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Gymnandrosoma aurantianum
(citrus fruit borer)

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Datasheet

Gymnandrosoma aurantianum (citrus fruit borer)

Summary

  • Last modified
  • 27 March 2020
  • Datasheet Type(s)
  • Invasive Species
  • Pest
  • Preferred Scientific Name
  • Gymnandrosoma aurantianum
  • Preferred Common Name
  • citrus fruit borer
  • Taxonomic Tree
  • Domain: Eukaryota
  •   Kingdom: Metazoa
  •     Phylum: Arthropoda
  •       Subphylum: Uniramia
  •         Class: Insecta
  • Summary of Invasiveness
  • Gymnandrosoma aurantianum is a small blackish brown to black tortricid moth with a whitish or pale pinkish, grub-like larva that feeds on the buds and fruit of several plant families, primarily Rutaceae and Sap...

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Pictures

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PictureTitleCaptionCopyright
Gymnandrosoma aurantianum (citrus fruit borer); adult female. Museum set specimen.
TitleAdult
CaptionGymnandrosoma aurantianum (citrus fruit borer); adult female. Museum set specimen.
Copyright©John W. Brown
Gymnandrosoma aurantianum (citrus fruit borer); adult female. Museum set specimen.
AdultGymnandrosoma aurantianum (citrus fruit borer); adult female. Museum set specimen.©John W. Brown
Gymnandrosoma aurantianum (citrus fruit borer); adult male. Museum set specimen.
TitleAdult
CaptionGymnandrosoma aurantianum (citrus fruit borer); adult male. Museum set specimen.
Copyright©John W. Brown
Gymnandrosoma aurantianum (citrus fruit borer); adult male. Museum set specimen.
AdultGymnandrosoma aurantianum (citrus fruit borer); adult male. Museum set specimen.©John W. Brown
Gymnandrosoma aurantianum (citrus fruit borer); adult female. Museum set specimen. USA.
TitleAdult
CaptionGymnandrosoma aurantianum (citrus fruit borer); adult female. Museum set specimen. USA.
Copyright©Todd M. Gilligan & Marc E. Epstein/TortAI: Tortricids of Agricultural Importance/USDA APHIS PPQ/Bugwood.org - CC BY-NC 3.0 US
Gymnandrosoma aurantianum (citrus fruit borer); adult female. Museum set specimen. USA.
AdultGymnandrosoma aurantianum (citrus fruit borer); adult female. Museum set specimen. USA.©Todd M. Gilligan & Marc E. Epstein/TortAI: Tortricids of Agricultural Importance/USDA APHIS PPQ/Bugwood.org - CC BY-NC 3.0 US
Gymnandrosoma aurantianum (citrus fruit borer); adult male. Museum set specimen. USA.
TitleAdult
CaptionGymnandrosoma aurantianum (citrus fruit borer); adult male. Museum set specimen. USA.
Copyright©Todd M. Gilligan & Marc E. Epstein/TortAI: Tortricids of Agricultural Importance/USDA APHIS PPQ/Bugwood.org - CC BY-NC 3.0 US
Gymnandrosoma aurantianum (citrus fruit borer); adult male. Museum set specimen. USA.
AdultGymnandrosoma aurantianum (citrus fruit borer); adult male. Museum set specimen. USA.©Todd M. Gilligan & Marc E. Epstein/TortAI: Tortricids of Agricultural Importance/USDA APHIS PPQ/Bugwood.org - CC BY-NC 3.0 US

Identity

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Preferred Scientific Name

  • Gymnandrosoma aurantianum Lima, 1927

Preferred Common Name

  • citrus fruit borer

Other Scientific Names

  • Acharneodes cnemoptila Meyrick, 1930
  • Argyroploce sideroptila Meyrick, 1932
  • Argyroploce torticornis Meyrick, 1931
  • Cryptophlebia cnemoptila Diakonoff, 1959
  • Ecdytolopha aurantiana White, 1993
  • Ecdytolopha aurantium Lima, 1927
  • Ecdytolopha pithecolobiae Powell et al., 1995
  • Ecdytolopha torticornis Powell et al., 1995
  • Gymnandrosoma pithecolobiae Busck, 1934
  • Gymnandrosoma torticornis Meyrick, 1931

International Common Names

  • English: macadamia nut borer; orange worm

EPPO code

  • ECDYAU (Ecdytolopha aurantianum)

Summary of Invasiveness

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Gymnandrosoma aurantianum is a small blackish brown to black tortricid moth with a whitish or pale pinkish, grub-like larva that feeds on the buds and fruit of several plant families, primarily Rutaceae and Sapindaceae. In 2000, economic loss caused by the damage of G. aurantianum to citrus fruit in the state of São Paulo, Brazil was estimated at 50 million USD. The species is native to much of South America, but may be introduced in Central America and the Caribbean, where it feeds on hosts other than citrus. It is encountered in native forests, orchards and urban landscapes, usually below 500 m elevation. In Costa Rica it has been found at higher elevations, such as Tilarán (564 m elevation), Turrialba (646 m elevation) and Juan Viñas (1165 m elevation). Although there is no evidence that it has successfully invaded any region outside of the New World tropics, the species has been intercepted at ports-of-entry on several occasions in shipments of citrus from Brazil, and the NPPO of Spain has suggested that G. aurantianum should be added to the EPPO Alert List.

Taxonomic Tree

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  • Domain: Eukaryota
  •     Kingdom: Metazoa
  •         Phylum: Arthropoda
  •             Subphylum: Uniramia
  •                 Class: Insecta
  •                     Order: Lepidoptera
  •                         Family: Tortricidae
  •                             Genus: Gymnandrosoma
  •                                 Species: Gymnandrosoma aurantianum

Notes on Taxonomy and Nomenclature

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Gymnandrosoma aurantianum was described by Lima (1927) from Brazil as a pest of orange trees. Meyrick (1930; 1931; 1932) subsequently described Acharneodes cnemoptila Meyrick, 1930 from Brazil; Argyroploce torticornis Meyrick, 1931 from Trinidad; and Argyroploce sideroptera Meyrick, 1932 from Brazil; and Busck (1934) described Gymnandrosoma pithecolobiae from Cuba. All of these species are now considered synonyms of which G. aurantianum is senior (i.e., the oldest name) (Adamski and Brown, 2001).

Upon examining the type of A. torticornis in the Natural History Museum (London), Clarke (1958) recognized that it was related to G. aurantianum and transferred it to Gymnandrosoma. Diakonoff (1959) synonymized Gymnandrosoma with Ecdytolopha Zeller, 1875 (the older of the two names) and transferred cnemoptila to Cryptophlebia. Apparently, he was unaware of the other Meyrick species. Based on the proposed synonymy of Gymnandrosoma with Ecdytolopha, White (1993) transferred aurantianum to Ecdytolopha. Powell et al. (1995) followed this concept and treated both aurantianum and pithecolobiae in Ecdytolopha.

In a revision of the New World members of the Ecdytolopha group of genera, Adamski and Brown (2001) proposed a phylogeny that supported the separation of Ecdytolopha from Gymnandrosoma, and returned aurantianum to its original combination – Gymnandrosoma aurantianum. They also proposed the synonymy of the Meyrick and Busck names mentioned above.

Description

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Adults are small moths (forewing length 6.2-10.5 mm) with a dark brown forewing with indistinct reddish brown and black markings. The forewing is broadly triangular with the termen (outer margin) weakly convex. Females are slightly larger than males. Most individuals have a small white dot in the distal one-third of the forewing, and females typically have a small pale triangular patch from near the apex of the forewing. Males are distinguished from other species in the genus by a shallow notch in the subbasal portion of the antenna (with flagellomeres 6-10 smaller than the surrounding flagellomeres) and a large cluster of scales (hairpencil) from the hind tibia (Adamski and Brown, 2001). Images can be found in Gilligan and Epstein (2012).

In the male genitalia, the uncus, socii and gnathos are absent. The valvae are somewhat parallel-sided, except for a small triangular expansion near the middle of the venter, and evenly upcurved in the distal one-half (cucullus), with a few (4-6) large spines around the lower margin of the cucullus. The phallus is large and tubular, curved in the basal one-fourth creating a slightly “pistol shape,” and there is a dense patch of 100-130 cornuti (tiny internal spines), but the latter are deciduous (lost during copulation), and may be absent (Adamski and Brown, 2001). The presence of short, vertically arranged cornuti in the vesica of the phallus serves to separate G. aurantianum from species of the closely related genus Ecdytolopha.

The female genitalia are typical of most tortricids with a pair of modified, flattened papillae anales (ovipositor lobes) and long, slender apophyses. The ductus bursae is long and narrow, and the corpus bursae is oblong with two crescent-shaped blades (signa) (Adamski and Brown, 2001). Mated females can be recognized by the presence of a hardened translucent mass or coil inside the corpus bursae.

Eggs are 1.1-1.3 mm in length, flattened and circular or ovoid (Blanco-Metzler, 1994). At oviposition they are pale cream; they darken to a reddish brown as development proceeds (Blanco-Metzler, 1994).

Last instar larvae are 16-19 mm in length. The head is pale yellow to pale orange or brown (Adamski and Brown, 2001; Gómez Orellana et al., 2008). The thorax has a distinct yellow prothoracic shield and a pale pinkish to creamy white meso- and metathorax. The L-pinaculum on the prothorax is expanded posteriorly, extending beneath the spiracle. The abdomen is pale pinkish to creamy white with large and conspicuous brown pinacula (spots at the origin of setae). As in most tortricids, there is a dorsal “saddle” on abdominal segment 9, which serves as the common pinaculum for the D2 setae (see Adamski and Brown, 2001). In contrast to most tortricid larvae, an anal fork is absent on abdominal segment 10 (Adamski and Brown, 2001).

When ready to pupate, last instar larvae usually exit the fruit by lowering themselves to the ground on a silken thread or crawl down branches or the trunk of the host tree (Blanco-Metzler, 1994). Once on the ground, they make a cocoon of silk, frass and soil (Blanco-Metzler, 1994).The pupa is fusiform, 9-12 mm in length, 2.5-3.0 mm in width and brown. As in most tortricids, there are two rows of tiny spines across the dorsum of abdominal segments 2-7 and singe rows on segments 8 and 9. The posterior end of the pupa is blunt with a row of large thorns and two pairs of hooked setae on the dorsum of segment 10. Pupae are usually found in the soil (Cabrera-Asencio et al., 2013), but they may occasionally be present in fruit.

Distribution

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Gymnandrosoma aurantianum is almost certainly native to Brazil and possibly Argentina. However, it is uncertain how widespread the species was prior to European colonization of South America and the subsequent spread of agriculture. Its distribution in Central America and the Caribbean is more likely the result of inadvertent introductions, especially in the Caribbean where G. aurantianum is sympatric with endemic congeners on several islands, which likely evolved in isolation. G. aurantianum is usually found below 500 m elevation in its native habitat and in fruit orchards and urban landscapes, with occasional records from as high as 1000 m.

Distribution Table

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The distribution in this summary table is based on all the information available. When several references are cited, they may give conflicting information on the status. Further details may be available for individual references in the Distribution Table Details section which can be selected by going to Generate Report.

Last updated: 30 Mar 2020
Continent/Country/Region Distribution Last Reported Origin First Reported Invasive Reference Notes

North America

BarbadosPresent1925Adamski and Brown (2001)In a bean pod from Barbados intercepted in New York
Costa RicaPresent1979Adamski and Brown (2001)
CubaPresent1930Adamski and Brown (2001)Collected as adults at two localities
DominicaAbsent, Unconfirmed presence record(s)Fennah (1942)Probably Gymnandrosoma leucothorax
HondurasPresent1973Adamski and Brown (2001)A single adult from Tegucigalpa
MexicoPresent1908Adamski and Brown (2001)A few old records from Colima, Veracruz and Tabasco
NicaraguaPresent1959Adamski and Brown (2001)
PanamaPresent1965Adamski and Brown (2001)
Puerto RicoPresent1938Adamski and Brown (2001)
Trinidad and TobagoPresent1939White (1993)

South America

ArgentinaPresent1918Adamski and Brown (2001)Present in Entre Rios, Misiones (NE Argentina), Tucumán (NW)
BrazilPresent, Widespread1927Vianna (2015); Da Costa Lima (1927)Present in all states where citrus is grown
-AlagoasPresent1994Adamski and Brown (2001)
-AmazonasPresent1993Adamski and Brown (2001)
-BahiaPresent1931Adamski and Brown (2001)
-Espirito SantoPresent1991Adamski and Brown (2001)
-GoiasPresent1977Adamski and Brown (2001)
-MaranhaoPresent1970Adamski and Brown (2001)
-Mato GrossoPresent1970Adamski and Brown (2001)
-Minas GeraisPresent, Widespread1933Adamski and Brown (2001)
-ParaPresent1984Adamski and Brown (2001)
-ParanaPresent1970Adamski and Brown (2001)
-Rio de JaneiroPresent1919Adamski and Brown (2001)
-RondoniaPresent1989Adamski and Brown (2001)
-Santa CatarinaPresent1935Adamski and Brown (2001)
-Sao PauloPresent, Widespread1935Adamski and Brown (2001)
ColombiaPresent1977Adamski and Brown (2001)
EcuadorPresent1985Noboa et al. (2018)
French GuianaPresent1906Adamski and Brown (2001)
PeruPresent1972Escalante et al. (1981)
SurinamePresent1927Adamski and Brown (2001)
VenezuelaPresent1937Adamski and Brown (2001)Recorded from macadamia, peaches and citrus in orchards

History of Introduction and Spread

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Because there are few historical records of microlepidoptera from South America (the earliest concerted efforts were by Costa Lima and Pastrana in the 1920s and 1930s), data upon which to speculate about the potential spread of this species throughout the Neotropics are limited. Although it is occasionally intercepted in commodities (primarily Citrus) at foreign ports-of-entry around the globe (especially Spain and USA), there is no evidence that G. aurantianum has successfully invaded any region outside of the New World tropics.

Risk of Introduction

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Importation of fruit containing larvae in baggage is perhaps the most likely pathway of introduction. In the last ten years, G. aurantianum larvae have been intercepted 51 times at US ports-of-entry, with a majority of these detected in fruits for personal consumption (PestID, 2018). Interceptions are from a variety of fruits, including Psidium guajava (guava), Theobroma cacao (cacao), Inga edulis (ice-cream bean), Prunus persica (peach), Byrsonima crassifolia (nance fruit), Punica granatum (pomegranate), Mangifera indica (mango), Citrus tangerina (tangerine), Citrusparadisi (grapefruit), Melicoccus bijugatus (Spanish lime), Phaseolus vulgaris (green bean) and Pithecellobium dulce (madras thorn) (PestID, 2018). The countries of origin of the intercepted fruit were Brazil, Colombia, Cuba, Dominican Republic, Ecuador, Jamaica, Mexico, Puerto Rico and Venezuela. Fewer interceptions were detected in permit cargo, including cacao pods from Ecuador and Spanish lime from the Dominican Republic.

The fruit of citrus and a few other hosts of G. aurantianum are exported around the world from countries known to harbour this pest species, especially Brazil. Hence, an important potential pathway of introduction and subsequent spread is exported fruit, where larvae are difficult to detect because they are internal-feeders. Soil in which larvae have pupated is a potential but less important pathway. Therefore, fruit and plant stock represent the most likely modes of dispersal of the species. The large volume of citrus exported from South America, combined with the fact that G. aurantianum has already been intercepted at ports-of-entry in the USA and Spain demonstrates that a pathway exists for the spread of this species.

Several of the hosts of G. aurantianum are economically important fruit crops grown in many regions around the world, especially those with a Mediterranean climate and/or mild winters. The entire Mediterranean Basin may provide conditions favourable for the establishment of G. aurantianum. Hence, the potential for establishment and subsequent economic loss are relatively high in this region. During the EU project DROPSA (Strategies to develop effective, innovative and practical approaches to protect major European fruit crops from pests and pathogens), G. aurantianum was considered a potential risk for fruit production in Europe.

Habitat

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As with related genera and species in the tribe Grapholitini, G. aurantianum larvae feed internally on the seeds and fruit of the host plants. Because of the relatively wide range of plant families attacked by G. aurantianum, the species may be abundant in its native habitat, urban landscapes and agricultural environments. However, it is not known from outside the tropical regions of South and Central America and the Caribbean, where it usually occurs in humid, lowland environments.

Habitat List

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CategorySub-CategoryHabitatPresenceStatus
Terrestrial
Terrestrial – ManagedCultivated / agricultural land Present, no further details Natural
Managed forests, plantations and orchards Present, no further details Natural
Disturbed areas Present, no further details Natural
Urban / peri-urban areas Present, no further details Natural
Terrestrial ‑ Natural / Semi-naturalNatural forests Present, no further details Natural
Scrub / shrublands Present, no further details Natural

Hosts/Species Affected

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Gymnandrosoma aurantianum was described by Lima (1927) as a pest of citrus. In Brazil, it has become one of the most important pests of citrus, and damage from its larvae can render citrus fruit unmarketable for both fresh consumption and processing (Carvalho et al., 2015). Infested areas in Brazil have experienced yield losses of 5-50% (Revista Citricultor, 2016). Damage to citrus in the State of São Paulo was estimated at $50 million per year during the 1990s (Revista Citricultor, 2016). Historically, a yield loss of 10% or greater was reported for oranges in Dominica in 1921 and 1922 (Agricultural Department of Dominica, 1923). In Puerto Rico in 2011, approximately 5% of Spanish lime fruits were damaged by G. aurantianum (Cabrera-Asencio et al., 2013).

Significant losses have been reported from other countries and on other crops. G. aurantianum also is known to attack cultivated Macadamia integrifolia (macadamia) (Blanco-Metzler, 1994), cacao (PestID, 2018) and Plukenetia volubilis (Inca nut) (Leandro, 2013), damaging fruit and reducing yield. Other hosts are listed by Adamski and Brown (2001).

Growth Stages

Top of page Fruiting stage, Post-harvest

Symptoms

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The first sign of infestation on citrus is the accumulation of frass (faeces) at a tiny entry hole made by the larva on the surface of the fruit (Carvalho et al., 2015). The hole eventually becomes a brown, necrotic area (White, 1999). In oranges, larval infestations can cause fruits to yellow and fall prematurely (Agricultural Department of Dominica, 1923; Fundecitrus, 2007), as larval feeding accelerates decomposition and renders the fruit unmarketable (Anonymous, 1957; Cabrera-Asencio et al., 2013). Secondary infection from bacteria, fungi and other insects contributes to further fruit damage (White, 1993).

On macadamia, larvae burrow into the nuts and feed on the kernel, where frass can be seen at the point of entry, usually in the narrow space between adjacent nuts in a cluster (Blanco-Metzler, 1994). Larval feeding reduces nut quality and may result in premature falling of the nuts (Blanco-Metzler et al., 2007). In Costa Rica, 4.6-27.5% of macadamia nuts were damaged by G. aurantianum, depending on the sample year (Blanco-Metzler, 1994) and differences in macadamia cultivar (Blanco-Metzler, 1994; Blanco-Metzler et al., 2013).

List of Symptoms/Signs

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SignLife StagesType
Fruit / discoloration
Fruit / frass visible
Fruit / internal feeding
Fruit / lesions: black or brown
Fruit / premature drop
Seeds / discolorations
Seeds / frass visible
Seeds / internal feeding

Biology and Ecology

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Genetics

There are no data on population genetics, but the species has been sequenced for the DNA barcode gene (cytochrome oxidase subunit I) (Barcode of Life Database, Biodiversity Institute of Ontario, University of Guelph). BOLD includes nine barcode sequences greater than 630 base pairs (BIN AAA4028), all from Costa Rica. The average distance among specimens is 0.22%, and the distance to the nearest neighbor is 1.44%. The DNA barcode appears to be a reliable character for the identification of all life stages.

Reproductive Biology ​

Garcia (1998) concluded that females show a preference for oviposition at a height between 1 and 2 m above the ground. On citrus, eggs are laid on mature fruit; however, green fruits are attacked when populations of the pest are high (Parra et al., 2004). On macadamia, eggs are laid individually on immature nuts that are 8-20 mm in diameter, usually within 3 m of the ground, where nut production is highest (Blanco-Metzler, 1994). Usually a single egg is laid, but sometimes two to four eggs may be oviposited per nut or fruit (Blanco-Metzler, 1994). Eggs hatch in 5 to 6 days (Blanco-Metzler, 1994). Over their lifetime, females lay an average of 37 eggs (Blanco-Metzler, 1994).

After eclosion, first-instar larvae require an average of 3 hours and 40 minutes (range 2-7 hours) to penetrate into the fruit (Carvalho, 2003). Carvalho (2003) observed that after 48 hours, about 50% of first instars reach the pulp, and mortality at this stage can be as high as 32%. Mortality may be associated with fruit pH (Parra et al., 2001).

In macadamia, there is typically one larva per nut, but under outbreak conditions, multiple larvae may be found per nut, usually of different instars (Blanco-Metzler, 1994). There are four to five larval instars (Blanco-Metzler, 1994; Pereira, 2008). When there are four, instars 1 through 3 require 3-4 days for development and instar 4 requires 3-9 days (Blanco-Metzler, 1994). When ready to pupate, larvae exit the fruit by lowering themselves to the ground on a silken thread or by crawling down tree branches and/or the trunk (Blanco-Metzler, 1994). On the ground they make a cocoon of silk, frass and soil (Blanco-Metzler, 1994). Although pupae are usually found in the soil (Cabrera-Asencio et al., 2013), they may be present in fruit as well.

In Costa Rica, G. aurantianum has been collected in all months of the year (Adamski and Brown, 2001). At low elevation sites it has a short lifecycle and may produce up to 10 generations a year (Blanco-Metzler, 1994). Under laboratory conditions, adult moths lived 16 days (Blanco-Metzler, 1994). In Brazil, most moths mate on the third and fourth nights after emergence (Bento et al., 2001a). On a daily basis, there are two peaks of moth activity, one at dawn and one at dusk (Bento et al., 2001a). Adults typically sit on leaves in the lower and middle crowns of citrus trees during the hottest times of day (Bento et al., 2001a, b), moving to the upper crowns of the tree in the evening. Nearly all mating occurs between 18:00-21:00 in the upper crown of citrus trees, with a peak (64%) between 19:00 and 20:00. Mating lasts an average of 1 hour and 40 minutes. From 20:00 there is a resting period until dawn, at which time there is another period of activity (Bento et al., 2001a, b). G. aurantianum males were captured in traps baited either with virgin females or female extracts, suggesting that courtship and mating is mediated by long-range sex pheromones. At close distance (1-2 cm), males and females display a short-range communication behaviour, with males exposing hair-pencils and vibrating their wings.

Environmental Requirements​

Temperature and relative humidity play an important role in G. aurantianum longevity and fecundity (Parra et al., 2004). Garcia (1998) found that the number of generations annually in the State of São Paulo varied as follows: 7.1 generations in Limeira; 8.3 in Barretos; 7.2 in Araraquara; 7.3 in Bebedouro; and 8.2 in São José do Rio Preto. During dry periods, females do not lay eggs and adults have a shorter life span (Parra et al., 2004). Soil moisture may be important as well, because most larvae (i.e., 78%) pupate in the soil. Saturated soils are unfavourable for adult emergence and dry soils may induce desiccation, hence soils with an intermediate moisture are considered most suitable (Parra et al., 2004). Although different varieties of citrus are attacked at different levels, G. aurantianum may be encountered on all varieties of Citrus.

Climate

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ClimateStatusDescriptionRemark
A - Tropical/Megathermal climate Preferred Average temp. of coolest month > 18°C, > 1500mm precipitation annually
Af - Tropical rainforest climate Preferred > 60mm precipitation per month
Aw - Tropical wet and dry savanna climate Tolerated < 60mm precipitation driest month (in winter) and < (100 - [total annual precipitation{mm}/25])

Latitude/Altitude Ranges

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Latitude North (°N)Latitude South (°S)Altitude Lower (m)Altitude Upper (m)
25 40

Air Temperature

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Parameter Lower limit Upper limit
Mean annual temperature (ºC) 10 40

Natural enemies

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Natural enemyTypeLife stagesSpecificityReferencesBiological control inBiological control on
Ascogaster Parasite Larvae not specific Brazil Citrus
Macrocentrus delicatus Parasite Larvae not specific Brazil Citrus
Microgastrinae Parasite Larvae not specific Brazil Citrus
Pristomerus Parasite Larvae not specific Brazil Citrus
Trichogramma atopovirilia Parasite Eggs not specific Brazil Citrus

Notes on Natural Enemies

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According to Garcia et al. (1998), parasitism by the braconid Hymenochaonia delicata (Hymenoptera: Braconidae) has been shown to reach 56.4% at certain times of the year. Parra et al. (2004) reported that H. delicata was of the most frequently-encountered parasitoid of G. aurantianum, parasitizing third instar larvae. The adult parasitoid subsequently emerges from the pest’s pupa.

During a three-year study, Blanco-Metzler et al. (2009) recovered one egg parasitoid belonging to Trichogrammatidae and four larval parasitoids: Microgastrine I, Microgastrine II, Ascogaster sp. (Hymenoptera: Braconidae) and Pristomerus sp. (Hymenoptera: Ichneumonidae). They reported parasitism of larvae by Microgastrine I was 15% in 1991, 16% in 1992 and 4% in 1993; Microgastrine II was not collected in 1991, but accounted for a 4.3% of parasitized larvae in 1992 and 3.7% in 1993; and Ascogaster sp. accounted for 3% parasitism in 1992 and 29% in 1993. Blanco-Metzler et al. (2009) found an inverse relationship between total parasitism and the mean number of damaged nuts; hence, parasitoids are assumed to play an important role in the reduction of the G. aurantianum populations. Torres et al. (2008) studied the performance of egg parasitoid Trichogramma atopovirilia (Hymenoptera: Trichogrammatidae) in the laboratory, and observed that highest parasitism of G. aurantianum eggs occurred at about 25˚C.

Means of Movement and Dispersal

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Adult moths can fly, but are thought to be poor fliers. The most likely mode of dispersal over long distances is the movement of infested fruits. Evidence of this includes interception records at ports-of-entry in the USA and Spain. G. aurantianum is not known to vector any pathogens or associated organisms; however, secondary infection from bacteria, fungi and other insects can occur following damage to fruit (White, 1993).

Pathway Causes

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CauseNotesLong DistanceLocalReferences
Crop productionThe most likely mode of dispersal is in the movement of fruit, either in baggage or commodity consignments Yes Yes PestID, 2018

Pathway Vectors

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VectorNotesLong DistanceLocalReferences
Bulk freight or cargoLarvae in fruit Yes PestID, 2018
ConsumablesLarvae in fruit Yes PestID, 2018

Plant Trade

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Plant parts liable to carry the pest in trade/transportPest stagesBorne internallyBorne externallyVisibility of pest or symptoms
Fruits (inc. pods) larvae Yes Pest or symptoms usually visible to the naked eye
Growing medium accompanying plants pupae Yes Pest or symptoms usually visible to the naked eye
Seedlings/Micropropagated plants pupae 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
Leaves
Roots
Stems (above ground)/Shoots/Trunks/Branches
True seeds (inc. grain)
Wood

Wood Packaging

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Wood Packaging not known to carry the pest in trade/transport
Loose wood packing material
Processed or treated wood
Solid wood packing material with bark
Solid wood packing material without bark

Impact Summary

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CategoryImpact
Economic/livelihood Negative

Impact

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The primary impact of G. aurantianum is the economic burden to farmers, which includes the loss of crops, a reduction in yield and the cost of its control. In the 1990s, the pest resulted in the loss of about $50 million per year in citrus production in the State of São Paulo, Brazil (Anonymous, 2000).

Because the species is native to Brazil where the greatest damage is documented, it is unlikely that it has a significantly adverse effect on native habitats and associated biodiversity, where the species apparently has been recruited from native hosts to cultivated crops. However, there are no data to support or refute this speculation. 

Risk and Impact Factors

Top of page Invasiveness
  • Invasive in its native range
  • Has a broad native range
  • Abundant in its native range
  • Is a habitat generalist
  • Benefits from human association (i.e. it is a human commensal)
Impact outcomes
  • Host damage
  • Negatively impacts agriculture
  • Negatively impacts livelihoods
  • Negatively impacts trade/international relations
Likelihood of entry/control
  • Highly likely to be transported internationally accidentally
  • Difficult/costly to control

Uses

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At present, G. aurantianum is not known to provide economic, social, or ecosystem benefits. However, as a native herbivore, it likely plays a role in local food webs in many neotropical environments.

Detection and Inspection

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Prior to the synthesis of the sex pheromone for detection and monitoring of G. aurantianum, the threshold for the application of chemical control was visual inspection revealing 2-10% of fruits showing damage. The shortcomings of this method are that by the time the decision is made to the apply control measures, the fruit is already irreparably compromised, and larvae inside of fruits are not affected by the control measures and become a source of re-infestation.

In 2001, Leal et al. identified the sex pheromone of G. aurantianum using gas chromatography coupled to an electroantennographic detector (GC-EAD). The major component was found to be (E)-8-dodecenyl acetate (E8-12:Ac) and a second a related alcohol, (E)-8-dodecenol (E8-12:OH). Field tests showed that captures of males in traps baited with a mixture of E8-12:Ac and E8-12:OH at 100:1 and 10:1 ratios were not significantly different from trap catches using two virgin females.

Using the pheromone developed by Leal et al. (2001), Bento et al. (2001b) proposed a system for monitoring G. aurantianum using sticky, delta-type traps with a pellet impregnated with the pheromone to attract males. They recommended that one trap should be placed in the upper portion of a citrus tree canopy every 10 hectares and should be evaluated weekly. Bento et al. (2001b) indicate that chemical/biological products should be applied when the number of males per trap is greater than 4 individuals per week. Preliminary assays in different regions of southern Brazil have shown that the use of pheromone traps has facilitated control in citrus orchards by helping identify the most effective time to apply insecticides and minimize their adverse effect on populations of natural enemies (Bento et al., 2004, 2016).

Parra et al. (2004) provide a summary of efforts from 1995 to 2000 to synthesize the sex pheromone of G. aurantianum. Their review discusses the development of an artificial diet (Garcia and Parra, 1999) for the insect, the study of its temperature and humidity requirements, behavioral studies and the synthesis of the pheromone up to its formulation and distribution to growers. At a cost of about $50K, involving inter- and multidisciplinary research, an IPM strategy was developed that may be adopted for other insect pests in Brazil.

Similarities to Other Species/Conditions

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In size, shape and forewing pattern, adults of G. aurantianum are similar to several species in the genus, all of which are confined to the New World and likely have similar biologies (e.g., Fennah, 1942). However, males of G. aurantianum are distinguished by the unusual shallow notch in the subbasal portion of the antenna (see ‘Description’ section). Males of the similar appearing genus Cryptaspasma are usually slightly larger and have entirely different genitalia. Females may require dissection of the genitalia and comparison with illustrations for accurate identification.

The larvae of Gymnandrosoma lack an anal fork (at the end of the abdomen), a trait shared with members of a few related genera (e.g., Ecdytolopha, Cryptophlebia). The presence of an anal fork is usually considered a diagnostic feature of tortricid larvae. This structure is lost secondarily in a few genera with internal-feeding larvae. So, for example, the larvae of Gymnandrosoma are easily distinguished from those of the related genus Grapholita, many species of which are also internal feeders in fruit, by the absence of an anal fork, as Grapholita spp. always have an anal fork.

The larvae of Gymnandrosoma also share with Ecdytolopha and Cryptophlebia an expanded L-pinaculum on the prothorax that extends beneath the spiracle, and comparatively large pinacula on the abdomen, some of which may have a narrow notch (rarely on all pinacula).

In the case of larvae intercepted on commodities, the origin of the consignment may provide the best means of separating Gymnandrosma from Cryptophlebia – the former is restricted to the New World tropics, while the latter is found mainly in the Old World tropics, especially Africa and Asia.

Prevention and Control

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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.

According to Parra et al. (2004), the indiscriminate application of insecticides in citrus orchards during the 1980s, in particular the use of pyrethroids sprayed using a hot fogging system, contributed to a reduction, and in some cases the elimination, of natural enemies. The result was an increase in populations of citrus pests, especially G. aurantianum. In the absence of pesticide applications, larval parasitism by the braconid Hymenochaonia delicata and egg parasitism by Trichogramma are much more effective at controlling pest populations. Although recent management advancements have been proposed to help maintain effective levels of parasitoids (e.g., Garcia, 1998; Molina, 2003), inappropriate application of agrochemicals persists.

Faria (1997) tested gamma radiation for use in quarantine situations against G. aurantianum and concluded that doses of over 200 Gy inhibited the emergence of viable adults. Doses of up to 500 Gy did not adversely affect the weight of mature oranges or the duration that they could be stored without loss of quality. However, irradiation of green fruit resulted in decreased fruit weight.

Gaps in Knowledge/Research Needs

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Citrus-growing regions of the world outside of the New world tropics appear to be the most vulnerable to the potential invasion of G. aurantianum. Some of these regions have Mediterranean climates (e.g., Spain), with long, dry summers. Hence, additional studies on the ability of G. aurantianum pupae to tolerate long periods of dry soil may shed additional light on the ability of the species to persist if inadvertently introduced into Mediterranean regions. For example, although the warm, humid climate of southern Florida may be compatible with long-term viability of G. aurantianum populations, the long, hot, dry summers of the Central Valley of California may represent conditions under which the pest may not survive.

The cold storage of fruit has been shown to effectively reduce the viability of pupae or larvae in fruit that is in transit. Hence, it may be worth investigating whether the global movement of citrus in cold storage could diminish the potential of introduction of viable individuals at the final destination of citrus commodities.

References

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Parra, J. R. P., Bento, J. M. S., Garcia, M. S., Yamamoto, P. T., Vilela, E. F., Leal, W. S., 2004. Development of a control alternative for the citrus fruit borer, Ecdytolopha aurantiana (Lepidoptera, Tortricidae): from basic research to the grower. Revista Brasileira de Entomologia, 48(4), 561-567. http://www.scielo.br/rbent doi: 10.1590/S0085-56262004000400020

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White, G. L., 1993. Outbreak of Ecdytolopha aurantianum (Lima) on citrus in Trinidad. FAO Plant Protection Bulletin, 41(2), 130-132.

White, G. L., 1999. Sapindus saponaria L. (Sapindaceae), a new host of Ecdytolopha aurantianum (Lima) (Lepidoptera: Tortricidae: Olethreutinae). International Journal of Pest Management, 45(4), 287-291. doi: 10.1080/096708799227699

Distribution References

Adamski D, Brown JW, 2001. Systematic revision of the Ecdytolopha group of genera (Lepidoptera: Tortricidae: Grapholitini) in the New World. Entomologica Scandinavica Supplement. 1-86.

Da Costa Lima A, 1927. Microlépidoptére nouveau dont la chenille devaste les Grangers du District Federal (Brésil). Compte rendu des seances de la Societe de biologie. 97 (25), 835-837 pp.

Escalante JA, Del Castillo M , Ochoa O, 1981. (Catalogo preliminar de las plagas insectiles de papa, maiz y frutales en el departamento del Cusco, Peru). Revista Peruana de Entomologia. 24 (1), 87-90.

Fennah R G, 1942. The " Orange Moth " of Dominica, B.W.I. Tropical Agriculture. 19 (4), 73-78 pp.

Noboa M, Medina L, Viera W, 2018. First Report of Gymnandrosoma aurantianum (Lepidoptera: Tortricidae) in mandarin (Citrus reticulata) in the Inter-Andean Valleys of Ecuador. Florida Entomologist. 101 (4), 699-701.

Vianna UR, 2015. Capítulo 2, Bicho-Furão. In: Pragas emergentes no Estado do Espírito Santo, 1a edição, [ed. by Alegre ES]. Vitória, Brazil: Universidade Federal do Espírito Santo.

White G L, 1993. Outbreak of Ecdytolopha aurantianum (Lima) on citrus in Trinidad. FAO Plant Protection Bulletin. 41 (2), 130-132.

Contributors

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03/07/2019 Original text by:

John W. Brown, Department of Entomology, National Museum of Natural History, Smithsonian Institution, Washington, DC, USA

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