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Current status of the biological control agent Neomusotima conspurcatalis (Lepidoptera: Crambidae), on Lygodium microphyllum (Polypodiales: Lygodiaceae) in Florida.

Old World climbing fern, Lygodium microphyllum (Cav.) R. Br (Polypodiales: Lygodiaceae), is an invasive weed that is widespread throughout wetland and mesic habitats in south Florida, and degrades critical ecosystem services and habitats of rare and endangered species (Pemberton & Ferriter 1998; Volin et al. 2004). Old World climbing fern likely arrived in Florida through the ornamental plant trade and was first reported naturalized in Florida in 1968 (Beckner 1968). By 1978 it was found commonly throughout Martin County and has now spread to many parts of the sensitive Everglades ecosystem including the Arthur R. Marshall Loxahatchee National Wildlife Refuge, Everglades National Park and Big Cypress National Preserve (Nauman & Austin 1978; Ferriter & Pernas 2006, www.eddMaps. org, accessed 13-IX-2013). Though various state, regional and federal agencies have sought for years to curb the spread of L. microphyllum, it continues to rapidly expand its range, which now includes much of south and central Florida and isolated points in northern Florida (e.g. Jacksonville, Daytona [www.eddmaps.org, accessed 14-I-2014], Ferriter & Pernas 2006).

An indeterminate rachis and extensive rhizomatous growth smother native understory vegetation and act as a fire ladder carrying low-intensity fires into the canopy, which causes extensive tree death (Pemberton & Ferriter 1998). Compounding the challenge to control L. microphyllum is the strong propagule pressure from spores that travel via wind currents and arrive at isolated sites. No native herbivores exert control over the fern's growth and herbicides are difficult to apply in habitats in which L. microphyllum invades. Although herbicides and fire kill above-ground biomass, new fiddleheads rapidly regrow from the underground rhizome (Stocker et al. 2008).

In 1997, scientists from the U.S. and Australia conducted foreign exploration for biological control agents of L. microphyllum in Asia and Australia. These surveys yielded several insects and one mite that negatively impact L. microphyllum in the native range (Pemberton 1998; Goolsby et al. 2003). Of these candidates, 2 moths (Austromusotima camptozonale Yen and Neomusotima conspurcatalis Warren, Lepidoptera: Crambidae) and one leaf-galling mite (Floracarus perrepae Knihinicki & Boczek, Acariformes: Eriophyidae) were approved for release by the USDA-APHIS Technical Advisory Group (APHIS-TAG). Austromusotima camptozonale was released from 2004 until 2007 and then again from 2010 to 2012, but failed to establish despite the release of more than 160,000 adults and larvae into the field (Boughton & Pemberton 2008). Floracarus perrepae was released from 2008 until 2010 and has established within isolated patches in Martin County and Everglades National Park (Lake et al. in press).

Neomusotima conspurcatalis Warren (Lepidoptera: Crambidae) is a Lygodium specialist native to Southeast Asia and Australia. This agent readily established populations in Old World climbing fern stands after its introduction in early 2008. By Dec 2008, large larval populations were present in Jonathan Dickinson State Park and caused measurable impacts on L. microphyllum (Boughton & Pemberton 2009; Boughton unpublished data). However, two consecutive cold winters followed in 2010 and 2011 and moth populations decreased or were reportedly extirpated from previously established sites (Boughton et al. 2012a; Boughton & Pemberton 2012).

In late 2012, land managers once again began to report large larval feeding events, known as brown outs, in areas of Loxahatchee National Wildlife Refuge, Jonathan Dickinson State Park, and Barley Barber Swamp Conservation Area (pers. com). To verify these reports and determine the current status of N. conspurcatalis populations, we resurveyed all original release sites (N = 18) from Oct 2012 to Mar 2013. Each site was searched by 2 investigators for approximately 30 min and then assigned an infestation score (0-5), according to the frequency of occurrence of characteristic leaf feeding damage and abundance of N. conspurcatalis. Sites where N. conspurcatalis was absent were assigned a score of 0; old signs of feeding, but no insects = 1; low densities, but insects present = 2; moderate infestation, insects present and patchy throughout the site = 3; feeding damage frequent with high moth presence = 4; and abundant populations and damage (brown outs) = 5. We then used a linear regression analysis to evaluate the relationship between release size and infestation score.

We recovered N. conspurcatalis in or adjacent to the site at all release points except Everglades National Park (Table 1). The single release made at Everglades National Park was conducted hurriedly due to thunderstorm activity during the release (H. Cooley, pers. com). An additional release made at Corbett National Wildlife Refuge was omitted from the analysis because the L. microphyllum in the release site was treated with herbicide. We found no significant linear relationship between release size and infestation score (P = 0.06). However all releases of 4,000 or more larvae successfully established populations that persisted for at least 5 years, and at many sites, releases of 2,200 larvae were adequate to establish persistent populations.

Neomusotima conspurcatalis occupies isolated, though large, areas within the Old World climbing fern range in Florida. Currently N. conspurcatalis does not extend beyond Central Florida, but warming temperatures and fewer frost events may facilitate a northward range expansion. Notwithstanding extenuating circumstances, all populations have persisted for at least 5 years. Despite cold temperatures and the acquisition of parasitoids (Boughton et al. 2012b), our findings indicate that N. conspurcatalis and the Lygodium galling mite, Floracarus perrepae, are more widely distributed in greater abundances than previously understood (Boughton & Pemberton 2011, Lake et al. in press). Further investigations will evaluate the impact of N. conspurcatalis on L. microphyllum as well as determine the northern limits for N. conspurcatalis and future L. microphyllum control candidates.

ACKNOWLEDGMENTS

We thank L. Jameson and C. Mason and the Arthur R. Marshall Loxahatchee National Wildlife Refuge for providing an airboat and other support to resurvey release sites. We also thank L. Rodgers and other representatives of the South Florida Water Management District for ongoing support for L. microphyllum biocontrol projects. H. Cooley of Everglades National Park facilitated helicopter transportation for sites within ENP. T. Center, G. Witkus and T. Wasylik (USDA-ARS, Invasive Plant Research Laboratory) were instrumental to relocating release sites and detecting agents in the field.

REFERENCES CITED

BECKNER, J. 1968. Lygodium microphyllum, another fern escaped in Florida. American Fern J. 58: 93-94.

BOUGHTON, A. J., AND PEMBERTON, R. W. 2008. Efforts to establish a foliage-feeding moth, Austromusotima camptozonale, against Lygodium microphyllum in Florida, considered in the light of a retrospective review of establishment success of weed biocontrol agents belonging to different arthropod taxa. Biol. Control. 47: 28-36.

BOUGHTON, A. J., AND PEMBERTON, R. W. 2009. Establishment of an imported natural enemy, Neomusotima conspurcatalis (Lepidoptera: Crambidae) against an invasive weed, Old World climbing fern, Lygodium microphyllum, in Florida. Biocontrol Sci. Technol. 19: 769-772.

BOUGHTON, A. J., AND PEMBERTON, R. W. 2011. Limited field establishment of a weed biocontrol agent, Floracarus perrepae (Acariformes: Eriophyidae), against Old World climbing fern in Florida-a possible role of mite resistant plant genotypes. Environ. Entomol. 40: 1448-1457.

BOUGHTON, A. J., AND PEMBERTON, R. W. 2012. Biology and reproductive parameters of the brown lygodium moth, Neomusotima conspurcatalis--A new biological control agent of Old World climbing fern in Florida. Environ. Entomol. 41: 308-316.

BOUGHTON, A. J., NELSON, B. B., AND CENTER, T. D. 2012a. Efforts to establish a biological control agent against incipient infestations of Old World climbing fern in Southwest Florida. Florida Entomol. 95: 482-484.

BOUGHTON, A. J., KULA, R. R., GATES, M., ZHANG, Y., NUNEZ, M., O'CONNOR, J., WHITFIELD, J. B., AND CENTER, T. D. 2012b. Parasitoids attacking larvae of a recently introduced weed biological control agent, Neomusotima conspurcatalis (Lepidoptera: Crambidae): Key to species, natural history, and integrative taxonomy. Ann. Entomol. Soc. America 105: 751-952.

EARLY DETECTION AND DISTRIBUTION AND MAPPING SYSTEM (EDDMAPS). The University of Georgia--Center for Invasive Species and Ecosystem Health. Accessed IX-2013. http://www.eddmaps.org.

FERRITER, A., AND PERNAS, T. 2006. An explosion in slow motion: tracking the spread of Lygodium microphyllum in Florida. Wildland Weeds 9: 7-9.

GOOLSBY, J. A., WRIGHT, A. D., AND PEMBERTON, R. W. 2003. Exploratory surveys in Australia and Asia for natural enemies of Old World climbing fern, Lygodium microphyllum: Lygodiaceae. Biol. Control 28: 33-46.

LAKE, E. C., SMITH, M. C., BOUGHTON, A. B., PRATT, P. D., AND PEMBERTON, R. W. 2014. Dispersal and establishment of new popultions of the biological control agent Floracarus perrepae (Acariformes: Eriophyidae) on Old World Climbing Fern, Lygodium microphyllum (Polypodiales: Lygodiace). Florida Entomol. in press.

NAUMAN, C. E., AND AUSTIN, D. F. 1978. Spread of the exotic fern Lygodium microphyllum in Florida. American Fern J. 68: 65-66.

PEMBERTON, R. W. 1998. The potential of biological control to manage Old World climbing fern (Lygodium microphyllum), an invasive weed in Florida. American Fern J. 88: 176-182.

PEMBERTON, R. W., AND FERRITER, A. P. 1998. Old World climbing fern (Lygodium microphyllum), a dangerous invasive weed in Florida. American Fern J. 88: 165-175.

STOCKER, R. K., MILLER, R. E., BLACK, D. W., FERRITER, A. P., AND THAYER, D. D. 2008. Using fire and herbicides to control Lygodium microphyllum and effects on a pine flatwoods plant community in south Florida. Natl. Areas J. 28: 144-154.

VOLIN, J. C., LOTT, M. S., MUSS, J. D., AND OWEN, D. 2004. Predicting rapid invasion of the Florida Everglades by Old World climbing fern (Lygodium microphyllum). Diversity Distrib. 10: 439-446.

MELISSA C. SMITH (1), *, ELLEN C. LAKE (1), PAUL D. PRATT (1), ANTHONY J. BOUGHTON (2) AND ROBERT W. PEMBERTON (3)

(1) USDA-ARS Invasive Plant Research Laboratory, 3225 College Avenue, Fort Lauderdale, FL 33314

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

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

* Corresponding author: E-mail: Melissa.smith@ars.usda.gov

TABLE 1. RELEASE HISTORY, FEEDING SCORE AND DATE OF LAST
ASSESSMENT FOR N. CONSPURCATALIS. SITES WITH (*) DENOTE THAT
THEY WERE SPRAYED WITH HERBICIDE AND WERE NOT USED IN THE
REGRESSION ANALYSIS. FEEDING LEVELS ARE SCORED AS FOLLOWS: 0,
NO FEEDING SIGNS; 1, SIGNS OF OLD FEEDING; 2, LOW DENSITIES,
BUT INSECTS PRESENT; 3, INSECTS PRESENT, BUT PATCHY THROUGHOUT
THE SITE; 4, FEEDING DAMAGE FREQUENT WITH HIGH MOTH PRESENCE;
AND 5, EXTENSIVE FEEDING DAMAGE AND POPULATION EXPLOSIONS
(BROWN OUTS). WITH THE EXCEPTION OF RODGER'S RIVER IN EVERGLADES
NATIONAL PARK AND TWO ISOLATED TREE ISLANDS IN LNWR, N.
CONSPURCATALIS ESTABLISHED POPULATIONS AT ALL SITES.

Location                 Site Name      Release Date(s)

Everglades National      Rodger's       13-May-09
  Park                     River,
                           Cape Sable
Jonathan Dickinson       JD24           22 May 2008-21 July 2010
  State Park
Jonathan Dickinson       JD25           31 March 2008-7 May 2008
  State Park
Jonathan Dickinson       JD44           31 Jan 2008-23 Aug 2010
  State Park
JW Corbett National      Corbett55      15-May-09
  Wildlife Refuge *
Lennar County            Lennar2        24 July 2008-28 Aug 2008
  Preserve
Loxahatchee National     Lox kiosk      28-Oct-09
  Wildlife Refuge *
Loxahatchee National     Lox12 New      28-Oct-09
  Wildlife Refuge *
Loxahatchee National     Lox32          29 Feb 2008-5 Dec 2008
  Wildlife Refuge          Strazzulla
Loxahatchee National     Lox41          27-Mar-09
  Wildlife Refuge
Loxahatchee National     Lox42          27-Mar-09
  Wildlife Refuge
Loxahatchee National     Lox43          27-Mar-09
  Wildlife Refuge
Loxahatchee National     Lox44          27-Mar-09
  Wildlife Refuge
Loxahatchee National     Lox5           10-Oct-08
  Wildlife Refuge
Cypress Creek Preserve   Cypress        2 April 2009-10 Nov 2010
  --SFWMD                  Creek
Kissimmee River          Kissimmee      2-Apr-09
  --SFWMD                  River 1
Flatword Swamp           Flatford       31 Aug 2009-11 Aug 2010
  --SFWMD                  Swamp 1
Flatword Swamp           Flatford       32 Aug 2009-11 Aug 2010
  --SFWMD                  Swamp 3

Location                 Total   Feeding   Date last
                                  Score    assessed

Everglades National      4050       0      13-Dec-12
  Park
Jonathan Dickinson       17100      3      31-Jan-13
  State Park
Jonathan Dickinson       14791      3      29-Jan-13
  State Park
Jonathan Dickinson       2750       2      31-Jan-13
  State Park
JW Corbett National      4250    sprayed   26-Mar-13
  Wildlife Refuge *
Lennar County            13358      2      31-Jan-13
  Preserve
Loxahatchee National     2000    sprayed   13-Feb-13
  Wildlife Refuge *
Loxahatchee National     2000    sprayed   13-Feb-13
  Wildlife Refuge *
Loxahatchee National     19289      2      13-Feb-13
  Wildlife Refuge
Loxahatchee National     2200       2      10-Oct-12
  Wildlife Refuge
Loxahatchee National     2200       2      10-Oct-12
  Wildlife Refuge
Loxahatchee National     2200       0      10-Oct-12
  Wildlife Refuge
Loxahatchee National     2200       0      10-Oct-12
  Wildlife Refuge
Loxahatchee National     4400       2      13-Feb-13
  Wildlife Refuge
Cypress Creek Preserve   59209      3      5-Feb-13
  --SFWMD
Kissimmee River          14821      4      23-Oct-12
  --SFWMD
Flatword Swamp           12000      2      6-Mar-13
  --SFWMD
Flatword Swamp           12000      2      6-Mar-13
  --SFWMD
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Title Annotation:Scientific Notes
Author:Smith, Melissa C.; Lake, Ellen C.; Pratt, Paul D.; Boughton, Anthony J.; Pemberton, Robert W.
Publication:Florida Entomologist
Article Type:Report
Geographic Code:1USA
Date:Jun 1, 2014
Words:1963
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