Scientific Notes 817

CURRENT STATUS OF THE BIOLOGICAL CONTROL AGENT NEOMUSOTIMA CONSPURCATALIS (: ), ON LYGODIUM MICROPHYLLUM (: LYGODIACEAE) IN FLORIDA

1, 1 1 2 3 Melissa C. Smith *, Ellen C. Lake , Paul D. Pratt , Anthony J. Boughton and Robert W. Pemberton 1USDA-ARS Invasive Research Laboratory, 3225 College Avenue, Fort Lauderdale, FL 33314

2University of Florida, Tropical Research & Education Center, Homestead, FL 33031

3Research Associate, Florida Museum of Natural History; USDA-Agricultural Research Service (retired)

*Corresponding author: E-mail: [email protected]

Old World climbing , Lygodium microphyl- camptozonale Yen and Neomusotima conspur- lum (Cav.) R. Br (Polypodiales: Lygodiaceae), is catalis Warren, Lepidoptera: Crambidae) and one an invasive weed that is widespread throughout leaf-galling mite (Floracarus perrepae Knihinicki wetland and mesic habitats in south Florida, and & Boczek, Acariformes: Eriophyidae) were ap- degrades critical ecosystem services and habitats proved for release by the USDA-APHIS Technical of rare and endangered species (Pemberton & Advisory Group (APHIS-TAG). Austromusotima Ferriter 1998; Volin et al. 2004). Old World climb- camptozonale was released from 2004 until 2007 ing fern likely arrived in Florida through the and then again from 2010 to 2012, but failed to ornamental plant trade and was first reported establish despite the release of more than 160,000 naturalized in Florida in 1968 (Beckner 1968). adults and larvae into the field (Boughton & Pem- By 1978 it was found commonly throughout Mar- berton 2008). Floracarus perrepae was released tin County and has now spread to many parts of from 2008 until 2010 and has established within the sensitive ecosystem including the isolated patches in Martin County and Everglades Arthur R. Marshall Loxahatchee National Wild- National Park (Lake et al. in press). life Refuge, and Big Neomusotima conspurcatalis Warren (Lepi- Cypress National Preserve (Nauman & Austin doptera: Crambidae) is a Lygodium specialist na- 1978; Ferriter & Pernas 2006, www.eddMaps. tive to Southeast Asia and Australia. This agent org, accessed 13-IX-2013). Though various state, readily established populations in Old World regional and federal agencies have sought for climbing fern stands after its introduction in years to curb the spread of L. microphyllum, it early 2008. By Dec 2008, large larval populations continues to rapidly expand its range, which now were present in Jonathan Dickinson State Park includes much of south and central Florida and and caused measurable impacts on L. microphyl- isolated points in northern Florida (e.g. Jackson- lum (Boughton & Pemberton 2009; Boughton un- ville, Daytona [www.eddmaps.org, accessed 14-I- published data). However, two consecutive cold w 2014], Ferriter & Pernas 2006). winters followed in 2010 and 2011 and pop- An indeterminate rachis and extensive rhizom- ulations decreased or were reportedly extirpated atous growth smother native understory vegeta- from previously established sites (Boughton et al. tion and act as a fire ladder carrying low-intensity 2012a; Boughton & Pemberton 2012). fires into the canopy, which causes extensive tree In late 2012, land managers once again began death (Pemberton & Ferriter 1998). Compound- to report large larval feeding events, known as ing the challenge to control L. microphyllum is brown outs, in areas of Loxahatchee National the strong propagule pressure from spores that Wildlife Refuge, Jonathan Dickinson State Park, travel via wind currents and arrive at isolated and Barley Barber Swamp Conservation Area sites. No native herbivores exert control over the (pers. com). To verify these reports and determine fern’s growth and herbicides are difficult to apply the current status of N. conspurcatalis popula- in habitats in which L. microphyllum invades. Al- tions, we resurveyed all original release sites (N though herbicides and fire kill above-ground bio- = 18) from Oct 2012 to Mar 2013. Each site was mass, new fiddleheads rapidly regrow from the searched by 2 investigators for approximately 30 underground rhizome (Stocker et al. 2008). min and then assigned an infestation score (0 – 5), In 1997, scientists from the U.S. and Australia according to the frequency of occurrence of char- conducted foreign exploration for biological control acteristic leaf feeding damage and abundance of agents of L. microphyllum in Asia and Australia. N. conspurcatalis. Sites where N. conspurcatalis These surveys yielded several and one mite was absent were assigned a score of 0; old signs that negatively impact L. microphyllum in the na- of feeding, but no insects = 1; low densities, but tive range (Pemberton 1998; Goolsby et al. 2003). insects present = 2; moderate infestation, insects Of these candidates, 2 (Austromusotima present and patchy throughout the site = 3; feed- 818 Florida Entomologist 97(2) June 2014

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elease an d b ut fee d ing tree R 1. a b le Flatword Swamp - SFWMD Flatword Swamp - SFWMD Kissimmee River - SFWMD Cypress Creek Preserve - SFWMD Loxahatchee National Wildlife Refuge Loxahatchee National Wildlife Loxahatchee National Wildlife Refuge Loxahatchee National Wildlife Loxahatchee National Wildlife Refuge Loxahatchee National Wildlife Loxahatchee National Wildlife Refuge Loxahatchee National Wildlife Loxahatchee National Wildlife Refuge Loxahatchee National Wildlife Loxahatchee National Wildlife Refuge Loxahatchee National Wildlife Loxahatchee National Wildlife Refuge * Loxahatchee National Wildlife Loxahatchee National Wildlife Refuge* Loxahatchee National Wildlife Lennar County Preserve JW Corbett National Wildlife Refuge* JW Corbett National Wildlife Jonathan Dickinson State Park Jonathan Dickinson State Park T Location Everglades National Park Jonathan Dickinson State Park Scientific Notes 819 ing damage frequent with high moth presence = Key Words: Lygodium microphyllum, Neomu- 4; and abundant populations and damage (brown sotima conspurcatalis, Jonathan Dickinson State outs) = 5. We then used a linear regression Park, establishment analysis to evaluate the relationship between release size and infestation score. Resumen We recovered N. conspurcatalis in or adja- cent to the site at all release points except Ev- La polilla marrón defoliadora del Lygodium, erglades National Park (Table 1). The single Neomusotima conspurcatalis Warren (Lepidop- release made at Everglades National Park was tera: Crambidae), fue liberada a partir del 2008 conducted hurriedly due to thunderstorm activ- para controlar el helecho trepador del Mundo ity during the release (H. Cooley, pers. com). Antiguo, Lygodium microphyllum (Cav.) R. Br. An additional release made at Corbett National (Polypodiales: Lygodiaceae). La polilla se estable- Wildlife Refuge was omitted from the analy- ció fácilmente en el Parque Estatal de Jonathan sis because the L. microphyllum in the release Dickinson, pero en otros lugares la población se site was treated with herbicide. We found no mantuvo en baja densidad o fue extinguida local- significant linear relationship between release mente. En 2012 y 2013, recuperamos poblaciones size and infestation score (P = 0.06). However de N. conspurcatalis en todos los sitios donde all releases of 4,000 or more larvae success- fueron liberadas inicialmente, excepto el Parque fully established populations that persisted for Nacional de los Everglades y los lugares tratados at least 5 years, and at many sites, releases of con herbicida. Las liberaciones iniciales de 4000 2,200 larvae were adequate to establish persis- o más individuos por sitio fueron completemente tent populations. exitosas, que apunta a una estrategia que se cen- Neomusotima conspurcatalis occupies iso- tra en liberar números en este nivel o más para lated, though large, areas within the Old World futuras liberaciones en la Florida. climbing fern range in Florida. Currently N. Palabras Clave: Lygodium microphyllum, Neo- conspurcatalis does not extend beyond Central musotima conspurcatalis, Parque Estatal de Jo- Florida, but warming temperatures and fewer nathan Dickinson, establecimiento frost events may facilitate a northward range expansion. Notwithstanding extenuating cir- cumstances, all populations have persisted for Acknowledgments at least 5 years. Despite cold temperatures and We thank L. Jameson and C. Mason and the Arthur the acquisition of parasitoids (Boughton et al. R. Marshall Loxahatchee National Wildlife Refuge for 2012b), our findings indicate thatN. conspur- providing an airboat and other support to resurvey re- catalis and the Lygodium galling mite, Flor- lease sites. We also thank L. Rodgers and other repre- acarus perrepae, are more widely distributed sentatives of the South Florida Water Management Dis- in greater abundances than previously under- trict for ongoing support for L. microphyllum biocontrol stood (Boughton & Pemberton 2011, Lake et al. projects. H. Cooley of Everglades National Park facili- in press). Further investigations will evaluate tated helicopter transportation for sites within ENP. T. the impact of N. conspurcatalis on L. microphyl- Center, G. Witkus and T. Wasylik (USDA-ARS, Invasive Plant Research Laboratory) were instrumental to relo- lum as well as determine the northern limits for cating release sites and detecting agents in the field. N. conspurcatalis and future L. microphyllum control candidates. References Cited

Summary Beckner, J. 1968. Lygodium microphyllum, another fern escaped in Florida. American Fern J. 58: 93-94. The brown Lygodium defoliating moth, Neo- Boughton, A. J., and Pemberton, R. W. 2008. Efforts musotima conspurcatalis Warren (Lepidoptera: to establish a foliage-feeding moth, Austromusotima Crambidae), was released beginning in 2008 to camptozonale, against Lygodium microphyllum in control Old World climbing fern, Lygodium mi- Florida, considered in the light of a retrospective crophyllum (Cav.) R. Br (Polypodiales: Lygodia- review of establishment success of weed biocontrol ceae). The moth readily established in Jonathan agents belonging to different taxa. Biol. Control. 47: 28-36. Dickinson State Park, but at other sites popula- Boughton, A. J., and Pemberton, R. W. 2009. Estab- tions remained at low densities or were locally lishment of an imported natural enemy, Neomu- extirpated. In 2012 and 2013, we recovered N. sotima conspurcatalis (Lepidoptera: Crambidae) conspurcatalis populations at all original release against an invasive weed, Old World climbing fern, sites except Everglades National Park and those Lygodium microphyllum, in Florida. Biocontrol Sci. treated with herbicide. The original releases of Technol. 19: 769-772. 4,000 or more individuals per site were entirely Boughton, A. J., and Pemberton, R. W. 2011. Limited successful, pointing to a strategy that focuses on field establishment of a weed biocontrol agent,Flor - numbers at this target level or beyond for future acarus perrepae (Acariformes: Eriophyidae), against Old World climbing fern in Florida-a possible role of releases in Florida. 820 Florida Entomologist 97(2) June 2014

mite resistant plant genotypes. Environ. Entomol. dium microphyllum: Lygodiaceae. Biol. Control 28: 40: 1448-1457. 33-46. Boughton, A. J., and Pemberton, R. W. 2012. Biology Lake, E. C., Smith, M. C., Boughton, A. B., Pratt, and reproductive parameters of the brown lygodium P. D., and Pemberton, R. W. 2014. Dispersal and moth, Neomusotima conspurcatalis - A new biologi- establishment of new popultions of the biological cal control agent of Old World climbing fern in Flor- control agent Floracarus perrepae (Acariformes: Eri- ida. Environ. Entomol. 41: 308-316. ophyidae) on Old World Climbing Fern, Lygodium Boughton, A. J., Nelson, B. B., and Center, T. D. microphyllum (Polypodiales: Lygodiace). Florida En- 2012a. Efforts to establish a biological control agent tomol. in press. against incipient infestations of Old World climbing Nauman, C. E., and Austin, D. F. 1978. Spread of fern in Southwest Florida. Florida Entomol. 95: 482- the exotic fern Lygodium microphyllum in Florida. 484. American Fern J. 68: 65-66. Boughton, A. J., Kula, R. R., Gates, M., Zhang, Y., Pemberton, R. W. 1998. The potential of biological con- Nunez, M., O’connor, J., Whitfield, J. B., and trol to manage Old World climbing fern (Lygodium Center, T. D. 2012b. Parasitoids attacking larvae of microphyllum), an invasive weed in Florida. Ameri- a recently introduced weed biological control agent, can Fern J. 88: 176-182. Neomusotima conspurcatalis (Lepidoptera: Crambi- Pemberton, R. W., and Ferriter, A. P. 1998. Old dae): Key to species, natural history, and integrative World climbing fern (Lygodium microphyllum), a . Ann. Entomol. Soc. America 105: 751-952. dangerous invasive weed in Florida. American Fern Early Detection and Distribution and Mapping J. 88: 165-175. System (EDDMapS). The University of Georgia – Stocker, R. K., Miller, R. E., Black, D. W., Ferriter, Center for Invasive Species and Ecosystem Health. A. P., and Thayer, D. D. 2008. Using fire and her- Accessed IX-2013. http://www.eddmaps.org. bicides to control Lygodium microphyllum and ef- Ferriter, A., and Pernas, T. 2006. An explosion in fects on a pine flatwoods plant community in south slow motion: tracking the spread of Lygodium mi- Florida. Natl. Areas J. 28: 144-154. crophyllum in Florida. Wildland Weeds 9: 7-9. Volin, J. C., Lott, M. S., Muss, J. D., and Owen, D. Goolsby, J. A., Wright, A. D., and Pemberton, R. W. 2004. Predicting rapid invasion of the Florida Ever- 2003. Exploratory surveys in Australia and Asia for glades by Old World climbing fern (Lygodium micro- natural enemies of Old World climbing fern, Lygo- phyllum). Diversity Distrib. 10: 439-446.