PROC. ENTOMOL. SOC. WASH. 112(1), 2010, pp. 61–68

STANTONIA PALLIDA (ASHMEAD) (HYMENOPTERA: BRACONIDAE) REARED FROM NEOMUSOTIMA CONSPURCATALIS WARREN (LEPIDOPTERA: CRAMBIDAE), A CLASSICAL BIOLOGICAL CONTROL AGENT OF LYGODIUM MICROPHYLLUM (CAV.) R. BR. (POLYPODIALES: LYGODIACEAE)

ROBERT R. KULA,ANTHONY J. BOUGHTON, AND ROBERT W. PEMBERTON

(RRK) Systematic Entomology Laboratory, Plant Sciences Institute, Agricultural Research Service, U.S. Department of Agriculture, c/o National Museum of Natural History, Smithsonian Institution, P.O. Box 37012, MRC 168, Washington, DC 20013-7012, U.S.A. (e-mail: [email protected]); (AJB, RWP) Invasive Plant Research Laboratory, Agricultural Research Service, U.S. Department of Agriculture, 3225 College Avenue, Fort Lauderdale, Florida 33314 U.S.A. (e-mail: AJB [email protected], RWP [email protected])

Abstract.—Stantonia pallida (Ashmead) sensu Braet and Quicke (2004) is reported from Neomusotima conspurcatalis Warren (Lepidoptera: Crambidae), a classical biological control agent of Lygodium microphyllum (Cav.) R. Br. (Polypodiales: Lygodiaceae) in Florida. It is the first reported parasitoid of N. conspurcatalis. One undetermined species each of Cotesia Cameron, Glyptapan- teles Ashmead, and Rhygoplitis Mason (Hymenoptera: Braconidae) are likely parasitoids of N. conspurcatalis but need to be confirmed through rearing from host larvae isolated individually. The use of S. pallida, under the name Stantonia lamprosemae Muesebeck, for control of Diaphania hyalinata (Linnaeus) and Diaphania nitidalis (Stoll) (Lepidoptera: Pyralidae) in Florida is reviewed and used to illustrate the importance of systematics and natural history collections to classical biological control. The potential effects of these parasitoids on control of L. microphyllum in Florida are discussed.

Key Words: Cotesia, Glyptapanteles, host record, invasive species, melonworm, Microgastrinae, nontarget effects, Old World climbing fern, Omiodes indicata, Orgilinae, pickleworm, Rhygoplitis, soybean leaffolder DOI: 10.4289.0013.8797.112.1.253.61

Lygodium microphyllum (Cav.) R. Palearctic regions (Pemberton 1998). It Br., Old World climbing fern, is an was first collected in Florida in 1958 invasive weed in Florida. It is endemic (Beckner 1968), but the earliest record to tropical and subtropical areas of the of it occurring as a naturalized plant in Australasian, Oriental, Oceanic, and the state is 1965 (Nauman and Austin 1978, Pemberton and Ferriter 1998). Its * Accepted by Michael W. Gates south to north range in Florida as of 62 PROCEEDINGS OF THE ENTOMOLOGICAL SOCIETY OF WASHINGTON

2006 was from Monroe County to L. microphyllum, and reiterate the Volusia County (Ferriter and Pernas importance of systematics and national 2006), an area that covers approximate- history collections to classical biologi- ly the southern two-thirds of peninsular cal control. Florida. It is listed as a noxious weed (DPI-FDACS 2006) and Class I invasive MATERIALS AND METHODS species (FLEPPC 2007) in Florida. Braconids reared in this study were Pemberton and Ferriter (1998), Pember- from N. conspurcatalis larvae collected ton et al. (2002), and Hutchinson et al. from August 2008 to March 2009 on L. (2006) detailed the characteristics that microphyllum in Jonathan Dickinson make this plant invasive, the threat it State Park, Martin County, Florida. At poses to ecosystems and natural resourc- each release site, collections of 50 es in Florida, methods used for control, mixed-instar N. conspurcatalis larvae and ecological/economic loss associated were made into 48-oz (20 3 20 3 6-cm) with the plant. Given the ineffectiveness clear plastic deli boxes (Genpakt, Glen of mechanical removal and prescribed Falls, NY) by clipping off individual burning and expense of chemical con- caterpillar-infested pinnae (leaflets) of trol, classical biological control is con- L. microphyllum. The second author sidered the best option for long-term examined collections under a stereomi- control (Pemberton 1998, Hutchinson et croscope in the laboratory to confirm al. 2006) and was initiated in 1997 the identity and number of N. conspur- (Pemberton et al. 2002). After foreign catalis larvae and ensure that no exploration for candidate biological unhatched eggs or other host species control agents (Pemberton et al. 2002, were in the boxes. All larvae were Goolsby et al. 2003) and host range active at the initial laboratory examina- testing of select agents (Goolsby et al. tion, and ectoparasitoids were not 2003, Goolsby et al. 2005, Boughton et observed. Lygodium microphyllum fo- al. 2009), the crambid Neomusotima liage was added to the rearing boxes as conspurcatalis Warren, known from the food for N. conspurcatalis larvae, and it Australasian, Oriental, and Palearctic was examined prior to addition to insure regions (Goolsby et al. 2003, Solis et al. that no other eggs or insect hosts were 2004), was released in Florida in 2007 introduced. Collections were incubated (Boughton et al. 2009) and has now in the laboratory at 258C and checked established populations at release sites daily for parasitoid emergence. The in southern Florida (Boughton and second author observed, after the initial Pemberton In press). examination, five unusually swollen and The second author recently reared the lethargic N. conspurcatalis larvae from orgiline braconid Stantonia pallida the March 2009 collection and placed (Ashmead) from field-collected N. con- them in separate vials to associate each spurcatalis larvae feeding on L. micro- parasitoid with its host. phyllum in Florida and also reared Specimens of Braconidae were dehy- microgastrine braconids in the genera drated following Heraty and Hawks Cotesia Cameron, Glyptapanteles Ash- (1998) and subsequently identified to mead, and Rhygoplitis Mason that are genus using keys in Achterberg (1997) likely parasitoids of N. conspurcatalis and Whitfield (1997). Stantonia pallida on L. microphyllum. The objectives of was identified initially using the key this article are to report these host and diagnosis in Braet and Quicke records, discuss how parasitism of N. (2004). The identification was con- conspurcatalis might affect control of firmed through comparison to the holo- VOLUME 112, NUMBER 1 63 type and five paratypes of Stantonia lamprosemae Muesebeck, a junior syn- onym of S. pallida (Braet and Quicke 2004), as well as 12 specimens of S. pallida determined by Y. Braet. All specimens used for comparison are in the Smithsonian Institution National Museum of Natural History, Washing- ton, DC (USNM). The specimens reared from N. conspurcatalis are deposited in the Florida State Collec- tion of Arthropods, Gainesville (FSCA) and the USNM. The following abbrevi- ations are used for label data: collected (coll.), county (Co.), and emerged (em.).

RESULTS Five specimens of S. pallida (Figs. 1– 2) were reared from N. conspurcatalis larvae. Host remains are associated with specimen JD11 (see label data below). Five specimens of Microgastrinae were also reared from host plant material infested with N. conspurcatalis larvae. However, hosts were not isolated indi- vidually, and thus, host remains are not are not associated with the specimens. Stantonia pallida is the first record of a parasitoid from N. conspurcatalis, and the microgastrines are likely parasitoids of N. conspurcatalis. The first author identified three female microgastrines as undetermined species of Cotesia, Glyp- tapanteles, and Rhygoplitis. The other two microgastrines appear to be con- specific with one another but are males and thus could not be identified to genus using Whitfield (1997). All were sent to J. B. Whitfield (University of Illinois at Urbana-Champaign) for further identifi- cation and are labeled with the follow- ing data: all FLORIDA: Martin Co., Figs. 1–2. Stantonia pallida. 1, Female. 2, Jonathan Dickinson State Park, 5 mi N Male. Scale bars ¼ 1.0 mm. Jupiter, A. J. Boughton, ex Neomusoti- ma conspurcatalis on Lygodium micro- teles det. Kula 2009; 1 ? parasitoid phyllum;1/ parasitoid JD2, site JD44, JD3, same data as previous except em. 27800.3930N 080808.1450W, coll. 11.ii.2009 [undetermined male]; 1 / 23.i.2009 em. 10.ii.2009, Glyptapan- parasitoid JD6, site JD25, 27801.7440N 64 PROCEEDINGS OF THE ENTOMOLOGICAL SOCIETY OF WASHINGTON

080808.2370W, coll. 23.i.2009 em. from South America (Brazil, Colombia, 14.ii.2009, Rhygoplitis det. Kula 2009; Paraguay, Venezuela) and North Amer- 1 ? parasitoid JD5, same data as ica (Costa Rica, Dominican Republic, previous except em. 12.ii.2009 [unde- Honduras, Mexico, Nicaragua, Panama, termined male]; 1 / parasitoid JD7, Puerto Rico, United States). Stantonia same data as previous except em. pallida has been reported, under the 15.ii.2009, Cotesia det. Kula 2009 name S. lamprosemae, from the pyralids (USNM). Diaphania hyalinata (Linnaeus) (mel- The specimens of S. pallida are onworm) and Diaphania nitidalis (Stoll) labeled with the following data: all (pickleworm) (Frank and McCoy 1993) FLORIDA: Martin Co., Jonathan Dick- and the crambid Omiodes indicata inson State Park, 5 mi N Jupiter, site Fabricius (soybean leaffolder) (Muese- JD24, 27800.5100N 080807.6900W, A. J. beck 1938). Boughton, ex Neomusotima conspurca- Stantonia pallida, under the name S. talis on Lygodium microphyllum, Stan- lamprosemae, was imported from Co- tonia pallida (Ashmead) det. Kula 2008 lombia and released in Florida to control or 2009; 1 ? parasitoid JD1, coll. D. hyalinata and D. nitidalis, pests of 23.x.2008 em. 12.xi.2008; 1 ? parasitoid cucurbit crops, in 1991 (Frank and JD11, coll. 2.iii.2009 em. 22.iii.2009 McCoy 1993). It is possible that the (FSCA); 1 ? parasitoid JD12, coll. specimens of S. pallida reared from N. 2.iii.2009 em. 21.iii.2009; 1 / parasitoid conspurcatalis in this study are from JD13, coll. 2.iii.2009 em. 22.iii.2009; 1 populations established via release of / parasitoid JD14, coll. 2.iii.2009 em. the Colombian specimens. However, 23.iii.2009 (USNM). Specimen JD11 Smith et al. (1994) noted that even in was reared from one of the five host the case of the cardiochiline braconid larvae that were isolated individually. It Cardiochiles diaphaniae Marsh, the was a solitary koinobiont endoparasi- most promising of the Colombian para- toid, as is the case for other orgilines for sitoids introduced to control Diaphania which host use is known (Achterberg spp., ‘‘establishment was not seriously 1997). Emergence of the parasitoid larva attempted.’’ Neither S. pallida nor S. from the host larva was not observed. A lamprosemae were mentioned in a thin-walled silk cocoon was observed recently revised publication discussing near the remains of the host larva, and the imported natural enemies for pickle- adult wasp emerged nine days later. worm management (Capinera 2005). Given its broad distribution in the DISCUSSION Western Hemisphere and presence in Stantonia pallida (including its syno- Cuba (see above), and the presence of nyms, see below) is broadly distributed one of its hosts (i.e., O. indicata)in in the Western Hemisphere, ranging Florida (Kimball 1965, Gentili and Solis from Brazil to Arizona and in the 1997), S. pallida sensu Braet and Quicke Antilles from St. Vincent Island to Cuba. (2004) was likely present in Florida Ashmead (1894) described it from a prior to release. The release of S. pallida female collected on St. Vincent Island. in Florida might represent a ‘‘type 2 Braet and Quicke (2004) synonymized error,’’ defined in Schauff and LaSalle Stantonia keiegeri Enderlein, known (1998) as ‘‘wasting time and money from Colombia (Enderlein 1905), and doing what is not necessary,’’ resulting S. lamprosemae, known from Cuba and from minimal systematic input in a Puerto Rico (Muesebeck 1938), with S. biological control program. Importation pallida. They also examined specimens of species already present in the release VOLUME 112, NUMBER 1 65 area is a common error due to insuffi- S. pallida using temporally intensive cient knowledge of the fauna in the area methods (e.g., Malaise trapping, pan (Schauff and LaSalle 1998). The known trapping) at localities where O. indicata distribution of S. lamprosemae in 1991 was known to occur. was Cuba, Puerto Rico, and Colombia. In addition to published host records, Pen˜a et al. (1987) surveyed the parasit- natural history collections are a valu- oid fauna of D. hyalinata and D. able source of host range and distribu- nitidalis larvae in Florida but did not tion data for prospective biological rear S. pallida sensu Braet and Quicke control agents (Sands and van Driesche (2004). That S. pallida was not recov- 2004). Collections with substantial ered in the survey could be regarded as holdings, particularly of specimens evidence that the specimens reared in from areas where the target and other this study are derived from wasps known hosts occur, should be surveyed released in 1991 or that the distribution prior to importation in addition to field- of S. pallida has expanded since the based surveys. Braet and Quicke (2004) survey. However, its absence was more examined specimens of Stantonia likely the result of limited sampling housed in natural history collections effort since sampling was restricted to and found that S. pallida occurs in larvae on two wild species of Cucurbi- tropical and subtropical areas through- taceae and cultivated calabaza, cucum- out the Western Hemisphere. The vast ber, squash, and zucchini (Pen˜a et al. majority of these specimens were col- 1987). Omiodes indicata larvae in Flor- lected prior to 1991, although their ida were not surveyed for S. pallida prior curatorial status prior to 2004 is un- to release of the wasp even though it was known. Had a systematist surveyed a known host for the parasitoid in Cuba specimens of Stantonia in these collec- (Muesebeck 1938). tions prior to importation of wasps from Schauff and LaSalle (1998) discussed Colombia to control Diaphania spp., he the importance of establishing collabo- or she likely would have discovered that rations with systematists at the outset of specimens fitting the concept of S. a biological control program in order to lamprosemae are broadly distributed, reduce the likelihood of error, such as suggesting its likely presence in Florida importing species already present in the prior to release. Also, examination of release area. In the case of biological the specimens might have resulted in control of D. hyalinata and D. nitidalis, synonymy of S. keiegeri and S. lamp- systematists were consulted for parasit- rosemae with S. pallida prior to 2004. oid identifications (Marsh 1986, Pen˜aet Native parasitoids have frequently al. 1987). Identifications are a critical attacked insects introduced to control component to successful biological weeds, but in most cases they have not control, but systematics input should induced enough mortality to limit the extend beyond identifications (Schauff biological control agent’s populations and LaSalle 1998). Prior to release of S. and effectiveness (Goeden and Louda pallida, input from systematists on its 1976, Hill and Hulley 1995). Parasit- distribution and host use, and the dis- oids introduced to control pest insects tribution of its known host, was not have also attacked insects introduced to requested, requested but not provided, control weeds. Among the studied cases or provided but overlooked or ignored. are braconids introduced to Hawaii to This information should have signaled control pest fruit flies (Tephritidae) that the need to survey O. indicata larvae in also attack three gall-inducing fruit fly Florida for S. pallida and sample for species introduced to control three 66 PROCEEDINGS OF THE ENTOMOLOGICAL SOCIETY OF WASHINGTON different weed species (Duan and Mess- and M. J. Sharkey, eds. Manual of the New ing 2000). The highest recorded para- World Genera of the Family Braconidae sitism on these gall-inducing biological (Hymenoptera). Special Publication No. 1. International Society of Hymenopterists, control agents was 10% (Duan and Washington, DC. Messing 2000). Rates of parasitism of Ashmead, W. H. 1894. Report on the parasitic N. conspurcatalis larvae observed in Cynipidae, part of the Braconidae, the field collections have been quite vari- Ichneumonidae, the Proctotrypidae, and part able. Some collections suffered no of the Chalcididae.—Part II, pp. 108–254. In parasitism and resulted in 100% emer- C. V. Riley, W. H. Ashmead, and L. O. gence of N. conspurcatalis adults. In Howard, Report upon the Parasitic Hyme- collections where parasitism was ob- noptera of the Island of St. Vincent. Journal served, rates ranged from 2–10% for S. of the Linnean Society 25: 56–254. Beckner, J. 1968. Lygodium microphyllum, an- pallida and from 6–24% for the micro- other fern escaped in Florida. American Fern gastrines (all presumably parasitoids of Journal 58: 93–94. N. conspurcatalis). Across all parasitoid Boughton, A. J. and R. W. Pemberton. In press. taxa, taking into account emerged wasps Establishment of an imported natural enemy, and unemerged wasp cocoons, the Neomusotima conspurcatalis (Lepidoptera: highest rate of parasitism observed in a Crambidae) against an invasive weed, Old N. conspurcatalis collection was 28%. World climbing fern, Lygodium microphyl- At present it is too early to predict how lum, in Florida. Biocontrol Science and Technology. these rates of parasitism will affect N. Boughton, A. J., C. A. Bennett, J. A. Goolsby, conspurcatalis populations and in turn and R. W. Pemberton. 2009. Laboratory host whether the potential for biological range testing of Neomusotima conspurcatalis control of L. microphyllum will be (Lepidoptera: Crambidae)—a potential bio- affected. Ongoing studies are planned logical control agent of the invasive weed, to investigate whether rates of N. con- Old World climbing fern, Lygodium micro- spurcatalis parasitism change over time. phyllum (Lygodiaceae). Biological Control Science and Technology 19: 369–390. Braet, Y. and D. L. J. Quicke. 2004. 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