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16 November 2021

Phyllocnistis citrella (citrus leaf miner)

Datasheet Types: Pest, Natural enemy, Invasive species

Abstract

This datasheet on Phyllocnistis citrella covers Identity, Overview, Distribution, Dispersal, Hosts/Species Affected, Diagnosis, Biology & Ecology, Natural Enemies, Impacts, Prevention/Control, Further Information.

Identity

Preferred Scientific Name
Phyllocnistis citrella Stainton
Preferred Common Name
citrus leaf miner
Other Scientific Names
Lithocolletis citricola
Phyllocnistis citricola Shiraki
International Common Names
English
citrus leafminer
leafminer of citrus
Spanish
minador de la hoja de los cítricos
minador de las hojas de los cítricos
French
mineuse des feuilles du l'oranger
mineuse du citronnier
Local Common Names
Germany
citrus-miniermotte
Schneckenmotten-Art
Japan
Mikan-hamoguriga
Netherlands
Citrus-bladboorder
Djeroek-mineerder
Mineerrups
EPPO code
PHYNCI (Phyllocnistis citrella)

Pictures

Phyllocnistis citrella (citrus leaf miner); the adult is a very small, whitish moth, only 2mm in length when at rest. Its wingspan is 4 mm.
Adult
Phyllocnistis citrella (citrus leaf miner); the adult is a very small, whitish moth, only 2mm in length when at rest. Its wingspan is 4 mm.
©David Agassiz
Phyllocnistis citrella (citrus leaf miner); symptoms on a citrus leaf. The larval stage causes serpentine mines with a silvery appearance.
Larval damage
Phyllocnistis citrella (citrus leaf miner); symptoms on a citrus leaf. The larval stage causes serpentine mines with a silvery appearance.
©David Agassiz
Phyllocnistis citrella (citrus leaf miner); young citrus leaf recently infested. The larva feeds in the epidermis causing the serpentine mine.
Larval damage
Phyllocnistis citrella (citrus leaf miner); young citrus leaf recently infested. The larva feeds in the epidermis causing the serpentine mine.
©Peter A.C. Ooi/Tropical Press Sdn Bnd

Taxonomic Tree

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Description

The morphology of P. citrella has been described by Heppner (1993) and Zhang et al. (1994):

Adults

P. citrella is a very small, whitish moth, only 2 mm in length when at rest. Its wingspan is 4 mm. Markings comprise black and brown lines with an apical black spot, placed so that when at rest it resembles a small insect facing in the opposite direction. The antennae are three-quarters the length of the wing.

Larvae

P. citrella larvae are 3 mm long when fully fed. They are translucent greenish-yellow. The mines in which they live have a distinctive silvery appearance. The fifth-instar larva and prepupa have been described by Heppner (1993).

Pupae

P. citrella pupae have been described by Heppner (1993).

Distribution

Originally an Asiatic species, P. citrella was discovered in Florida, USA, in 1993 and has since spread throughout the state. It was found in the Mediterranean basin in 1994 where it has since spread rapidly. It is also spreading in Central and South America and has been reported from southern Africa and West Africa.

In addition to the records on the map, P. citrella has been identified in Lebanon, Libya, Mozambique, Brazil and Colombia (J LaSalle, IIE, UK, personal communication, 1997). It has also been identified in Oman (T Pittaway, CABI, Wallingford, UK, personal communication, 1996) and Zimbabwe (DJL Agassiz, IIE, UK, personal communication, 1997).

Distribution Map

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Distribution Table

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Risk of Introduction

Now that P. citrella is found in all of the world's citrus-growing areas the question of phytosanitary risk has little meaning.

Plant Trade

Plant parts liable to carry the pest in trade/transportPest stagesBorne internallyBorne externallyVisibility of pest or symptoms
Leaves
arthropods/eggs
arthropods/larvae
Yes Pest or symptoms usually visible to the naked eye
Plant parts not known to carry the pest in trade/transport
Bark
Bulbs/Tubers/Corms/Rhizomes
Flowers/Inflorescences/Cones/Calyx
Fruits (inc. pods)
Growing medium accompanying plants
Roots
Seedlings/Micropropagated plants
Stems (above ground)/Shoots/Trunks/Branches
True seeds (inc. grain)
Wood

Hosts/Species Affected

A list of reported and potential hosts is given by Heppner (1993). A pest of citrus, P. citrella also attacks other Rutaceae.

Hosts also include Loranthus sp. (on citrus), Pongamia pinnata and Alseodaphne semicarpifolia.

Host Plants and Other Plants Affected

HostFamilyHost statusReferences
Aegle marmelos (golden apple)RutaceaeUnknown
Cinnamomum verum (cinnamon)LauraceaeOther 
CitrusRutaceaeMain
Citrus aurantiifolia (lime)RutaceaeOther
Citrus aurantium (sour orange)RutaceaeMain
Citrus iyo Unknown
Citrus jambhiri (rough lemon)RutaceaeUnknown
Citrus limetta (sweet lemon tree)RutaceaeUnknown
Citrus limon (lemon)RutaceaeUnknown
Citrus limonia (mandarin lime)RutaceaeUnknown
Citrus maxima (pummelo)RutaceaeUnknown
Citrus medica (citron)RutaceaeUnknown
Citrus reticulata (mandarin)RutaceaeUnknown
Citrus sinensis (sweet orange)RutaceaeUnknown
Citrus unshiu (satsuma)RutaceaeUnknown
Citrus x paradisi (grapefruit)RutaceaeMain
Jasminum (jasmine)OleaceaeOther 

Growth Stages

Vegetative growing stage

Symptoms

The mines produced by P. citrella, chiefly on the underside of leaves, are easily detected. Mining results in deformed leaves and reduced photosynthetic capacity.

List of Symptoms/Signs

Symptom or signLife stagesSign or diagnosisDisease stage
Plants/Leaves/abnormal leaf fall   
Plants/Leaves/internal feeding   
Plants/Leaves/internal feeding   
Plants/Leaves/leaves rolled or folded   
Plants/Leaves/necrotic areas   

Habitat List

CategorySub categoryHabitatPresenceStatus
Terrestrial    

Biology and Ecology

Descriptions are given by Heppner (1993) and Zhang et al. (1994):

Eggs

P. citrella eggs are laid singly on the underside of leaves of the host plant. They hatch in 2-10 days.

Larvae

P. citrella larvae usually mine the under surface of a leaf, but attack both surfaces in heavy infestations, and occasionally fruit. The serpentine mine has a silvery appearance and reaches a length of 50-100 mm. Young leaves are attacked and mines can cause leaf curl. Up to 20 mines per leaf have been recorded on elephant lemon in India. There are four larval instars including a pre-pupal stage when the larva does not feed. Development time is 5-20 days.

Pupae

Pupation takes place within the mine, near the leaf margin, under a slight curl of the leaf. Pupation takes 6-22 days.

Adults

P. citrella adults emerge at dawn and are active in the morning. They also fly at dusk and by night. Continuously brooded, up to 13 generations have been reported in a year in India and Egypt, 7 in a year in Tuscany, Italy.

Overwintering usually takes place in the larval or pupal stage.

Natural enemy of

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Notes on Natural Enemies

A list of parasitoids recorded is provided by Heppner (1993). Further lists in many countries have been produced since that date, notably Ujiye et al. (1996).

There is a vast guild of parasitoids which can attack P. citrella but those which have been recorded as having a significant effect are Ageniaspis citricola, Cirrospilus ingenus and Tetrastichus spp. in Taiwan; Citrostichus phyllocnistoides, Tetrastichus spp., Chrysonotomyia spp., Apleurotropis spp. and Cirrospilus quadristriatus in southern China. The green lacewings (Neuroptera) are important predators.

Natural enemies

Natural enemyTypeLife stagesSpecificityReferencesBiological control inBiological control on
Ageniaspis citricolaParasite
Larvae
    
Ancylopteryx octopunctataPredator
Eggs
Larvae
Pupae
    
Apotetrastichus sericothoraxParasite     
Asecodes delucchiiParasite     
Asecodes erxiasParasite     
Bacillus thuringiensis (Bt)      
Chrysocharis pentheusParasite     
Chrysocharis vononesParasite    
Cirrospilus brevisParasite    
Cirrospilus diallusParasite     
Cirrospilus floridensisParasite    
Cirrospilus neotropicusParasite    
Cirrospilus pictusParasite     
Cirrospilus quadristriatusParasite
Pupae
    
Citrostichus phyllocnistoidesParasite
Larvae
    
Closterocerus trifasciatusParasite     
Elasmus phyllocnistoidesParasite    
Mallada boninensisPredator
Adults
Eggs
Larvae
Nymphs
Pupae
    
Orius albidipennisPredator     
Pnigalio agraulesParasite     
Pnigalio minioParasite     
QuadrastichusParasite
Larvae
    
Semielacher petiolatusParasite
Larvae
    
Sympiesis striatipesParasite     
Zagrammosoma multilineatumParasite     
Zaommomentedon brevipetiolatusParasite     
Zaommomentodon brevipetiolarisParasite
Larvae
    

Impact

P. citrella is a major pest of citrus, found in virtually all major citrus-producing areas. Heavy infestations can hinder the growth of newly planted trees or reduce fruit production of mature trees. Larval feeding reduces the photosynthetic capacity of leaves and increases the susceptibility of leaves to citrus bacterial canker, Xanthomonas axonopodis pv. citri (Gottwald et al., 2007; Hall et al., 2010)
Originating in the Far East, P. citrella spread rapidly to other citrus-growing areas during the 1990s. Damage to young trees can be severe and populations can increase dramatically under heavy pesticide regimes such as those currently practiced in Florida (USA) for control of a separate pest and vector of citrus greening disease, the Asian citrus psyllid Diaphorina citri. The location of larvae inside the mine protects the insects from most topical sprays.
Huang and Li (1989) considered the economic threshold of P. citrella to be 0.74 larvae per susceptible (tender) leaf. If the percentage of damaged area in susceptible leaves is below 20% there will be no negative impact on growth, development or yield of citrus fruit. However, a major concern of producers of high quality fresh fruit for export markets is the increased susceptibility of leaves damaged by the leafminer to infection by citrus canker disease. Loss of access to international markets due to phytosanitary controls is a major economic impact related to leafminer damage.

Detection and Inspection

Look on the young leaves of citrus, especially the underside, for evidence of a serpentine mine with a silvery appearance.

Prevention and Control

Due to the variable regulations around (de)registration of pesticides, your national list of registered pesticides or relevant authority should be consulted to determine which products are legally allowed for use in your country when considering chemical control. Pesticides should always be used in a lawful manner, consistent with the product's label.
Cultural Control

In Italy, Mineo et al. (1997) found that if Parietaria is grown near the citrus trees affected there is a lepidopterous leaf miner Cosmopterix pulchrimella which is an alternative host to several of the parasitoids and therefore a reservoir for them.

Zhou et al. (1994) found that planting Ageratum conyzoides as ground cover in hilly citrus orchards in Hunan, China, increased relative humidity in summer and temperature in winter and also decreased summer temperatures in the canopy and soil, thus improving conditions for the survival of P. citrella's natural enemies. As a consequence, damage by P. citrella in spring was reduced.

Zhang et al. (1994) describe a traditional Chinese management method which includes the collection and destruction of fallen leaves in winter and pruning to restrict budding to late autumn, ensuring even budding stands. This restricts growth to the season when P. citrella moths are at lowest density. In addition, fertilization and the avoidance of drought keeps trees in a healthy state, thus improving their resistance to attack by P. citrella.

Biological Control

Smith and Hoy (1995) have described the use of the parasitoids Ageniaspis citricola and Cirrospilus quadristriatus in classical biological control.

In southern China, Chen et al. (1989) found that the naturally occurring predators Ancylopteryx octopunctata and Chrysopa boninensis [Mallada boninensis] controlled the population, and only if weather or chemical sprays reduce their numbers did these need supplementation by laboratory-reared insects.

Bacillus thuringiensis strains 04-1, 454 and HD-1 have all been found to cause 80-97% mortality in P. citrella (Zhang et al., 1994).

In Taiwan, Lao and Chiu (1986) (quoted in Zhang et al., 1994) reported that natural enemies attack 90% of leaf-miners, making chemical control unnecessary.

To combat the recent spread of P. citrella, biological control programmes have been started in several countries. To date, natural enemies have been established in Florida, USA (Smith and Hoy, 1995), Australia (Neale et al., 1995) and Israel (Argov and Rossler, 1996). It is not yet known if these introductions will succeed in bringing P. citrella under satisfactory control.

A list of the natural enemies introduced into Italy is given by Siscaro et al. (1999). A general list of introductions is given by Schauff et al. (1998).

Host-Plant Resistance

Padmanaban (1994) evaluated 31 species or varieties of citrus for leaf-miner infestation at Basar, India. Lowest infestation levels were observed in the sweet orange variety Ruby Malta (9.33%) and in the hybrid variety Kinnow Mandarin (8.34%). The data obtained indicated that the variation in susceptibility could be due to the availability of tender flushes and seasonal fluctuation in the leaf-miner population.

Batra et al. (1992) in the Indian Punjab tested 134 citrus species/cultivars for resistance to P. citrella. The varieties Carrizo, Sacaton, Savage, Troyer, Yama Citrange, Citrumelo (Poncirus trifoliata x grapefruit), Cambell Valencia, Pomary and Rubidoux, and Muraya koenigii were resistant to P. citrella on the basis of leaf infestation. Nineteen species/cultivars were fairly resistant, 27 slightly susceptible, 53 moderately susceptible and 25 highly susceptible. Cleopatra, a promising rootstock for sweet orange, was slightly susceptible whereas the commercial rootstock Jatti Khatti [C. jambhiri] was highly susceptible. Of 26 hybrids studied, P. trifoliata x sweet orange, Rangpur Lime x Troyer and Kinnow x Mosambi were the least susceptible.

Singh and Rao (1978) tested 34 cultivars of citrus for susceptibility in India in 1975 and 1976. Queen mandarin had the least incidence of infestation, and Meyer lemon and Rangpur lime were the most susceptible in both years. In general, Citrus reticulata, Kinnow mandarin, Citrus reshni and Poncirus trifoliata had less incidence compared to limes (C. limonia, C. latifolia and C. aurantifolia), lemons and satsumas. Variation in susceptibility of the species and cultivars was linked to growth flushes and seasonal fluctuations in the leaf-miner population.

Chemical Control

Many insecticides are effective against P. citrella, but they are always liable also to reduce numbers of natural enemies which may control the pest to within acceptable thresholds. The location of larvae inside the mine protects the insects from most topical sprays. Systemic insecticides are only effective in young trees. Natural enemies can be effective if management practices allow.

Vargas et al. (1999) tested the percentage efficacy of three insecticides for selective control through a field trial carried out on orange trees in Chile, evaluating larval mortality at new growing shoots, in the spring season of 1998. Treatments, applied by spraying on the foliage, were the following: abamectin, imidacloprid, tebufenozide and an untreated control. Mortality values, evaluated by sampling on the fourth day after application, were corrected for control mortality using Abbott's formula, and were as follows: imidacloprid 80.34%, tebufenozide 44.59%, and abamectin, 39.62%.

Nucifora et al. (1999) found that a single application of imidacloprid resulted in the control of P. citrella for >100 days.

Buchelos and Foudoulakis (2000) in Greece applied fenoxycarb on young citrus trees. During 1996, the compound, applied every 10 days (with or without adjuvant), gave satisfactory protection from P. citrella without substantially harming C. noacki populations. No phytotoxicity symptoms were observed during the experiments.

Smith and Hoy (1995) have described chemical control as not viable because of the cost of multiple applications, the inaccessibility of larvae within the mine and the likely development of resistance.

Zhang et al. (1994) stated that pyrethrins have been chiefly used in China, although Huang and Li (1989) showed that P. citrella has already built up resistance to them. Pyrethroids such as cypermethrin, cyhalothrin, fenvalerate, fenpropathrin, esfenvalerate and deltamethrin have been used. The organophosphates phosmet, quinalphos and dimethoate and the carbamates carbaryl and cartap, have also been used.

In Australia, the biorational insect growth regulator fenoxycarb has been used more frequently than more harmful broad-spectrum compounds (CDFA, 1993).

Liu et al. (1992) found that treatment of citrus with avermectins gave 86.2-100% control of P. citrella.

In field trials in Nagpur, Maharashtra, India, Katole et al. (1993) found that fish oil resin soap and Pongamia oil were the most effective treatments, followed by dimethoate, mahua (Madhuca longifolia) oil and neem oil. Indiara (of unstated composition), castor oil and Neemark (an extract of neem) were ineffective.

However, in Karnataka, India in 1989 Jothi et al. (1993) tested neem, mahua (Madhuca longifolia) and Pongamia oils (2 and 4%) and neem and Pongamia seed extracts (2%) against P. citrella on limes. All the treatments reduced the P. citrella population, with neem seed extract being the most effective.

Pheromonal Control
Ando et al. (1985) found Japanese populations of P. citrella were attracted to traps baited with (Z,Z)-7,11-hexadecadienal; however, attempts to show attraction of this material to populations in other countries were not successful (Sant’ana et al., 2003).
Leal et al. (2006) and Moreira et al. (2006) detected three active compounds from female pheromone gland extracts. Of these, (Z,Z,E)-7,11,13-hexadecatrienal (triene) and (Z,Z)-7,11-hexadecadienal (diene) used together were shown to be necessary and sufficient for attraction in Florida, USA (Lapointe et al., 2006; 2009). Control of P. citrella by mating disruption with these two extracts was effective at very low rates of pheromone deployment (Stelinski et al., 2008). Either pheromone compound alone is capable of disrupting mating. Initially, an emulsified wax formulation was developed for slow-release of P. citrella pheromone applied to citrus by a specialized tractor-mounted applicator (Lapointe et al., 2009; Lapointe and Stelinski, 2011; Stelinski et al., 2010). The triene was approximately 13 times more effective compared with the diene alone and was as effective or more effective compared with the natural 3:1 blend (Lapointe et al., 2009; 2011; 2015). As a result, an emulsified wax was formulated with the triene component only as the active ingredient. A hand-applied solid elastomeric dispenser was developed and marketed in limited quantities in 2014. A single application of the device may be capable of effective mating disruption for an entire growing season (Lapointe et al., 2015).

IPM Programmes

Zhang et al. (1994) outlined a programme using cultural practices, with the possibility of releasing parasitoids and predators when necessary, with carefully timed applications of Bacillus thuringiensis. Mating disruption should provide an excellent management option if the pheromone dispensers become widely available to growers, especially when combined with biological control and minimal chemical control. 

Links to Websites

NameURLComment
GISD/IASPMR: Invasive Alien Species Pathway Management Resource and DAISIE European Invasive Alien Species Gatewayhttps://doi.org/10.5061/dryad.m93f6Data source for updated system data added to species habitat list.
Global register of Introduced and Invasive species (GRIIS)http://griis.org/Data source for updated system data added to species habitat list.

References

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