Journal of Economic Entomology Advance Access published January 25, 2015 BIOLOGICAL
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MICROBIAL CONTROL
Functional Response, Prey Stage Preference, and Mutual Interference of the Tamarixia triozae (Hymenoptera: Eulophidae) on Tomato and Bell Pepper XIANG-BING YANG,1 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. 1–11 (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) (Hymenoptera: Eulophidae). Here, laboratory evaluations of host stage preference, parasitoid mutual interference, 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 preferences 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 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
Introduction The potato psyllid, Bactericera cockerelli (sˇulc), is a damaging insect pest of potato, tomato, and other cultivated solanaceous crops in the United States, Mexico, Central America, and New Zealand (Munyaneza et al. 2007; Hansen et al. 2008; Liefting et al. 2008; Munyaneza and Henne 2012). Potato psyllids damage plants by direct feeding and, more importantly, by transmitting the bacterial pathogen ‘Candidatus Liberibacter solanacearum (syn. psyllaurous)’ to solanaceous plants and causing zebra chip disease of potato (Hansen et al. 2008; Liefting et al. 2008). In the United States, millions of dollars in potato production losses have been reported, with severely affected potato farms being devastated by zebra chip disease, particularly in Texas (Goolsby et al. 2007). Currently, frequent insecticide applications to control B. cockerelli remain the optimal management option because of the need for immediate efficacy to control bacterialiferous adults (Goolsby et al. 2007; Gharalari et al. 2009; Yang et al. 2010). However, B. cockerelli are becoming resistant to some insecticides, leading to increased Liberibacter
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Corresponding author, e-mail:
[email protected].
transmission (Butler et al. 2011). Therefore, biological control of B. cockerelli by natural enemies and its compatibility with insecticide programs needs more attention. Previous studies of the potential for effective biological control of B. cockerelli are limited. Biological control has been used successfully in pest management programs for decades (van Lenteren and Woets 1988; Bailey et al. 2009), and incorporating beneficial predators and parasitoids in integrated pest management programs have helped reduce reliance on chemical control. Tamarixia triozae (Burks) (Hymenoptera: Eulophidae) is the only known arrhenotokous ectoparasitoid of nymphal B. cockerelli. Described previously as Tetrastichus sp. and Tetrastichus triozae, T. triozae is the current accepted name (Romney 1939; Burks 1943). In the United States and Mexico, T. triozae occur naturally in fields and greenhouses (Lomeli-Flores and Bueno 2002; Bravo and Lopez 2007). Previous field studies of T. triozae used brief scouting in potato and tomato fields, and high parasitoid pupal mortality (38–100%) and low parasitism rates (7 yr under laboratory conditions of 26.7 6 2 C, 75 6 5% relative humidity (RH), and a photoperiod of 14:10 (L:D) h. The B. cockerelli nymphs from heavily infested tomato plants were prepared for colonizing by T. triozae. T. triozae was originally collected in March 2013 from insecticide-free potato research fields located at the Texas A&M AgriLife Research and Extension Center at Weslaco, TX. Because T. triozae only parasitizes host nymphs, leaf samples containing B. cockerelli mummies were placed inside a polyvinyl chloride bucket (30 cm in diameter by 30 cm in height). A removable transparent container was attached to the top of the bucket lid, covering a 13-cm-diameter hole that was excised on the bucket lid to allow emerging T. triozae adults access to the transparent container. The lid of the transparent container was glued over the hole, and a smaller diameter hole was bored out of the lid. The buckets containing the mummy samples were placed on a light rack and emerging T. triozae inside the bucket accessed the transparent container by phototaxis. Newly emerged T. triozae adults were aspirated from the transparent container and released into a screen cage (60 by 60 by 60 cm [L by W by H]) containing tomato plants that were heavily infested with B. cockerelli nymphs. A cup holding a sterilized sponge that was soaked with a 10% honey (v:v) solution was hung inside the cage to feed adult T. triozae. When the nymph populations were low, additional B. cockerelli nymphs were supplied as needed. The T. triozae colony was maintained under similar laboratory conditions as that mentioned above. Tomato, S. lycopersicum L. (variety Florida Lanai), and bell pepper, Capsicum annuum L. (variety “Capistrano”) were seeded first in a foam tray with cone-shaped pots (3 by 3 by 4 cm) and maintained in a greenhouse at 28–32 C and under natural light conditions. One week after germination, the plant seedlings were individually transplanted into 1-liter plastic pots. The seedlings were fertilized weekly with 0.6 g liter1 Water Soluble Plant Food (N:P:K ¼ 15:30:15; Chemisco, Division of United Industries Corp. St. Louis, MO) and watered as needed. Four-week-old plants were used in all experiments. Host stage preference No-Choice Test. A no-choice experiment was conducted under laboratory conditions to determine female T. triozae parasitism efficiency on each of the five B. cockerelli nymphal stages. Using a sterilized blade, the top two or three fully expanded tomato and bell pepper leaves were excised from 4-wk-old greenhouse plants, and leaf petioles were immediately immersed into plastic transparent vials (10 ml) filled with reverse osmosis water. The vials and leaves were placed individually into transparent plastic containers (0.9 liter), of which the open top was covered with a
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YANG ET AL.: FUNCTIONAL RESPONSE, PREY STAGE PREFERENCE, AND MUTUAL INTERFERENCE
52-mesh polyethylene screen (Yang and Liu 2009). This setup was used for all experiments in the study. Using a camel hair paintbrush, 40 newly exuviated B. cockerelli nymphs of each instar were gently transferred onto the leaf within the transparent container to expose them to T. triozae parasitism. A preliminary experiment revealed B. cockerelli nymphs suffered no mortality when gently transferred with a camel hair paintbrush. Tomato leaves with numerous B. cockerelli mummies were collected from a T. triozae colony and placed in the clear container for T. triozae adult collection. Newly emerged T. triozae adults
