgriLife Research and Extension Cen- tween proportions of hosts consumed/parasitized by a ter at Weslaco, TX, in 2006. B. cockerelli from this col- predator/parasitoid at increasing host densities up to a lection were maintained within screen cages on tomato, maximum, or satiation, level and are key to understand- Solanum lycopersicum L. (variety “Florida Lanai”), for ing how a predator or parasitoid behaves under differ- >7 yr under laboratory conditions of 26.7 6 2C, ent host population densities (Holling 1959). Such 75 6 5% relative humidity (RH), and a photoperiod of studies are important for predicting successful field re- 14:10 (L:D) h. The B. cockerelli nymphs from heavily leases of biological control agents (Xiao and Fadamiro infested tomato plants were prepared for colonizing by 2010). Predator–prey functional responses relationships T. triozae. are generally modeled by three empirical relationships: T. triozae was originally collected in March 2013 linear (Type I), convex (Type II), and sigmoid (Type from insecticide-free potato research fields located at III; Holling 1959, 1961, 1966; Trexler et al. 1988; the Texas A&M AgriLife Research and Extension Cen- Timms et al. 2008). Type I models characterize an line- ter at Weslaco, TX. Because T. triozae only parasitizes arly increasing predation rate where predators attack host nymphs, leaf samples containing B. cockerelli prey randomly, and the proportion of prey consumed mummies were placed inside a polyvinyl chloride increases when prey density increases, up to a maxi- bucket (30 cm in diameter by 30 cm in height). mum level where the attack rate becomes constant. A removable transparent container was attached to the Type II and III models describe predator–prey rela- top of the bucket lid, covering a 13-cm-diameter hole tionships that are nonlinear between the proportion of that was excised on the bucket lid to allow emerging Downloaded from prey consumed and prey density; in a Type II func- T. triozae adults access to the transparent container. tional response, the proportion of prey consumed is a The lid of the transparent container was glued over the hyperbolic curve, and in Type III, it is a sigmoidal hole, and a smaller diameter hole was bored out of the curve. In both Type II and Type III models, the pro- lid. The buckets containing the mummy samples were portion of prey consumed reaches an asymptote be- placed on a light rack and emerging T. triozae inside cause of the time required for handling prey (Chong the bucket accessed the transparent container by pho- http://jee.oxfordjournals.org/ and Oetting 2006; Parajulee et al. 2006). Hence, under- totaxis. Newly emerged T. triozae adults were aspirated standing the functional response of T. triozae is critical from the transparent container and released into a to capture details of its predation and parasitism behav- screen cage (60 by 60 by 60 cm [L by W by H]) con- ior, and will also facilitate conservation of beneficial taining tomato plants that were heavily infested with natural enemies (Parajulee et al. 2006). B. cockerelli nymphs. A cup holding a sterilized sponge Augmentation of natural enemies is an important as- that was soaked with a 10% honey (v:v) solution was pect of biological control. Banker plants application hung inside the cage to feed adult T. triozae.Whenthe provides a sustainable reproducing population of natu- nymph populations were low, additional B. cockerelli ral enemies within the selected crops or plants to pro- nymphs were supplied as needed. The T. triozae colony by guest on October 3, 2016 vide long-term pest suppression (Frank 2009). The was maintained under similar laboratory conditions as critical step in a successful banker plant system is to that mentioned above. find host plants, often noncultivated, that are tolerant Tomato, S. lycopersicum L. (variety Florida Lanai), of the pest host, will attract beneficial natural enemies, and bell pepper, Capsicum annuum L. (variety and will serve as alternative food or host for natural en- “Capistrano”) were seeded first in a foam tray with emies to reproduce sustainably to control the target cone-shaped pots (3 by 3 by 4 cm) and maintained in a pest on the primary crop (Bennison 1992; Bennison greenhouse at 28–32C and under natural light condi- and Corless
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