Role of Beneficial Insects and Mites in Suppression of Psyllids and Other Citrus Pests Jawwad A. Qureshi and Philip A. Stansly Southwest Florida

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Role of Beneficial Insects and Mites in Suppression of Psyllids and Other Citrus Pests Jawwad A. Qureshi and Philip A. Stansly Southwest Florida Research and Education Center

Major Pest Threats To Florida Citrus 1 Asian citrus psyllid (ACP)/ Huanglongbing, citrus greening 2 Citrus leafminer (CLM)/ Citrus canker Other significant pests Rust mites, Spider mites, Aphids, Scales, Mealybugs, White flies, Black flies, Thrips, Weevils Biological control is critical for sustainable and economical citrus pest management

Presentation Outline Predators and parasitoids of ACP, CLM and other citrus pests common in Florida citrus Augmentation of predators and parasitoids Monitoring (scouting) for natural enemies Impact of natural enemies on ACP and CLM populations What else can we do to enhance biological control, conservation? Conclusions and implications

COMMON PREDATORS AND PARASITOIDS

Southern 2-spotted ladybeetle Olla v-nigrum Primarily a mite feeder Also feeds on aphids and psyllids Its abundance increased in response to psyllid invasion P. Stansly

Multicolored asian ladybeetle Harmonia axyridis An introduced species A good predator of aphids and psyllids Also feeds on mites, scales, mealybugs, leafminers, and eggs and larvae of several other insects R. Venette

Blood-red ladybeetle Cycloneda sanguinea Important predator of aphids and psyllids Also feeds on mites, scales, and mealybugs J. P. Michaud

Metallic blue ladybeetle Curinus coeruleus Imported from Mexico in 1950s Primarily a scale feeder Also feeds on aphids, and psyllids

Little red ladybeetle Exochomus childreni A native species abundant in central Florida Primarily a scale feeder Also feeds on aphids and psyllids J. P. Michaud

Lacewings - Chrysopidae Chrysoperla spp. Psyllid Eggs & Nymphs Ceraeochrysa spp. P. Stansly

Other Predators Asian cockroach Blattella asahinai Sac spider Pseudomyrmex ants Acrobat ants Crematogaster

ACP Parasitoid: Tamarixia radiata: Adult Life Cycle Egg Larva Mummies Pupa Prepupa

ACP Parasitoid: Diaphorencyrtus aligarhensis

Indigenous Parasitoids of CLM Families: Eulophidae, Encyrtidae, Elasmidae, Eurytomidae and Pteromalidae Species LaSalle and Schauff 1996 Cirrospilus nigrivariegatus C. sp. Zagrammosoma americanum Z. multilineatum Pnigalio minio P. sp Sympiesis sp Horismenus sardus Closterocerus cinctpennis Elasmus tischeriae Catolaccus aeneoviridis Schauff et al. 1998, Pomerinke and Stansly 1998

Introduced Parasitoids of CLM Ageniaspis citricola Cirrospilus ingenuus From Australia in 1994 Hoy and Nguyen 1994 J. Lotz

Introduced Parasitoids of CLM Citrostichus phyllocnistoides From Spain in 2006 Reduced citrus leafminer infestations to non-economic levels in Spain Major role in other Mediterranean countries and in Asia. 1.2 1 0.8 0.6 0.4 0.2 0 Natives C. phyllocnistoides 1999 2000 2001 Vercher et al. 2005 A. Urbaneja

Semielacher petiolatus Another effective parasitoid Plays a major role in Citrus leafminer control in the Mediterranean as well as its native Australia Similar biology to C. phyllocnistoides L. Zappala

AUGMENTATION OF PREDATORS AND PARASITOIDS

Winter Aggregation of Hippodamia convergens

Millions of Hippodamia convergens released in Southwest and Central Florida Commercial Groves (2008-2010)

Initial releases of T. radiata in Florida 1999-2001 37, 000 from a mixed colony established at DPI Gainesville, FL, from parasitoids imported from Taiwan and south Vietnam (Hoy and Nguyen 2001, Skelly and Hoy 2004)

Our efforts to enhance parasitism rates of T. radiata in the United States Importation and introduction of T. radiata from Pakistan, South China, and North Vietnam (Qureshi and Stansly 2008), and their genetic characterization (Barr et al. 2009) 150000 100000 T. radiata released in Florida 2009-2011 50000 0 Florida strain* North Vietnam Pakistan South China *Originally brought in from Taiwan and south Vietnam

Citrostichus phyllocnistoides Over 12,000 (4,000 females) released in SW Florida during 2006-07 (Qureshi and Stansly)

MONITORING (SCOUTING) FOR NATURAL ENEMIES

Monitoring (Scouting) Natural Enemies 1. Tap sample - 22 x 28 cm laminated white sheet of paper - Clipboard or a white smooth surface - Place 1 ft below a leafy branch - Tap branches three times with hand or piece of PVC tube - Count and record insects, spiders, and mites that fall on the sheet - Use black surface when scouting for mites 2. Shoot Observation Shoots infested with aphids, psyllids, leafminers, scales, mealybugs etc. Qureshi and Stansly (2007), Qureshi et al. (2009)

Methods to evaluate parasitism rates Cages with apertures to allow parasitoids but not large predacious insects access to colonies in the field. (Michaud, 2004, Qureshi and Stansly, 2009) Examination of nymphs under the microscope to look for parasitoid eggs larvae or pupae (Qureshi et al. 2009) Larva Egg Pupa

Methods to evaluate parasitism rates Laboratory rearing of field collected nymphs through adult emergence. (Qureshi and Stansly, 2009, Qureshi et al. 2009) Exposure of plants infested with psyllid nymphs to natural populations of the parasitoid in the field (Qureshi and Stansly, 2009)

IMPACT OF NATURAL ENEMIES ON ACP AND CLM

Ladybeetle Abundance Before and After Psyllid Invasion in Florida Citrus 1997-1998 2000-2001 C. sanguinea H. axyridis O. v-nigrum Other spp. J. P. Michaud (2001)

Methods to measure the impact of natural mortality factors on psyllid populations 1. Full cage exclusion 2. Partial cage exclusion 3. Sticky barrier exclusion 4. No exclusion 1-2 3 4 Qureshi and Stansly (2009)

Net Reproductive Rate (R 0 ) Impact of natural enemies on psyllid populations Suppression of Psyllid Populations Mainly by Predacious Insects and Spiders (Qureshi and Stansly, Biological Control, 2009) Uncaged Caged 300 250 200 150 100 50 0 Cohort initiation date (2006-2007) R o = Estimated production of progeny from one female psyllid

Predators Observed on Colonies and Sticky Barriers No. observed Qureshi and Stansly (2009)

Demographic parameters of H. convergens on three citrus pests Qureshi and Stansly, 2011

Statewide evaluation of T. radiata Parasitism (%) Mar April May June July Aug Sept Oct Nov Dec Jan Feb Mar April in Florida (Qureshi et al. 2009, Qureshi and Stansly, 2009) Studies revealed widespread establishment of T. radiata throughout Florida, but incidence of parasitism was generally low. 100 80 60 2006-2007 Southwest Region Central Region Eastern Coastal Region 40 20 less than 20% 0

Parasitism (%) Parasitism rates of feral nymphs in groves with releases of newly imported T. radiata (October 2009) 60 40 20 0 SWFREC Zolfo Springs Lake Wales Pakistan/1447 S. China/2166 N. Vietnam/4378 Release sites/origin of T. radiata/no. released

Parasitism observed during Oct-Nov of feral nymphs in conventional groves with and without T. radiata releases, 2009 30 25 20 Parasitism (%) Average 20% 15 10 10% 5 0 Groves with releases Groves without releases 1834 2567 0 0 No. Released: Florida Colony Groves with releases Groves without releases

Parasitism (%) Nymphs parasitized by T. radiata on sentinel plants hung in citrus trees at SWFREC and a conventional grove, Immokalee, FL (Collier County) 60 SWFREC Conventional grove 40 20 0 SWFREC Conv. grove Apr09 Nov09 Jan10 Mar10 Apr10 Jun10 1400 1100 1364/1447 1834 1813/5012 2169 0/3352 0 1717/4450 0 0/4438 0 No. Released: Florida colony / Pakistan colony

Nymphs parasitized by T. radiata on sentinel plants hung in citrus trees in blocks with or without releases at SWFREC and a conventional grove, Immokalee, FL (Collier County), 2010 Parasitism (%) 80 Blocks with releases Blocks without releases 60 40 20 0 April June April June SWFREC grove Conventional grove

Parasitism (%) Parasitism observed during Jul-Aug of feral nymphs at SWFREC in blocks with and without T. radiata releases, Immokalee, FL (Collier County) 2011 60 40 Blocks with releases Blocks without releases 20 0 No. Released: July August Pakistan colony 17200 15300

Parasitism (%) Nymphs parasitized by T. radiata during Aug-Sept on sentinel plants hung in citrus trees at SWFREC in blocks with or without T. radiata releases, Immokalee, FL (Collier County), 2011 100 80 Blocks with releases Blocks without releases 60 40 20 0 No. Released: Pakistan colony August September 15300 14900

Field cages to augment T. radiata parasitism, SWFREC

Nymphs parasitized by T. radiata on citrus trees in field cages, SWFREC, 2010 100 80 Nymphs (4-5 instar)/shoot) Percent parasitism 60 40 20 0 Cage1 Cage2 Cage3

Collaborative studies with Orange Co. 2012 o Assessment of the effectiveness of T. radiata releases against ACP on caged trees o Assessment of the effectiveness of T. radiata releases using sentinel plants under different psyllid control programs

Biological control of ACP, using the predatory mite Amblyseius swirskii Glasshouse study Lab study

Dead D. citri eggs/shoot Live D. citri nymphs/shoot Results: Laboratory Study D. citri nymphs/shoot Dead D. citri nymphs/shoot 30 A. swirskii 60 A. swirskii Control Control 20 40 10 20 0 40 30 2 4 6 Day of evaluation A. swirskii Control 0 80 60 2 4 6 Day of evaluation A. swirskii Control 20 40 10 20 0 2 4 6 Day of evaluation 0 2 4 6 Day of evaluation Juan-Blasco et al (2012)

Results: Glasshouse Study Juan-Blasco et al (2012)

The Citrus Leafminer also Faces Sig- nificant Natural Mortality in Florida

Marginal Death Rate of Citrus Leafminer in Florida: 2002 0.8 0.6 0.4 Predation Parasitism A. citricola: 8-29% Other species: 10-15% 0.2 0 1st instar larva 2nd instar larva 3rd instar larva Prepupa and pupa Total Xiao et al. 2007

WHAT ELSE CAN WE DO TO ENHANCE BIOLOGICAL CONTROL, CONSERVATION?

Florida Citrus Psyllids use buds and young shoots to develop and reproduce Unfolded leaves protect psyllid eggs and nymphs from contact with foliar sprays Qureshi et al. 2009 Qureshi and Stansly 2010

Adults / tap sample Dormant Season Foliar Applications: Effect of Chlorpyrifos (Lorsban 4 E, 3 lbs/acre) Treatment on Psyllid, 2007 Silver Strand North, Immokalee, FL 4 3 2 1 0 Untreated Lorsban (3 lb/acre) Significantly different 1//22 3/8 3/29 4/12 4/25 5/29 6/22 7/24 8/27 Application Jan, 15 NS Qureshi and Stansly (2007, 2010)

Ladybeetles / tap sample Dormant Season Foliar Applications: Ladybeetles Equally Abundant in Chlorpyrifos (Lorsban 4 E, 3 lbs/acre) Treated and Untreated Trees, 2007 Silver Strand North, Immokalee, FL 0.20 0.15 Untreated Lorsban (3 lb/acre) 0.10 0.05 0.00 1//22 3/8 3/29 4/12 4/25 5/29 6/22 7/24 8/27 Application Jan, 15 Qureshi and Stansly (2007, 2010)

Individuals Foliar Applications Directed at Immatures on Young Flush: Effects on Psyllid and Ladybeetles, June 2006 Untreated Acetamiprid (Assail 30 SG, 7 oz/ac) Imidacloprid (Provado 1.6 F, 10 oz/ac) 20 1.2 15 10 5 * 0.8 0.4 0 * * Ladybeetles/20 shoots 0 Nymphs/shoot Adults/tap sample 14 days after treatment Qureshi and Stansly (2007)

Parasitism (%) Citrus blackfly parasitism based on number of adults emerged, Hendry County, December 2010 100 80 60 40 20 0 Treated (Dimethoate 24 oz/acre) Calendar Application Treatment Untreated

CONCLUSIONS AND IMPLICATIONS

Spring flush and bloom: Movento (pre bloom) Portal, Micromite if needed Summer flush Movento, Delegate if needed Fall flush: Systemic insecticide if needed Plan to Use Biological Control in Comprehensive Management Program for Asian citrus psyllid Dormant Season: Broadspectrum insecticide to target ACP adults Monitor ACP Conserve predators and parasitoids Tamarixia radiata releases Post-bloom: Various possibilities if needed Neonicotinoid drench for young trees Summer: Relatively low risk. Monitor and spray as needed. Various options. OP Pyrethroid Spray prior to anticipated new growth Oil Option Nov Dec Jan Feb Mar Apr May Jun Jul Aug Sep Oct Soil applied systemic insecticides in young plants to avoid direct effects of foliar sprays on beneficials

Acknowledgements Funding: Florida Citrus Production Research Advisory Council Insecticide industry particularly Bayer Cropscience and Dow Agroscience for large scale studies All participating growers and companies particularly Barron Collier Company for large scale studies Koppert Biological Systems SWFREC Entomology Team, B. Kostyk, R. Riefer, R. Gallegos, J. Mendez, K. Perez, M. Triana, C. Monzo, S. Croxton, B. Pena