BIOLOGICAL CONTROL Functional Response of the Azalea Plant Bug (Heteroptera: Miridae) and a Green Lacewing Chrysoperla rufilabris (Neuroptera: Chrysopidae), Two Predators of the Azalea Lace Bug (Heteroptera: Tingidae) 1 2 COLIN D. STEWART, S. KRISTINE BRAMAN, AND ANDREW F. PENDLEY University of Georgia Department of Entomology, 1109Experiment Street, GrifÞn, GA 30223Ð1797 Environ. Entomol. 31(6): 1184Ð1190 (2002) ABSTRACT Azalea plant bug (Rhinocapsus vanduzeei Uhler) Þfth instars and a commercially obtained green lacewing (Chrysoperla rufilabris Burmeister) Þrst and second instars exhibited a type II functional response when caged with varying densities of fourth or Þfth instar azalea lace bug, Stephanitis pyrioides (Scott), prey. Attack coefÞcients for combined fourth and Þfth instar prey were statistically similar for R. vanduzeei and C. rufilabris (0.052 and 0.057, respectively). The handling time was signiÞcantly greater for R. vanduzeei (3.96 h) than C. rufilabris (2.41 h). Search efÞciency generally declined for both predators as initial azalea lace bug density increased. C. rufilabris killed signiÞcantly more fourth and Þfth instar prey than R. vanduzeei (8.0 and 6.0, respectively) in 24 h. Results indicate that C. rufilabris is a more suitable candidate for augmentative, not inoculative, release for azalea lace bug control than R. vanduzeei. However, R. vanduzeei can effect reductions in azalea lace bug populations in the landscape as a component of the guild of lace bugÕs natural enemies and should be considered in conservation efforts. KEY WORDS Augmentative release, Chrysoperla rufilabris, functional response, Stephanitis pyri- oides, Rhinocapsus vanduzeei, urban landscape AZALEAS ARE ONE of the most common landscape shrubs Uhler (Braman and Beshear 1994), and Stethoconus in the eastern United States. In Maryland, they rep- japonicus Schumacher (Henry et al. 1986, Neal et al. resented between 15 and 21% of the shrubbery or total 1991). D. rhododendri and R. vanduzeei are generalists. woody plant material monitored (Hellman et al. 1982, S. japonicus, an obligate lace bug predator (Neal and Holmes and Davidson 1984, Raupp and Noland 1984). Haldemann 1992), has been reported only in Belts- In the metropolitan Atlanta area, 87% of landscape ville, MD, and in Rockland County, NY (Schwartz managers reported azaleas among the plants that are 1989). most often treated with insecticides (Braman et al. The azalea plant bug, R. vanduzeei, described in 1998). The azalea lace bug, Stephanitis pyrioides 1890 (Uhler 1890), is a generalist predator found on (Scott), was Þrst reported in the United States by azaleas (Wheeler and Herring 1979) and raspberry Weiss (1916). It is the most important pest of azaleas (Van Duzee 1904). It is univoltine, and egg hatch is (Neal and Douglass 1988, Braman and Pendley 1992) synchronized with azalea bloom. R. vanduzeei has and has four generations a year in Georgia (Braman et been observed feeding on the azalea lace bug, white- al. 1992). Adults and nymphs feed on the underside of ßies, leafhoppers, aphids, small ßies, thrips (Braman the leaf by piercing and removing cell contents from and Beshear 1994), fall armyworm [Spodoptera frugi- the upper palisade parenchyma layer (Buntin et al. perda (J. E. Smith)] eggs and larvae, twospotted spider 1996) causing stippling and, in severe infestations, leaf mite (Tetranychus urticae Koch), azalea leafminer desiccation (Schultz 1993). [Caloptilia azaleella (Brants)] pupae, each other Few natural enemies of the azalea lace bug have (Stewart and Braman 1999), and azalea pollen been reported (Neal et al. 1991, Balsdon et al. 1996). (Wheeler and Herring 1979). This predator has been These include the mymarid, Anagrus takeyanus Gordh observed on Alabama (Rhododendron alabamense Re- (an egg parasitoid), and three predatory mirids Dicy- hder), Flame [Rhododendron austrinum (Small) Re- phus rhododendri Dolling, Rhinocapsus vanduzeei hder], Korean azaleas [Rhododendron yedoense Maxi- mowicz variety poukhanense (Leveille) Nakai], 1 Current address: University of Maine Pest Management OfÞce, Piedmont [Rhododendron calendulaceum (Michaux) 491 College Avenue, Orono, ME 04473Ð1295. Torrey], and wild swamp Rhododendron viscosum (L.) 2 E-mail: [email protected]Þn.peachnet.edu. Torrey, as well as the Ghent hybrids of the ßame 0046-225X/02/1184Ð1190$02.00/0 ᭧ 2002 Entomological Society of America December 2002 STEWART ET AL.: FUNCTIONAL RESPONSE OF AZALEA LACE BUG PREDATORS 1185 azalea. Its recorded range is from Quebec (Moore dishes with only a moist paper towel immediately 1907) and Maine to Florida and as far west as Missouri before testing. (Wheeler and Herring 1979). It has also been reported Problems with comparing functional response stud- in Manitoba, Canada (Henry and Wheeler 1988). ies in petri dishes with whole-plant Þeld studies have Green lacewings feed on a diverse array of arthro- been discussed in detail elsewhere (OÕNeil 1997). pod prey including azalea lace bugs (Principi and Cages containing azalea terminals were used instead Canard 1984, and references therein; Ehler and Kinsey of petri dishes in our studies to more closely simulate 1995; Shrewsbury and Smith-Fiola 2000). Although plant architecture and thus produce a more Þeld- little data for relative abundance of lacewing species applicable functional response curve (Messina and on azaleas exists, studies in Georgia indicate that C. Hanks 1998). Mesh screen (Chicopee Manufacturing rufilabris is the dominant species in Georgian pecan Co., Cornelia, GA) (4.96 ϫ 4.96 apertures/cm2) was orchards (Dinkins et al. 1994, Smith et al. 1995). Fur- attached to cover the 3.2-cm diameter hole in the base thermore, C. rufilabris seems better adapted than of the 11.0 cm ϫ 5.0 cm plastic cage (Thornton Plastic Chrysoperla carnea Stephens to the more humid con- Co., Salt Lake City, UT) (Klingeman et al. 2000a). ditions in the southeastern United States (Tauber and Inner cage surface area equaled 212.1 cm2. An azalea Tauber 1983). terminal (Rhododendron obtusum ÔHinodegiriÕ) with The functional response, Þrst discussed by Solomon four to seven leaves was inserted through a 2.0-cm long (1949), describes the relationship between prey den- section of 6.4-mm i.d. Nalgene Grade VI Premium sity and the number of prey consumed by an individ- NonToxic Tubing (Nalge Co., Rochester, NY) and ual predator. Holling (1959) described three possible sealed using ParaÞlm “M” Laboratory Film (American responses in which the number of prey consumed rises Can Co., Greenwich, CT) (Klingeman et al. 2000a). linearly, hyperbolically, or sigmoidally, for a type I, The stem was inserted through a 0.95-cm diameter type II, and type III response, respectively. The gen- hole in the lower half of a Falcon 1007 60 ϫ 15 mm eralist predatory mirid Deraeocoris nebulosus Uhler petri dish (Becton Dickinson, Lincoln Park, NJ), exhibited a type II response, characteristic of most which served as the bottom of the cage. Azalea lace arthropod predators, when challenged with varying bugs do not feed on new growth; thus terminal foliage levels of oak lace bug [Corythuca arcuata (Say)] was removed. The stem was in contact with 60 ml of fourth and Þfth instars (Wheeler et al. 1975). C. rufi- water contained in a 120-ml plastic cup. labris exhibited a type I or a type II functional re- One, 3, 5, 10, 15, 20, 25, and 30 Þfth instar azalea lace sponse when fed cotton aphids (Aphis gossypii bugs were placed on the top of the foliage. One Þfth Glover) or Heliothis virescens (F.) eggs or larvae (Nor- instar R. vanduzeei was introduced on the bottom dlund and Morrison 1990). portion of the stem. Controls were maintained without In our study, the functional response, handling time, the predator present. After 24 h, the predator was and attack coefÞcient of R. vanduzeei and C. rufilabris removed from the cage, and the number of live azalea to fourth or Þfth instar azalea lace bugs, Stephanitis lace bugs was determined. All tests were performed in pyrioides, on azaleas were determined, as was the an environmental chamber (Percival Co., Boone, IA) number of azalea lace bugs killed in 24 h. at 21ЊC, 91% RH, and a photoperiod of 14:10 (L:D) h. Stem length and diameter were measured, and leaf area was determined using a Li-Cor model 3100 leaf Materials and Methods area meter (Li-Cor, Lincoln, NE). The experiment Azalea lace bugs were collected in GrifÞn, GA, and was repeated on seven occasions until a minimum of were kept in 1.0 m3 screened cages at 27 Ϯ 1ЊC and a 15 replications at all densities were obtained. The photoperiod of 14:10 (L:D) h, and fed azaleas (various experiment was also repeated simultaneously on seven cultivars) as needed. occasions using fourth instar azalea lace bugs as prey Immature R. vanduzeei were collected from native at all densities. azaleas, Rhododendron canescens (Michaux) Sweet, Commercially obtained, “prefed” late Þrst or early and Rhododendron austrinum at Callaway Gardens second instar green lacewings (BeneÞcial Insectary, (Pine Mountain, GA) on 9, 13, 20 April 1999 by beating Oak Run, CA) were tested using the system described, the foliage over a 40 cm ϫ 24 cm enamel pan. They except the larvae were not starved for 24 h but were were placed in individual 11 cm diameter ϫ 2.4 cm used within 18 h from the time they were received. petri plates containing one fall armyworm egg mass, an Preliminary data indicated that the Þrst and second azalea leaf, and piece of damp paper towel. The dishes instars were capable of capturing and killing azalea were placed in an environmental chamber (Percival lace bug fourth and Þfth instars. Tests were conducted Co., Boone, IA) at 21ЊC, 91% RH, and a photoperiod using 1, 3, 5, 10, 15, 20, 30, and 40 azalea lace bug fourth of 14:10 (L:D) h. The predators were checked every or Þfth instars per cage. Leaf area was determined as 24 h to determine if they had molted.