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Huanglongbing (HLB) & the Asian Psyllid Biology, history in and survey tactics

Adam J. Silagyi, DPM State Survey Coordinator Florida CAPS Objectives ‰ Biology of the Asian citrus psyllid (ASP). ‰ Biology of Huanglongbing (HLB). ‰ History of HLB & ACP in Florida. ‰ Survey history and tactics for both in Florida. Biology of the ACP Asian citrus psyllid Diaphorina citri Kuwayama

Photo: Jeff Lotz, DPI Biology of the ACP Asian citrus psyllid Diaphorina citri 9 Adults about 2-3 mm Kuwayama 9 Wings have distinct brownish bars on the top and bottom 9 Antennae with black tip 9 Covered with whitish, waxy secretion 9 Jumping will distinguish them from sluggish aphids Biology of the ACP Asian citrus psyllid Diaphorina citri Kuwayama

Photo: Jeff Lotz, DPI Photo: Univ of FL Biology of the ACP Asian citrus psyllid Diaphorina citri 9 Nymphs are small and Kuwayama often difficult to see: (0.25 - 1.7 mm) 9 Color generally green to yellowish- with no abdominal spots 9 Psyllid nymphs have large wing pads.

Photo: Univ of FL Biology of the ACP

9 Eggs are 0.3 mm long, elongated, football shaped. 9 Deposited on new flush with the long axis vertical to Psyllid eggs on surface. 9 Color begins as pale then to yellow and finally to orange as they reach maturity. Biology of the ACP

9 Females lay around 800 eggs during lifetime. 9 Eggs laid on tips of new growth and between unfurling . 9 Eggs hatch in 2-4 days. 9 Optimum developmental temperature 25-28 ºC. 9 Five nymphal instars completed in 11-15 days.

Catling, 1970.

Adult female and nymphal instars Biology of the ACP

9 Life cycle from 15 to 47 days. 9 Adults can live several months. 9 Nine to 10 generations/year. 9 No diapause

Catling, 1970.

Adult female and nymphal instars Biology of the ACP

9 Life cycle from 15 to 47 days. Mean number of adult psyllids per trap 9 Adults can live several months. 30 Fort Pierce 9 Nine to 10 generations/year. 20 9 No diapause 10

Psyllids are found year 0 round in Florida, however 30 Vero Beach

populations fluctuate. The 20 graph to the right gives an 10 example of peaking 0 population levels through 1/1 3/1 5/1 7/1 9/1

the year. Date USDA-ARS Asian citrus psyllid damage

9 Asian citrus psyllids are restricted to citrus and closely related . 9 A preferred host is Murraya paniculata (Orange Jasmine), an ornamental that is widely grown in southern Florida. Photo: Susan Halbert, DPI Citrus sp. Asian citrus psyllid damage

9 Asian citrus psyllids are restricted to citrus and closely related Rutaceae. 9 A preferred host is Murraya

Photo: Stephen M. Garnsey paniculata (Orange Jasmine), an ornamental that is widely grown in southern Florida.

Orange jasmine: Murraya paniculata Asian citrus psyllid damage

Many times psyllids will not be present, but evidence of the feeding can still be found. The notch is a result of prior feeding by the psyllid.

Mason, 2005 Mason, 2005 Asian citrus psyllid damage

9 Large amounts of honeydew 9 Moderate amounts of distortion 9 Notched and curled leaves 9 In dry weather observations of curled waxy secretions from nymphs Photo: Susan Halbert, DPI African citrus psyllid (Trioza erytreae)

9 Only on Citrus and citrus relatives 9 Possibly cause more direct damage than D. citri. 9 Damage looks like early stages of scab 9 Not in Western andAnnecke,1968. Catling Hemisphere; yet! African citrus psyllid

9 Only on Citrus and Photo: Stephen M. Garnsey citrus relatives 9 Possibly cause more direct damage than D. citri. 9 Damage looks like early stages of scab 9 Not in Western Hemisphere; yet!

(Trioza erytreae) African citrus psyllid

9 Only on Citrus and Photo: Stephen M. Garnsey citrus relatives 9 Possibly cause more direct damage than D. citri. 9 Damage looks like early stages of scab 9 Not in Western Hemisphere; yet! Discovery of the Asian citrus psyllid

Ellen Tannehill, DPI Inspector Discovery of the Asian citrus psyllid

9After Asian citrus psyllid colonized SE Florida (red), it moved on Murraya paniculata to other counties very rapidly via the retail & discount nurseries industry. 9D. citri now found all over the State.

DiaphorinaDiaphorina citricitri hosts:hosts: (Adapted(Adapted fromfrom HalbertHalbert andand Manjunath,Manjunath, 2004)2004)

Aegle marmelos (L.) Clausena indica Oliver Aeglopsis chevalieri Swingle Clausena lansium (Lour.) Skeels Afraegle gabonensis Engl. Eremocitrus glauca (Lindley) Swingle Afraegle paniculata (Schaum.) Engl. Eremocitrus hybrid Atalantia missionis Oliver Fortunella crassifolia Swingle Atalantia monophylla (L.) Corr. Fortunella margarita (Lour.) Swingle Atalantia sp. Fortunella polyandra (Ridley) Tanaka Balsamocitrus dawei Stapf Fortunella spp., Citropsis gilletiana Swingle & M. Kellerman Limonia acidissima L. Citropsis schweinfurthii (Engl.)Swingle & Kellerm. Merrillia caloxylon (Ridley) Swingle Citrus aurantifolia (Christm.) Swingle Microcitrus australasica (F.J. Muell.) Swingle Citrus aurantium L. Microcitrus australis (Planch.) Swingle Citrus deliciosa Tenore Microcitrus papuana H.F. Winters Citrus grandis (L.) Osbeck (C. maxima) Microcitrus sp. ‘Sidney’ Citrus hystrix DC. Murraya exotica L. Citrus jambhiri Lushington Murraya koenigii (L.) Sprengel Citrus limon (L.) Burm. Murraya paniculata (L.) Jack Citrus madurensis Loar. Naringi crenulata (Royb.) Nicholson Citrus maxima (Burm.) Merr. Pamburus missionis (Wight) Swingle Citrus medica L. Poncirus trifoliata (L.) Raf. Citrus meyeri Tan Severinia buxifolia (Poiret) Ten. Citrus x nobilis Lour. Swinglea glutinosa (Blanco) Merr. Citrus obovoidea Hort. ex Tanaka cv ‘Kinkoji’ Toddalia asiatica (L.) Lam Citrus x paradisi Macfad. trifolia (Burm. f.) P. Wilson Citrus reticulata Blanco Vepris lanceolata G. Don Citrus sinensis (L.) Osbeck Aubert fagara (L.) Sarg.. Citrus spp. Apparent non-hosts: Clausena anisum-olens Merrill Casimiroa edulis Llave & Lex. Clausena excavata Burm Zanthoxylum clava-herculis L Artocarpus heterophyllus Lamarck - removed LiberibacterLiberibacter hosts:hosts: (Adapted(Adapted from from Halbert Halbert and and Manjunath, Manjunath, 2004) 2004)

Aeglopsis chevalieri Swingle Citrus oto Hort. ex Tanaka Atalantia missionis Oliver Citrus x paradisi Macfad. Balsamocitrus dawei Stapf. Citrus reticulata Blanco Calodendrum capensis Thunb. Citrus sinensis (L.) Osbeck Catharanthus roseus (L.) G. Don Citrus sunki Hort. ex Tanaka X Citroncirus webberi J. Ingram & H. E. Moore (Mack.) Marc Citrus amblycarpa Ochse Clausena indica Oliver Citrus aurantiifolia (Christm.) Swingle Clausena lansium (Lour.) Skeels Citrus aurantium L. Cuscuta australis R. Br. (Convolvulaceae, Hayata Cuscutaceae)) Citrus grandis (L.) Osbeck Fortunella spp. Citrus hassaku Hort. ex Tanaka Limonia acidissima L. Citrus hystrix DC. Microcitrus australasica (F. J. Muell.) Swingle Citrus ichangensis Swingle Murraya koenigii (L.) Citrus jambhiri Lushington Murraya paniculata (L.) Jack Citrus junos Sieb. ex Tanaka Poncirus trifoliata (L.) Raf. Citrus kabuchi Hort. ex Tanaka Swinglea glutinosa (Blanco) Merr. Citrus limon (L.) Burm. Toddalia lanceolata Lam Citrus × limonia Osbeck (Burm. f.) P. Wilson Citrus x nobilis Lour. ‘Ortanique’ Possible non-hosts: Citrus maxima (pummelo/shaddock) Tanaka Citrus x nobilis Lour. Risso Montrons Movement of pathogen & vector

9 Citrus & ornamentals 9 Potted

Pot Movement of pathogen & vector

9 Citrus & ornamentals 9 Potted plants 9 Flight distance??? 9 Safe isolation distance for budwood production? Movement of pathogen & vector

9 Citrus & ornamentals

9 Potted plants r=4750 ft 9 Flight distance??? r=1900 ft 9 Safe isolation distance for budwood production? 9Canker arc = 1900 ft or 260 acres 9Psyllid arc* = 4750 ft or 1,627 acres (6.25x larger)

*Data based on African citrus psyllid Biology of Huanglongbing

Symptoms of HLB in pummelo, Florida City Biology of Huanglongbing 9 Candidatus Liberibacter sp. 9 Candidatus L. africanus 9 Candidatus L. asiaticus 9 Candidatus L. americanus 9 Phloem-limited bacteria 9 Never cultured on artificial media 9 Causes symptoms easily confused with abiotic disorders, i.e., nutrition.

Photo: Susan Halbert Greening in commercial sweet orange Biology of Huanglongbing

9 Asian: warmer climates, transmitted primarily by Asian citrus psyllid (now in FL) 9 African: cooler climates, transmitted primarily by African citrus psyllid 9 American: the third was found in Brazil in 2004 9 Both psyllids can transmit Asian and African greening.

Photo: Susan Halbert Greening in commercial sweet orange Psyllid feeds on Psyllids acquire Bacteria multiply infected citrus bacteria in psyllid for at least 15-30 min, feed % of population carrying bacteria Circumstantial evidence in phloem tissues can be small, varies from <1% to 40% Latent period for transmission 8-12 days Pathogen in haemolymph and salivary glands

Full blown HLB syndrome on host Life cycle of Psyllid feeds on Yellow shoot syndrome healthy citrus Irregular leaf mottle and chlorosis Huanglongbing Prefer new flush Zn deficiency mimic Root degeneration (HLB) Poor fruiting, misshapen fruits, seed abortion (aka Citrus Greening) Defoliation and dieback Feeding process in Vector: Diaphorina citri phloem Pathogen: Candidatus Liberibacter asiaticus transmits bacteria Estimated feeding time to transmit varies from 30 min to 5-7 hrs, Symptoms commence in host Only nymphs 4- 5 & adults transmit Can take 1-3 years to manifest 1-80% single insect transmission rate Infected young plants express more quickly Bacteria spread Earliest detection in grafted is 2.5-3.5 mos. systemically in plant Transmission possible from symptomless citrus? th Pathogen can sector in host 15-20% symptomatic by 5 year in orchard setting Move 30-50 cm in 12 mos. Spread mostly in new growth Often confused for HLB

Mason

Phytophthora foot rot Iron (Fe) deficiency Manganese (Mn) deficiency

Potassium (K) deficiency Magnesium (Mg) deficiency Zinc (Zn) deficiency Often confused for HLB Photo: Susan Halbert Photo: Phil Mason foot rot HLB in Florida in sour orange Citrus greening symptomology

9 Mottle that crosses veins in slightly older leaves

Photo: Susan Halbert, DPI Citrus greening symptomology

9 Mottle that crosses veins in slightly older leaves 9 Early symptoms differ Infected from nutrient deficiencies branch with sectoring of branches

Healthy branches Citrus greening in Florida Citrus greening in Florida

Photos: Susan Halbert Citrus greening symptomology

9 Mottle that crosses veins in slightly older leaves 9 Early symptoms differ from nutrient deficiencies with sectoring of branches 9 Smaller lopsided fruit 9 Often with seed abortion 9 Poor color poor taste Citrus greening in Florida grapefruit

Photos: Susan Halbert HLB in Brazil

9 Reported in Brazil July 2004 9 C. L. asiaticus and americanus 9 Have only D. citri Fruit symptoms of HLB in Brazil

Photos: Jose Luiz Rodrigues Discovery of HLB in Florida

9 2004 & 2005 focused on Tampa & Orlando areas using demographics.

9 Found August 2005 during a cooperative survey with CAPS, SITC and FDACS- DPI in South Florida.

9 Quickly launched a unified command of USDA-APHIS- PPQ and FDACS-DPI led Incident Command System (ICS). HLB ICS ORGANIZATIONAL CHART COMMAND STAFF

Co-Incident Commanders M. Brodie – DPI P. Hornby - USDA

PIO Safety Officer M. Fagan - DPI J. McKee - USDA

IT Specialist Security Specialist J. Medina - USDA C. Lee - USDA

OPS Chief Planning Chief Logistics Chief Finance/Admin. Chief A. Silagyi – DPI T. Wright – DPI J. Head - USDA S. Fitzgerald - USDA HLB ICS ORGANIZATIONAL CHART OPERATIONS SECTION

OPS Chief Adam Silagyi – DPI

Residential Survey Regulatory Strike Grove Survey IES Task Force Ldr. Branch Dir. Team Ldr. Branch Dir. M. Conners - USDA E. Varona - USDA D. Chisholm - DPI J. Walker - DPI

Group A Supv. Group B Supv. Group A Supv. Group B Supv. B. Saunders - USDA M. Meadows - DPI S. Mills - USDA D. Wolfe - DPI

Strike Team A Strike Team A Strike Team A Strike Team A

Strike Team B Strike Team B Strike Team B Strike Team B

Strike Team C Strike Team C Strike Team C Strike Team C

Strike Team D Strike Team D Strike Team D Strike Team D Discovery of HLB in Florida

Southeast Florida ICS Sept 13 to Oct 14, 2005

•2,328 properties surveyed

•1361 samples taken

•179 positive

•156 positive properties in 80 TRS’s Discovery of HLB in Florida

Commercial Citrus Nursery Environ Survey Nov 1 to Dec 16, 2005 Discovery of HLB in Florida

Commercial Citrus Nursery Environ Survey Nov 1 to Dec 16, 2005 91,112 properties surveyed 922,074 trees inspected 9156 TRS’s 92 positive properties 9 One residential in Highlands County 9 One commercial grove in Desoto County Discovery of HLB in Florida

Southwest Florida ICS Jan 23 to Feb 17, 2006

9 RESEDENTIAL = 287 TRS’s = 1 positive TRS

9 GROVE = 305 TRS’s = 11 positive TRS’s = 31, 285 trees

? Arizona

¾ D. citri not known to occur in Arizona ¾ D. citri occurs in Texas and Mexico ¾ D. citri survives dry areas like Saudi Arabia and Yemen ¾ Spread by D. citri and Humans (movement of infected material and grafts) ¾ Look out for D. citri ¾ Any psyllids in Citrus sp. are NOT good ¾ Retail & discount stores ¾ Hot Zones of interest ¾ Asian farms ¾ Demographics