Identification, Biology and Control of Key Aboveground Citrus Pests

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1 Identification, Biology and Control of Key Aboveground Citrus Pests

2 You can spray for bugs or you can manage their populations, the later requires knowledge of their ways.

3 Citrus Production System generally a stable ecosystem (in the absence of pesticides) perennial crop retention of beneficial species more successful cases of biological control than any other cropping system

4 Entry Into New Regions (Invasive Pests) Citrus Leafminer (1993) Asian citrus psyllid (1998) Diaprepes root weevil (1964) Brown citrus aphid (1995)

5 Arthropod Pests Affecting Florida Citrus Production

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7 Vedalia lady beetle (Rodolia cardinalis) Introduced into California in 1888 First outstanding success in the field of classical biological control Successfully repeated in Florida in 1899 Cottony cushion scale (Icerya purchasi)

8 Arthropod Effects on Citrus Fruit Pests Foliage Pests Vectors of Disease

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10 Fruit Pests Direct damage to fruit feeding reduces fruit quality, shape, or size Reduction in yield or cause fruit to drop Concern for fruit grown for both fresh and processed markets Damage to peel Cosmetic in nature Fruit grown for fresh market

11 Rust mites Predominant arthropod pest of fresh and processed citrus in Florida Pink citrus rust mite (Aculops pelekassi) Citrus rust mite (Phyllocoptruta oleivora)

12 Rust mite damage to citrus Feeding injury Russeting of fruit and leaves Mild to severe distortion of new leaf growth Brown lesions on lower surfaces and along midribs of immature leaves May produce mesophyll collapse, chlorosis and leaf drop

13 Citrus rust mite Phyllocoptruta oleivora (Ashmead)

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15 Rust mite development Females lay 2 eggs / day (~30 lifetime) Egg to adult in 6 days Adult male longevity ~ 6 days Adult female longevity ~ 14 days

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17 Citrus rust mite seasonality 0 J a n F e b M a r Ap r M a y J u n J u l Au g Se p Oc t No v De c

18 Pink citrus rust mite Aculops pelekassi (Keifer)

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20 Pink citrus rust mite seasonality 0 J a n F e b M a r Ap r M a y J u n J u l Au g Se p Oc t No v De c

21 Early in the season, pink citrus rust mites also appear to be more prone to damage leaves than the citrus rust mite

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23 Hirsutella thompsonii

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25 Action threshold for control of rust mites Processed fruit : 10 rust mites / 2 cm 2 (1-3 oil or miticide applications / season) Fresh fruit : 2 rust mites / 2 cm 2 (3-5 miticide applications / season)

26 Citrus Mealybug (Planococcus citri)

27 Citrus Mealybug (Planococcus citri) Most common in spring and early summer Prefer sheltered locations within citrus trees females lay eggs feeding causes cosmetic damage to fresh fruit most significant problem is large amounts of honeydew produced cultivars most affected include grapefruit, navals, and valencia heavy fruit drop can occur on grapefruit

28 Citrus Mealybug Sooty-mold

29 Natural enemies of the citrus mealybug In most cases, mealybugs occur at low levels and are under good biological control by three natural enemies Ladybird beetle Cryptolaemus montrouzieri - the mealybug destroyer - abundant May - July Fungus - Entomophthora fumosa - prevalent after summer rainy season begins Hymenopteran parasitoid - Leptomastidae abnormis

30 Coccinellid spp. contribute mortality to several species Of Homoptera in Florida Cryptolaemus montrouzieri The mealybug destroyer nymphal stage of C. montouzieri

31 Control of Mealybugs Effective products for mealybugs have negative effects on beneficial insect populations Pesticides should only be applied to severe infestations Applications are most effective when applied before mealybugs have settled between fruit clusters

32 Scale Insect Pests of Fruit Armored scales (examples: Red scale, purple scale, etc ) scale insects in Florida citrus are under biological control by a large number of natural enemies No longer key pests in the development of pest management programs

33 Biological control of scale insects Factors for success Sessile (slow-moving or no movement of pest) High number of offspring to support natural enemy population growth Populations are concentrated (easy for natural enemies to find) (aggregation of red scale on green fruit)

34 Florida Red Scale (Chrysomphalus aonidum) Homoptera: Diaspididae Feeding occurs only on leaves and fruit Feeding on fruit results in discoloration at feeding site

35 Florida Red Scale (Chrysomphalus aonidum) Red scale now under biological control by parasitic wasps released in Florida (Aphytis wasps) Good example of successful classical biological control

36 FLORIDA RED SCALE Left: FRS Adult Female with Cover Lifted Lower left: 3rd instars of Aphytis holoxanthus on adult female scale Below: 5 fresh pupae of Aphytis holoxanthus under FRS cover

37 Purple Scale (Lepidosaphes beckii) Once a major pest affecting fruit, leaves and twigs Introduction of parasitoid Aphytis lepidosaphes (1950 s) Another example of successful classical biological control Parasitoid exit hole

38 Chaff Scale (Parlatoria pergandii) Most often on trunk Fruit feeding causes spotting

39 Thrips (Order Thysanoptera) Species found in Florida Flower thrips Frankliniella bispinosa Frankliniella kelliae Orchid thrips Chaetanaphothrips orchidii Danothrips trifasciatus Greenhouse thrips Heliothrips haemorrhoidalis F. bispinosa Chili thrips*** Scirtothrips dorsalis

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44 Control of F. bispinosa on Navel (Childers 1992) J. Econ. Entomol. 85: Treatment Rate Application date Chlorpyrifos 4EC 7.01 L 14 Feb Mean no. fruit/m 3 % increase vs. untreated Formetanate hydrochloride 92 SP 1.4 kg 1 Mar 34.2a 43 Dimethoate 4 EC 8.18 L 14 Feb Formetanate hydrochloride 92 SP 1.4 kg 1 Mar 33.9a 42 Formetanate hydrochloride 92 SP 1.4 kg 15 Feb 27.9b 17 untreated c ----

45 1921 The Citrus Industry 2(3): 19 J.R. Watson

46 1940 The Citrus Industry 21: 5, 8-9, 12-13, 17 the so-called thrips marks are caused by the young fruit being rubbed against leaves and twigs not by thrips. (W.C. Thompson)

47 Does F. bispinosa cause scarring damage to Murcott tangors?

48 Thrips caging study on Murcott blooms

49 35 days after thrips caging No thrips 10 thrips 25 thrips

50 Thrips (F. bispinosa) feeding damage on Murcott fruit Economic injury levels have not yet been determined

51 Orchid and Greenhouse Thrips Cause rind blemish problems on developing fruit develop in protected areas (i.e., under fruit calyx and between touching fruit) Ring spotting Primarily a problem on red grapefruit varieties but can occur on white grapefruit varieties as well

52 Greenhouse thrips (Heliothrips haemorrhoidalis)

53 Ring scarring where fruit in clusters were touching

54 Monitoring Orchid and Greenhouse thrips Examine interior clusters of red grapefruit when fruit are beginning to touch Use 10x hand lens to search for thrips (larvae and adults) on fruit where touching If most clusters sampled contain thrips, then insecticide application may be justified This damage is cosmetic in nature and does not affect internal fruit quality

55 Chili Thrips (Scirtothrips dorsalis) Recently introduced pest in Florida (2005) damage leaves and scar fruit Host Plants: Over 150 host plants including banana, beans, chrysanthemum, citrus, corn, cotton, cocoa, eggplant, ficus, grape, grasses, holly, jasmine, kiwi, litchi, longan, mango, onion, peach, peanut, pepper, rose, soybean, strawberry, tea, tobacco, tomato, viburnum, etc.

56 Chilli Thrips - rose

57 Ligustrum

58 Pittosporum

59 Chilli Thrips-pepper

60 Chilli Thrips-Indian Hawthorn

61 Chilli Thrips-Schefflera

62 Chilli Thrips-strawberry

63 Scirtothrips spp. (Thysanoptera: Thripidae) S. aurantii Faure - (South Africa) S. dorsalis Hood (Japan & Africa) S. citri (Moulton) (California & Arizona)

64 Scirtothrips citri (Moulton)

65 Foliage Pests Primarily concerned with protection of foliage on young trees On mature trees, a few pests are occasionally problematic (i.e., spider mites) Pest problems typically associated with new flush

66 Young Trees Goal: Optimize tree growth and vigor to bring trees into production within 3-4 years after setting

67 Young Tree Pest Problems

68 Citrus leafminer Phyllocnistis citrella

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70 Pupal stage 6-22 days Citrus Leafminer Lifecycle 4 larval instars 5-22 days Egg 2-10 days

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73 CLM can also cause damage to green twigs and in rare cases cause mining on fruit surface

74 Seasonality of CLM in Florida overwinter as adults with no reproductive diapause very low populations exist throughout winter months on the low levels of new flush being produced with warmer weather, CLM produce more offspring more rapidly populations build up to noticeable levels when the summer flush occurs (usually May to June)

75 Bearing citrus Mean percent damage Leaf damage /31/06 4/30/06 5/30/06 6/29/06 Date 7/29/06 8/28/06 9/27/06 10/27/06

76 Non-bearing citrus Leaf damage Mean percent damage /31/06 4/30/06 5/30/06 Date 6/29/06 7/29/06 8/28/06 9/27/06

77 Importance of CLM Damage Damage alone not significant on mature trees (New flush : Canopy) Damage on non-bearing trees can reduce tree growth increased time to bring trees into production

78 Canker / CLM Relationship Canker incidence can be up to 50% higher in groves where CLM damage is abundant (Sohi and Sandhu, 1968)

79 Choice & Timing of Pesticide Non-bearing citrus Applications soil-applied imidacloprid application is the best option for preventing CLM damage applications should be made days prior to anticipated flush expect about 8 weeks of control

80 Choice & Timing of Pesticide Non-bearing citrus Applications soil-applied imidacloprid just prior to summer flush and again just prior to the fall flush will provide control of CLM during this peak time for CLM damage will also provide control of Asian citrus psyllid during these times as well.

81 Choice & Timing of Pesticide Applications Bearing citrus preventing damage on bearing trees for canker management much more difficult must rely on foliar applications if control warranted there are no soil-applied systemic insecticides available for CLM control on large, bearing trees

82 Choice & Timing of Pesticide Bearing citrus Applications as a general rule, there have never been any soilapplied systemic organophosphate or carbamate insecticides shown to provide effective control of CLM damage this includes aldicarb (Temik), dimethoate, oxamyl (Vydate), metasystox (MSR)

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85 Control of Damage by Citrus Leafminer Soil imidacloprid application: Sept. 4; Foliar applications: Sept. 18

86 Control of Damage by 60 Citrus Leafminer Spint or Agr i- mek + oil Unt r eat ed Percent leaf damage June 6 June 13 June 21 Treatments applied May 19

87 Timing of application for leafminer control [FOLIAR APPLICATIONS] 13 days from general budbreak is earliest time for application Last potential date for leafminer application is 31 days after budbreak

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89 Effects of Cultural Practices Promoting winter flush may result in higher CLM populations earlier in the season hedging and topping excessive irrigation fertilization regimes

90 Biological Control of Citrus Leafminer Ageniaspis citricola: Imported into Florida from Australia in 1994 Parasitism rates up to 86% observed late in the season

91 Use of Pheromones in Leafminer Management New non-pesticide approaches to CLM control in development Previous lecture by L. Stelinski

92 Aphids (Order Homoptera)

93 Aphids Depend on newly expanding leaves for their development Leaf curling Large amounts of honeydew (blocks photosynthesis) treatment warranted on young trees when > 50% of new foliage is infested

94 Brown Citrus Aphid (BCA) Toxoptera citricida Vector of citrus tristeza virus

95 Pseudodorus clavatus Diptera: Syrphidae

96 Cycloneda sanguinea Harmonia axyridis

97 Green Lacewings Order: Neuroptera Family: Chrysopidae

98 Partitioned Mortality among BCA Cohorts Immokalee, FL, % 80% 60% 40% 20% Unknown Hardening Multiple Chrysopids Syrphids Coccinellids 0% Spring Summer Fall

99 Once a serious pest, especially from s No longer a serious problem Citrus Whitefly, Dialeurodes citri

100 Natural Enemies of Citrus Whitefly

101 EXOTIC PARASITOID OF CITRUS WHITEFLY Encarsia lahorensis Adult Successfully established in Florida in 1977 Whitefly nymph with parasitoid larva and pupa

102 Whitefly Fungi Effective with the right environmental conditions Aegerita sp. Aschersonia spp.

103 Foliage Pests Mature Trees Pests that reduce the overall health of tree Leaf drop Honeydew / sooty mold development

104 Spider Mites Citrus Red Mite (Panonychus citri) Texas Citrus Mite (Eutetranychus banksi)

105 Spider Mites Dry conditions favor rapid population growth Natural enemies exist, but can t keep up with populations under dry conditions Highest populations September May (dry period) 5-10 spider mites per leaf is action level for treatment if populations are not in decline Higher percentage of males indicates population declining

106 Leaf drop caused by spider mites (January)

107 Females (Short legs) Male (long legs) Many females, eggs present, few males = population rapidly growing

108 Scale pests of foliage Brown Soft Scale, Coccus hesperidum Black Scale, Saisettia neglecta Cottony Cushion Scale, Icerya purchasi Green scale, Coccus viridis

109 Honeydew from scale insects deposited on leaves = sooty mold

110 Why do many Homopterans / Hemipterans produce honeydew? too much water can be a bad thing mechanism to cope with foods high in water content? Scale insects psyllids

111 Foregut Temporary storage and grinding of food Midgut Digestion & absorption of nutrients into body Alkaline ph 7 Hindgut Re-absorption of water, salt & other nutrients before excretion of (dry) nitrogenous waste (frass)

112 Insect Digestive and Excretory Systems Homopteran insects honeydew producers FC = filter chamber; used to pass water directly out the rectum thus concentrating plant sap before it is absorbed into the insect body

113 Insects and Mites associated with plant diseases Brief overview of biology pathogen aspects will be covered in more detail in March 16 lecture

114 Asian citrus psyllid Diaphorina citri First found in Florida June 1998

115 Citrus Greening Disease

116 Asian Citrus Psyllid Distribution (FL) First detected in dooryard citrus trees in south Florida in 1998 subsequent finds in nursery plants (orange jasmine [Murraya paniculata]) in discount stores throughout the state psyllid well established in primary citrus growing areas of FL and cannot be eradicated

117 The Home Depot Effect After Asian citrus psyllid colonized SE Florida (red), it moved on Murraya paniculata to other counties very rapidly. Rapid movement made eradication unfeasible Now found in SE areas of Texas and Mexico and CA in 2008

118 Asian Citrus Psyllid 5 nymphal stages 10 generations / year Life cycle takes days egg adult in 2 weeks at F

119 Adult Asian citrus psyllids 3-4 mm in length mottled wings wings held rooflike over body

120 Asian Citrus Psyllid Adults Adult psyllids can feed on both new and mature leaf flushes; prefer young leaves When young leaves not available, adult psyllids are found on underside of mature leaves feeding on leaf midvein Mean longevity of females increases with decreasing temperature within F (= C)

121 Adults gather at newly emerging growing tips and on young flushes, feed and mate

122 Factors affecting psyllid populations The two main factors regulating psyllid population growth are: 1.Temperature 2.New leaf flush

123 Asian Citrus Psyllid Eggs Adults oviposit ONLY on young leaf flush Eggs are about 0.3 mm long and almond shaped Eggs are pale when deposited, turn yellow then orange as they mature. Often difficult to see without hand lens

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125 Duration of egg stage (in days) and hatch survival Temp ( F/ C) Days to hatch Survival 50 F / 10 C F / 15 C 9.74 ± % 68 F / 20 C 7.03 ± % 77 F / 25 C 4.15 ± % 82 F / 28 C 3.46 ± % 86 F / 30 C 3.29 ± % 91.4 F / 33 C 0 0 Data from Liu & Tsai, Ann. Appl. Biol. 137:

126 Psyllid developmental times (in days) Temp ( F/ C) Egg to adult 50 F / 10 C 0 59 F / 15 C 49.3 ± F / 20 C 28.8 ± F / 25 C 17.0 ± F / 28 C 14.1 ± F / 30 C 16.3 ± F / 0 33 C Data from Liu & Tsai, Ann. Appl. Biol. 137:

127 Asian Citrus Psyllid Nymphs 0.3 mm long in the first instar 1.6 mm long as fifth instars. Nymphs are yellow in color with red eyes and visible wing pads in larger nymphs

128 Asian Citrus Psyllid Nymphs early nymphal stages easily mistaken for aphids white carbohydrate secretions provides an easy means of distinguishing from aphids at a distance.

129 Nymphal developmental times (in days) Temp ( F/ C) Total nymphal stages Survival (%) 50 F / 10 C Failed to develop beyond 3 rd instar 59 F / 15 C 39.6 ± F / 20 C 21.8 ± F / 25 C 12.8 ± F / 28 C 10.6 ± F / 30 C 13.0 ± F / 33 C Failed to develop beyond 4 th or 5 th instar Data from Liu & Tsai, Ann. Appl. Biol. 137:

130 Low temperature developmental thresholds 1 st instar 53 F (11.7 C) 2 nd instar 51 F (10.7 C) 3 rd instar 50 F (10.1 C) 4 th instar 51 F (10.5 C) 5 th instar 52 F (10.9 C)

131 Effects of Cold Weather on Psyllid Populations January 2-3, 2008

132 CREC Research Grove 8-10 Hamlin orange

133 Evaluating psyllid mortality Caged 600 psyllids (30 psyllids/tree) Cages placed in plots with and without freeze protection (irrigation) Inside vs outer canopy

134 Factors Evaluated Freeze protection vs. no freeze protection Effects of location of psyllids in tree canopy Recorded leaf temperatures and trunk base temperatures every 2 hours Data loggers within cages recorded temps every 15 mins. Weather station data also collected

135 CREC Jan 3, 2008 (8:00 AM)

136 CREC Temp s (Jan 2-3, 2008) 10+ hrs below freezing

137 Effects of Freeze Protection on Psyllid Survival F = 3.55 P = 0.076

138 Mortality of Psyllids Located Inside and Outside Canopy F = 2.31 P =

139 Overall Psyllid Mortality Average mortality rate: 60.8% Minimum mortality observed: 20.7% Lowest mortality in freeze protection plots With no freeze protection lowest 41.2% Maximum mortality observed: 86.8%

140 Conclusions At CREC location sustained freezing temperatures reduced psyllid populations an average of 60% Psyllid mortality likely to vary by location based on duration and intensity of cold Cold temperatures in the citrus growing regions of Florida are not enough to reduce the need for early season psyllid control

141 Psyllid feeding damage In the absence of the greening pathogen, psyllid control previously targeted young trees to protect new growth from damage that results in reduced tree growth.

142 Dieback of new growth

143 Witche s broom effect

144 Psyllid nymphs produce waxy secretions similar to aphid or scale insect honeydew

145 Sooty mold - growing on sticky residues from secretions from psyllid nymphs

146 Monitoring Psyllid Populations Important to monitor when new flush is available Critical time is spring and fall when temperatures are cooler and flush is abundant Check expanding terminals for aggregations of psyllids Adult psyllids found on underside of leaves near leaf midvein when no new flush is available

147 Monitoring Psyllid Populations Eggs tucked away in very young, newly forming leaves and leaf buds.

148 Monitoring Psyllid Populations Inspect new leaf and shoot flushes of citrus and citrus relatives such as orange jasmine, Murraya paniculata. Look for white honeydew and leaf distortion on new leaf flush and shoots.

149 Biological Control of Psyllids There are numerous natural enemies of psyllids present that suppress psyllid populations, especially in the summer and fall Use of broad spectrum foliar insecticides will present a problem in maintaining populations of the natural enemies of psyllids and other potential pest species

150 Natural Enemies of Juvenile D. citri in Florida Ladybeetles (Coccinellidae) Curinus coeruleus Cycloneda sanguinea Exochomus childreni Harmonia axyridis Olla v-nigrum Green Lacewings (Chrysopidae) Chrysoperla rufilabris Ceraeochrysa spp. (2-3) Brown Lacewings (Hemerobiidae) Micromus posticus Hoverflies (Syrphidae) Allograpta obliqua Spiders Hibana velox (Anyphaenidae) Chiracanthium inclusum (Clubionidae) Hentzia palmarum (Salticidae) Oxyopes sp. (Oxyopidae) Hemiptera (Anthocoridae) Orius sp. Ants (Formicidae) Dorymyrmex bureni Pseudodmyrmex gracilis Parasitoids Tamarixia radiata

151 Biological Control: Olla v-nigrum J. P. Michaud

152 Biological Control: Harmonia axyridis Multicolored Asian ladybeetle

153 Classical Biological Control Tamarixia radiata External Parasite Originally from India Variable incidence in Florida.

154 Tamarixia Radiata: Adult and Egg

155 T. radiata: Larva and Prepupa

156 Tamarixia Survey surveyed major citrus growing areas establishment of Tamarixia? parasitism rates?

157 T. radiata parasitism (%) Tamarixia survey average parasitism rates less than 20% throughout most of the season 100 C M A M J J A S O N D J F M A

158 Additional Parasitoid Introductions Diaphorencyrtis aligarhensis Encyrtidae Originally released along with T. radiata; failed to establish Releases now being made with parasitoids from geographic regions with climates more similar to FL

159 Chemical Control of the Asian Citrus Psyllid

160 Soil-applied Insecticides for Psyllid Control Young trees (< 6-8 feet tall) Soil applied systemic insecticides are most effective (imidacloprid, thiamethoxam, clothianidin) must be applied about 2 weeks prior to flush for best results in sandy soils, can be washed away if heavy rains occur with hr post treatment have fewer negative effects on natural enemy populations

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162 Foliar-applied Insecticides for Psyllid Control Use on both young and mature trees: best to target psyllids before new flush present Control adults before eggs laid typically broad-spectrum products most have negative effects on natural enemies Will discuss in more detail later (next lecture)

163 Brevipalpus mites and Citrus Leprosis

164 Tenuipalpidae Over 622 species in 26 genera worldwide False spider mites, flat mites Primarily found in tropical/subtropical areas Genus Brevipalpus most important economic group

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166 Adult female Adult male Egg Teliochrysalis Life cycle of a false spider mite Larva Deutonymph Protochrysalis Deutochrysalis Protonymph

167 Comparative developmental rates, egg production and adult longevity of Brevipalpus phoenicis and Panonychus citri at 27 0 C (Duration in days) B. phoenicis P. citri Egg Larva Protonymph Deutonymph Egg-Adult Adult Longevity Host Oroxylum indicum Citrus sp. Authors: Beavers & Hampton 1971; Lal 1978; Saito 1979

168 Brevipalpus californicus, B. obovatus and B. phoenicis Two problems: Mites can develop to large numbers on various host plants. They have toxic saliva that can result in feeding injuries to citrus and other economic crops. Mites are vectors of one or more unassigned Rhabdoviruses in citrus, coffee, passion fruit, orchids and numerous woody ornamental plants.

169 Brevipalpus spp. Examples of direct feeding damage The following images ARE NOT LEPROSIS

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178 Leprosis Problem on sweet orange varieties Caused by virus that is not systemic in plant B. phoenicis is the only confirmed vector Miticide costs on Brazilian citrus exceed 90 million US dollars per year (Omoto 2000) Currently not in Florida (is present in Mexico)

179 Citrus Leprosis (symptoms) Chlorotic leaf lesions becoming brown with or without necrotic centers Flat or slightly raised necrotic areas on twigs and leaves Flat or depressed lesions on fruit with concentric patterns and gumming Abscission of leaves and fruit and twig dieback due to extensive lesion development

180 Leprosis: Fruit Lesions

181 Leprosis : Fruit Drop

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183 Sharpshooters and Citrus Variegated Chlorosis

184 Citrus Variegated Chlorosis Causal agent Xylella fastidiosa, a xylem limited bacteria Found in Brazil, Argentina, Paraguay and recently identified in Costa Rica Transmitted by sharpshooter leafhoppers Infects most citrus cultivars

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187 My Next Lecture Insecticides and modes of action How to develop a comprehensive pest management program in the presence of ACP/HLB