Natural enemies managing the invasion of the fig whitefly, Singhiella simplex (Hemiptera: Aleyrodidae), infesting a Ficus benjamina hedge.
Article Type: Report
Subject: Aleyrodidae (Control)
Invasive species (Control)
Insect pests (Biological control)
Insect pests (Methods)
Authors: Avery, Pasco B.
Mannion, Catharine M.
Powell, Charles A.
McKenzie, Cindy L.
Osborne, Lance S.
Pub Date: 09/01/2011
Publication: Name: Florida Entomologist Publisher: Florida Entomological Society Audience: Academic Format: Magazine/Journal Subject: Biological sciences Copyright: COPYRIGHT 2011 Florida Entomological Society ISSN: 0015-4040
Issue: Date: Sept, 2011 Source Volume: 94 Source Issue: 3
Geographic: Geographic Scope: United States Geographic Code: 1USA United States
Accession Number: 298614271
Full Text: The fig whitefly, Singhiella simplex (Singh), a recent adventive species native of Burma, China and India (Singh 1931) has become a major pest in Florida (Hodges 2007) feeding on and defoliating Ficus shrubs and trees. This pest, first discovered in Miami-Dade County in 2007, is spreading throughout Florida; and recently it was found in Saint Lucie County, FL (personal observation, Avery 2009). Literature on the biology of the fig whitefly is sparse and most references are extension documents (Mannion et al. 2008; Caldwell 2009; Mannion 2010). The life cycle may be similar to that of the other Singhiella species that are present in Florida, (Singhiella citrifolii (Morgan), with at least three generations per year (Hodges 2007). Leaves of Ficus that turn yellow prior to defoliation are one of the most obvious symptoms of a fig whitefly infestation. The fig whitefly is most commonly found infesting weeping fig (Ficus benjamina), but may eventually damage other species of Ficus as well (Mannion et al. 2008).

In the landscape, several natural enemies have been observed attacking this whitefly, which may play an important role in long term control. Awareness of these natural enemies is very important in making pesticide application decisions so as not to adversely affect them. Commonly observed natural enemies include ladybird beetle predators, Harmonia axyridis (Pallas), Olla-v-nigrum (Mulsant), Exochomus children Mulsant, Chilocorus nigritis (F.), Curinus coeruleus (Mulsant); parasitoids, Encarsia protransvena Viggiani, Amitus bennetti Viggiani & Evans; and lacewings, Chrysopa spp. (Mannion 2010). Moreover, enzootic entomopathogenic fungi may also play a role in managing this pest (Elliot et al. 2000; Torres-Barragan et al. 2004). However, no entomopathogenic fungus isolated from the fig whitefly in Florida has been reported to date.

During the fall of 2009, a fig whitefly invasion occurred on a F. benjamina hedge at a residence in Ft. Pierce, Florida. We used this opportunity to: 1) identify and inventory the natural enemies present, and 2) determine their effectiveness for managing the fig whitefly over the Sep to Nov time period.

The layout for the study was a complete block design with four plots in a linear design. Each plot measured ~5 m of a F. benjamina hedge (~10-15 plants), which ran along a concrete block wall (~1.2 m tall) located at a residence in Ft. Pierce, Florida. Each hedge segment (northern 27'22"50.94 N x 80'22"00.22 W and southern 27'22"48.96 N x 80'22"00.25 W) was divided by a concrete driveway; and the northern side was more severely affected by leaf drop than the southern. Randomly chosen leaf samples (10 per plot) were detached from the hedge on a weekly basis for 7 wk. Each sample was placed into individual re-sealable plastic bags and brought back to the lab for examination under a binocular microscope (40X) to count the number of live, dead, or parasitized whitefly nymphs. Parasitism was recognized either by observing the development of the parasitoid inside the translucent nymphal case, or by observing a blackened (melanized) nymphal case with or without an exit hole. A total of 40 disks were punched with a #5 cork borer (50.3 [mm.sup.2] diam) near the center of each leaf on one side of the midrib. The abaxial and adaxial sides of 1 disk per leaf were used for observation and counting the number of nymphs of each category mentioned above. The total weekly mean ([+ or -] SEM) number of nymphs, number parasitized, and percent parasitism on the leaf disks were determined for 49 d. Based on photos of the parasitized nymphs (Mannion et al. 2008; Mannion 2010), the parasitoids appear to be E. protransvena; however, Encarsia species identification was not confirmed.

Disks were then placed on moist filter paper in a Petri dish, covered, sealed with Parafilm[TM], and incubated at 25[degrees]C for 14 d to allow for the development of mycosis, and to determine percent mortality due to fungal pathogens. After incubation, 5 mycosed nymphs/disk randomly chosen were removed from the leaf disk using a pin and placed on water agar (20 per plate) for isolation and identification of the fungal pathogen. Percent nymphs infected with a fungal species were determined for 0, 14, and 49 d post initial observation. Agar plates were sealed with Parafilm[TM], and incubated at 25[degrees]C under a 16 h photophase for at least 1 week. The fungi were re-isolated from the mycosed nymphs and grown on PDA plates for identification. Voucher fungal in vitro culture isolates were sent to Svetlana Gouli at the University of Vermont, Dr. Richard Humber at the USDA, Ithaca, New York and to Dr. Rob Samson's research team at the CBS-KNAW Fungal Diversity Centre in The Netherlands for identification and deposition.

The insect pests observed included the fig whitefly, S. simplex, another whitefly, Tetraleurodes fici Quaintance & Baker (one parasitized with an exit hole) and the weeping ficus thrips, Gynaikothrips uzeli Zimmerman (Table 1). The parasitoids, Encarsia species (all appeared to be E. protransvena) were observed after parasitization, and within the melanized nymphal case with or without an exit hole. Adult ladybird beetles, C. coeruleus, H. axyridis and eggs and larvae of the green lacewing, Chrysopa species were observed on the leaves. The natural enzootic pathogenic fungi isolated were Isaria fumosorosea Wize, Paecilomyces lilacinus Thom (Samson), and Lecanicillium, Fusarium, and Aspergillus species.

The total percent nymphal mortality per leaf disk due to pathogenic fungi varied overtime. I. fumosorosea and Lecanicillium, Aspergillus and Fusarium species were isolated from 5, 5, 48 and 50% of the dead nymphs at d 0, respectively. After 14 d, 85 and 15% of the nymphs were infected with Aspergillus sp. and P. lilacinus, respectively. At d 49, Aspergillus and Fusarium species were isolated 65% and 35% of the time, respectively. The fungal species isolated from the mycosed nymphs were assumed to have caused the mortality of the insect; however, Koch's postulate was not confirmed.

The total weekly mean ([+ or -] SEM) number of nymphs, number parasitized, and percent parasitism observed on both sides of the leaf disks over 49 d were 57.7 [+ or -] 9.91, 5.9 [+ or -] 3.72, and 7.3 [+ or -] 3.62, respectively. The proportion of nymphal mortality on a weekly basis due to parasitism was ~10% up to 35 d post initial observation; after that, no parasitized nymphs (second- fourth instars) were observed on leaf disks.

Gerling et al. (2001) indicated that all Encarsia species parasitize and emerge from the fourth instar of their whitefly host, but attack mainly the second- fourth instar hosts. Therefore, the low number of older (third--fourth instars) nymphs available to be parasitized after 35 d, may have resulted from leaf drop. Throughout this field pilot study based on leaf disk samples, only ~10% mortality was attributed to parasitization by Encarsia species, ~90% was due to other natural causes; i.e. enzootic entomopathogenic fungi, predation, etc. This finding warrants confirmation through in-depth research.

This is the first record of Hypocreales fungi; I. fumosorosea, P. lilacinus, and Aspergillus, Lecanicillium, and Fusarium species being isolated from dead fig whitefly nymphs on F. benjamina. Aspergillus and Fusarium species, not commonly known as entomopathogenic, are now being tested as potential biocontrol agents for controlling whitefly species (Panyasiri et al. 2007). The other fungal species, I. fumosorosea, P. lilacinus and Lecanicillium species are commonly used as biopesticides (de Faria & Wraight 2007) for controlling whitefly (Avery et al. 2008; Cabanillas & Jones 2009; Shinde et al. 2010), except P. lilacinus which is nematophagous. However, recently P. lilacinus has demonstrated potential for controlling whitefly species (Gokce & Er 2005; Fiedler & Sosnowska 2007).

Based on this study, it would be recommended that the endemic population of parasitoids and enzootic entomopathogenic fungi be considered as part of a multi-trophic ecosystem, which may be adversely impacted by the application of any pesticide. Therefore, it is important to assess the long term ecological impact that a pesticide application against the fig whitefly may have on the natural enemies in the landscape ecosystem.

SUMMARY

Based on leaf disk samples taken in this field pilot study, only ~10% of the fig whitefly mortality was attributed to parasitization by Encarsia species, ~90% was due to other natural causes; i.e. enzootic entomopathogenic fungi, predation, etc. This is the first record of the Hypocreales fungi, I. fumosorosea, P. lilacinus, and Aspergillus, Lecanicillium, and Fusarium species being isolated from dead S. simplex nymphs on F. benjamina. It is important to assess the long term impacts pesticide applications made for managing the fig whitefly may have on the ecosystem, and especially the ecological impact on the natural enemies which include enzootic entomopathogenic fungi.

ACKNOWLEDGMENTS

Many thanks go to John Prokop for his labor and technical assistance, and Anna Sara Hill, for the fig whitefly insectary work, at the USDA-ARS, U.S. Horticultural Research Laboratory; to Eliza Duane and Phyllis Hebert for their technical assistance at IRREC. We thank Svetlana Gouli at the University of Vermont, Invertebrate Pathology and Microbial Pest Control Laboratory in Burlington, Vermont, Dr. Richard Humber at the USDA-ARS Collection of Entomopathogenic Fungal Cultures (ARSEF), in Ithaca, New York and Dr. Rob Samson's research team at the CBS-KNAW Fungal Diversity Centre, Utrecht, The Netherlands for identification of the fungal isolates. We are grateful for funding through the USDA's Tropical and Subtropical Agriculture Research (T-STAR) Program, American Floral Endowment, and the USDA-ARS Floriculture and Nursery Research Initiative.

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PASCO B. AVERY (1), CATHARINE M. MANNION (2), CHARLES A. POWELL (1), CINDY L. MCKENZIE (3) AND LANCE S. OSBORNE (4)

(1) University of Florida, Institute of Food and Agricultural Sciences, Indian River Research and Education Center, 2199 South Rock Road, Fort Pierce, FL 34945

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

(3) USDA, ARS, U.S. Horticultural Research Laboratory, Subtropical Insect Research Unit, 2001 S. Rock Rd., Ft. Pierce, FL 34945

(4) Mid Florida Research and Education Center, University of Florida, Apopka, FL 32703
TABLE 1. INSECT PESTS AND NATURAL ENEMIES OBSERVED ON A RESIDENTIAL
FICUS BENJAMINA HEDGE IN FT. PIERCE, FLORIDA BETWEEN SEP-NOV 2009.

Category          Order          Family

Insect pests
                  Hemiptera      aleyrodidae
                  Hemiptera      Aleyrodidae
                  Thysanoptera   Phlaeothripidae

Natural Enemies
                  hymenoptera    Aphelinidae
                  coleoptera     Coccinellidae
                  coleoptera     Coccinellidae
                  Neuroptera     Chrysopidae
                  Hypocreales    cordycipitaceae
                  Hypocreales    Clavicipitaceae
                  Hypocreales    Cordycipitaceae
                  Hypocreales    Nectriaceae
                  Eurotiales     Trichocomaceae

Category          Scientific name

Insect pests
                  Singhiella simplex
                  Tetraleurodes fici
                  Gynaikothrips uzeli

Natural Enemies
                  Encarsia sp. *
                  Harmonia axyridis
                  curinus coeruleus
                  chrysopid sp.
                  isaria fumosorosea
                  Paecilomyces lilacinus
                  Lecanicillium sp.
                  Fusarium sp.
                  aspergillus sp.

Category          Common Name

Insect pests
                  fig whitefly
                  whitefly
                  weeping ficus thrip

Natural Enemies
                  parasitoid
                  multicolored Asian lady beetle
                  metallic blue lady beetle
                  green lacewing
                  entomopathogenic fungi
                  entomopathogenic fungi
                  entomopathogenic fungi
                  filamentous fungi
                  green mold

Category          observations

Insect pests
                  feeding on leaves
                  feeding on leaves
                  in leaf fold galls

Natural Enemies
                  parasitized fig whitefly nymphs
                  adults roaming on leaves
                  adults roaming on leaves
                  eggs and larvae on a leaves
                  leaf surface and on fig whitefly
                  leaf surface and on fig whitefly
                  leaf surface and on fig whitefly
                  leaf surface and on fig whitefly
                  leaf surface and on fig whitefly

* All appeared to be E. protransvena.
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