Invasive Species Compendium

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Datasheet

Leptocybe invasa
(blue gum chalcid)

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Datasheet

Leptocybe invasa (blue gum chalcid)

Summary

  • Last modified
  • 21 November 2018
  • Datasheet Type(s)
  • Invasive Species
  • Pest
  • Preferred Scientific Name
  • Leptocybe invasa
  • Preferred Common Name
  • blue gum chalcid
  • Taxonomic Tree
  • Domain: Eukaryota
  •   Kingdom: Metazoa
  •     Phylum: Arthropoda
  •       Subphylum: Uniramia
  •         Class: Insecta
  • Summary of Invasiveness
  • Leptocybe invasa is believed to be native to Australia or to the native range of its host plants Eucalyptus - Australia, New Guinea, Indonesia and Philippines -, although it has only been detected in A...

  • Principal Source
  • Draft datasheet under review

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Pictures

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PictureTitleCaptionCopyright
Leptocybe invasa (blue gum chalcid): female.
TitleFemale
CaptionLeptocybe invasa (blue gum chalcid): female.
Copyright©Francesco Nugnes
Leptocybe invasa (blue gum chalcid): female.
FemaleLeptocybe invasa (blue gum chalcid): female.©Francesco Nugnes
Leptocybe invasa (blue gum chalcid): male.
TitleMale
CaptionLeptocybe invasa (blue gum chalcid): male.
Copyright©Francesco Nugnes
Leptocybe invasa (blue gum chalcid): male.
MaleLeptocybe invasa (blue gum chalcid): male.©Francesco Nugnes
Leptocybe invasa (blue gum chalcid); petioles of Eucalyptus sp. with galls. Italy. August 2015.
TitleGalls
CaptionLeptocybe invasa (blue gum chalcid); petioles of Eucalyptus sp. with galls. Italy. August 2015.
Copyright©Francesco Nugnes
Leptocybe invasa (blue gum chalcid); petioles of Eucalyptus sp. with galls. Italy. August 2015.
GallsLeptocybe invasa (blue gum chalcid); petioles of Eucalyptus sp. with galls. Italy. August 2015.©Francesco Nugnes
Leptocybe invasa (blue gum chalcid); young apical stems of Eucalyptus sp. deformed by the presence of the blue gum chalcid galls. Italy. August 2015.
TitleGalls
CaptionLeptocybe invasa (blue gum chalcid); young apical stems of Eucalyptus sp. deformed by the presence of the blue gum chalcid galls. Italy. August 2015.
Copyright©Francesco Nugnes
Leptocybe invasa (blue gum chalcid); young apical stems of Eucalyptus sp. deformed by the presence of the blue gum chalcid galls. Italy. August 2015.
GallsLeptocybe invasa (blue gum chalcid); young apical stems of Eucalyptus sp. deformed by the presence of the blue gum chalcid galls. Italy. August 2015.©Francesco Nugnes
Leptocybe invasa (blue gum chalcid); galls on Eucalyptus. Lesbos, Greece. October 2012.
TitleGalls
CaptionLeptocybe invasa (blue gum chalcid); galls on Eucalyptus. Lesbos, Greece. October 2012.
CopyrightPublic Domain - Released Bj.schoenmakers/via wikipedia - CC0 1.0
Leptocybe invasa (blue gum chalcid); galls on Eucalyptus. Lesbos, Greece. October 2012.
GallsLeptocybe invasa (blue gum chalcid); galls on Eucalyptus. Lesbos, Greece. October 2012.Public Domain - Released Bj.schoenmakers/via wikipedia - CC0 1.0
Leptocybe invasa (blue gum chalcid); leaf of Eucalyptus with mature galls along the midrib. Italy. May 2011.
TitleGalls
CaptionLeptocybe invasa (blue gum chalcid); leaf of Eucalyptus with mature galls along the midrib. Italy. May 2011.
Copyright©Francesco Nugnes
Leptocybe invasa (blue gum chalcid); leaf of Eucalyptus with mature galls along the midrib. Italy. May 2011.
GallsLeptocybe invasa (blue gum chalcid); leaf of Eucalyptus with mature galls along the midrib. Italy. May 2011.©Francesco Nugnes
Leptocybe invasa (blue gum chalcid); close-up of Eucalyptus leaf with mature galls along the midrib. Italy. May 2011.
TitleGalls
CaptionLeptocybe invasa (blue gum chalcid); close-up of Eucalyptus leaf with mature galls along the midrib. Italy. May 2011.
Copyright©Francesco Nugnes
Leptocybe invasa (blue gum chalcid); close-up of Eucalyptus leaf with mature galls along the midrib. Italy. May 2011.
GallsLeptocybe invasa (blue gum chalcid); close-up of Eucalyptus leaf with mature galls along the midrib. Italy. May 2011.©Francesco Nugnes
Leptocybe invasa (blue gum chalcid); leaf-curling caused by the presence of numerous galls on midribs of Eucalyptus sp. Italy. August 2015.
TitleLeaf-curling
CaptionLeptocybe invasa (blue gum chalcid); leaf-curling caused by the presence of numerous galls on midribs of Eucalyptus sp. Italy. August 2015.
Copyright©Francesco Nugnes
Leptocybe invasa (blue gum chalcid); leaf-curling caused by the presence of numerous galls on midribs of Eucalyptus sp. Italy. August 2015.
Leaf-curlingLeptocybe invasa (blue gum chalcid); leaf-curling caused by the presence of numerous galls on midribs of Eucalyptus sp. Italy. August 2015.©Francesco Nugnes
Leptocybe invasa (blue gum chalcid); acute attack on stems of Eucalyptus sp. Italy. March 2014.
TitleGalls
CaptionLeptocybe invasa (blue gum chalcid); acute attack on stems of Eucalyptus sp. Italy. March 2014.
Copyright©Francesco Nugnes
Leptocybe invasa (blue gum chalcid); acute attack on stems of Eucalyptus sp. Italy. March 2014.
GallsLeptocybe invasa (blue gum chalcid); acute attack on stems of Eucalyptus sp. Italy. March 2014.©Francesco Nugnes
Leptocybe invasa (blue gum chalcid); mature gall with exit hole made by emerging adult. Italy. May 2011.
TitleGall
CaptionLeptocybe invasa (blue gum chalcid); mature gall with exit hole made by emerging adult. Italy. May 2011.
Copyright©Francesco Nugnes
Leptocybe invasa (blue gum chalcid); mature gall with exit hole made by emerging adult. Italy. May 2011.
GallLeptocybe invasa (blue gum chalcid); mature gall with exit hole made by emerging adult. Italy. May 2011.©Francesco Nugnes
Leptocybe invasa (blue gum chalcid); natural enemy, the parasitic wasp, Megastigmus viggianii. (Hymenoptera: Torymidae). (a) dorsal view of female;  (b) lateral view of male.  From: (2016). "Parasitoids of the eucalyptus gall wasp Leptocybe invasa (Hymenoptera: Eulophidae) in China". Parasite 23: 58. DOI:10.1051/parasite/2016071. ISSN 1776-1042.
TitleNatural enemy
CaptionLeptocybe invasa (blue gum chalcid); natural enemy, the parasitic wasp, Megastigmus viggianii. (Hymenoptera: Torymidae). (a) dorsal view of female; (b) lateral view of male. From: (2016). "Parasitoids of the eucalyptus gall wasp Leptocybe invasa (Hymenoptera: Eulophidae) in China". Parasite 23: 58. DOI:10.1051/parasite/2016071. ISSN 1776-1042.
Copyright©Xia-Lin Zheng, Zong-You Huang, Dan Dong, Chun-Hui Guo, Jun Li, Zhen-De Yang, Xiu-Hao Yang and Wen Lu/via wikipedia - CC BY 4.0
Leptocybe invasa (blue gum chalcid); natural enemy, the parasitic wasp, Megastigmus viggianii. (Hymenoptera: Torymidae). (a) dorsal view of female;  (b) lateral view of male.  From: (2016). "Parasitoids of the eucalyptus gall wasp Leptocybe invasa (Hymenoptera: Eulophidae) in China". Parasite 23: 58. DOI:10.1051/parasite/2016071. ISSN 1776-1042.
Natural enemyLeptocybe invasa (blue gum chalcid); natural enemy, the parasitic wasp, Megastigmus viggianii. (Hymenoptera: Torymidae). (a) dorsal view of female; (b) lateral view of male. From: (2016). "Parasitoids of the eucalyptus gall wasp Leptocybe invasa (Hymenoptera: Eulophidae) in China". Parasite 23: 58. DOI:10.1051/parasite/2016071. ISSN 1776-1042.©Xia-Lin Zheng, Zong-You Huang, Dan Dong, Chun-Hui Guo, Jun Li, Zhen-De Yang, Xiu-Hao Yang and Wen Lu/via wikipedia - CC BY 4.0

Identity

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Preferred Scientific Name

  • Leptocybe invasa Fisher & La Salle, 2004

Preferred Common Name

  • blue gum chalcid

International Common Names

  • English: Eucalyptus gall wasp

Local Common Names

  • Argentina: avispa de la agalla del eucalipto
  • Portugal: vespa da galha

Summary of Invasiveness

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Leptocybe invasa is believed to be native to Australia or to the native range of its host plants Eucalyptus - Australia, New Guinea, Indonesia and Philippines -, although it has only been detected in Australia in Queensland and New South Wales. During the last two decades, L. invasa has spread worldwide, invading all the continents where Eucalyptus has been imported to (Asia, Africa, Europe, South and North America). The invasive potential of L. invasa is very high. Its broad host range, polyvoltinism, overlapping generations, concealed life style (galls) and reproductive modalities allow the pest to quickly spread and exponentially grow from few individuals. L. invasa is considered thelytokous because sex ratio of the most widespread lineage is female biased, but a biparental lineage also exists.

Taxonomic Tree

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  • Domain: Eukaryota
  •     Kingdom: Metazoa
  •         Phylum: Arthropoda
  •             Subphylum: Uniramia
  •                 Class: Insecta
  •                     Order: Hymenoptera
  •                         Family: Eulophidae
  •                             Genus: Leptocybe
  •                                 Species: Leptocybe invasa

Notes on Taxonomy and Nomenclature

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L. invasa was unknown until the early 2000s, when it was recorded in Italy in 2001 as Aprostocetus sp. (Viggiani et al., 2002) and in Turkey (Aytar, 2003). Simultaneously, severe damages to eucalypt plantations in Israel and consequent economic losses encouraged studies about this unknown eulophid wasp causing galling on eucalypts, which resulted in the first description of L. invasa (Mendel et al., 2004). The original description included only female specimens, because the male was never found, thus the species was considered thelytokous. The first male was reported in Turkey in 2004 (Doganlar, 2005). To date, the genus Leptocybe includes only the species L. invasa, although recent studies based on molecular and biological evidence have underlined the presence of two lineages behind the morphospecies L. invasa, the first from the Mediterranean region and South America and the other from China (Nugnes et al., 2015).

Description

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Adult:

- Female: body brownish with metallic shine (blue or dark green), 1.1-1.4 mm in length; head brown with mouth margin slightly lighter or yellow; antennae with scape yellow becoming darker in the apex, while funicle and club are brown or light brown; middle and hind coxae brown (as the body), while the fore coxa is yellow. The remaining parts of the legs are yellow, except the last tarsal segments that turn brown apically. Wings hyaline with light brown veins. The original and detailed description is available in Mendel et al. (2004). The female holotype is deposited at the Australian National Insect Collection, CSIRO, Canberra, Australia.
- Male: body length 0.8-1.2 mm; mesosoma brown with metallic shine (blue or dark green); metasoma brown with a very little metallic hint on the dorsal portion. Antennae with scape yellow becoming darker dorsally in the apex and ventral plaque; pedicellus yellow, with the dorsal basal portion darker, funicle and club yellow. Wings hyaline with yellow veins. Original and detailed description is available in Doganlar (2005).

Egg: shiny-white; mature oocyte with a peduncle (Sangtongpraow et al., 2011; Nugnes et al., 2015).

Larvae: preliminary studies supposed that L. invasa preimaginal development consisted of a single larval instar, whitish, spherical and with a body diameter ranging from 0.1 to 0.5 mm, without visible segmentation and spiracles (De Marzo, 2014). However, successive studies confirmed the presence of a globular young larva, totally immersed in the liquid material contained in the gall (Viggiani, 2015), but recorded and described as a mature larva also. The whitish mature larva looks hymenopteriform (Dittrich-Schröder et al., 2014), without visible spiracles; 0.8-1.0 mm in length; the body appears indistinctly segmented with a well-developed head. Presence of sclerotized, triangular mandibles. Inside the gall, mature larvae assume a curved posture due to the small space (Viggiani, 2015). Oviposition and secretions of the larva induce hyperplasy and metaplasy of the leaves and stems tissues, causing the formation of galls (Mendel et al., 2004). Each larva lives in a cavity inside the gall, feeding on growing tissues (Zhu et al., 2012; Kumar et al., 2015).

Distribution

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L. invasa is believed to be native either only to Australia or to the whole native range of its host plants Eucalyptus, i.e. Australia, New Guinea, Indonesia and Philippines (Hill and Johnson, 2000; Nugnes et al., 2015). The species is closely related to its host plants and, in principle, could be found everywhere Eucalyptus is grown. At the moment, it seems to have spread from its native region into Africa, Asia, Europe, South and North America (Nugnes et al., 2015).

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.

Continent/Country/RegionDistributionLast ReportedOriginFirst ReportedInvasiveReferenceNotes

Asia

CambodiaPresentIntroduced Invasive FAO, 2012
ChinaRestricted distributionEPPO, 2014
-FujianPresentIntroduced Invasive Zhang et al., 2012
-GuangdongPresentIntroduced Invasive Tang et al., 2008; EPPO, 2014
-GuangxiPresentIntroduced2007 Invasive Wu et al., 2009; EPPO, 2014
-HainanPresentIntroduced2008 Invasive Tang et al., 2008; EPPO, 2014
-JiangxiPresentIntroducedChen et al., 2015
-SichuanPresentIntroduced Invasive Zheng et al., 2016
IndiaPresentCABI/EPPO, 2007; EPPO, 2014
-Andhra PradeshPresentIntroduced Invasive CABI/EPPO, 2007; Jacob et al., 2007; Narendran, 2007; EPPO, 2014
-DelhiPresent, 2011
-GoaPresentIntroducedKumar et al., 2007
-GujaratPresentIntroducedKumar et al., 2007
-HaryanaPresentIntroducedRamanagouda et al., 2011
-Indian PunjabPresentIntroduced2009 Invasive Sangha et al., 2011
-Jammu and KashmirPresentIntroducedRamanagouda et al., 2011
-KarnatakaPresentIntroduced Invasive CABI/EPPO, 2007; Jhala et al., 2010; Kavitha Kumari et al., 2010; Ramanagouda et al., 2011; EPPO, 2014Noticed in 2001
-KeralaPresentIntroduced2004 Invasive CABI/EPPO, 2007; Jacob et al., 2007; Narendran, 2007; EPPO, 2014
-Madhya PradeshPresentKumar et al., 2007
-MaharashtraPresentKumar et al., 2007
-OdishaPresentIntroduced Invasive Ramanagouda et al., 2011
-Tamil NaduPresentIntroduced Invasive CABI/EPPO, 2007; Jacob et al., 2007; Narendran, 2007; Kavitha Kumari et al., 2010; EPPO, 2014Noticed in 2002
-Uttar PradeshPresentIntroduced2007 Invasive Jacob and Ramesh, 2009
-UttarakhandPresentIntroduced Invasive Ramanagouda et al., 2011
IranPresentIntroduced2005 Invasive Hesami et al., 2005; CABI/EPPO, 2007; EPPO, 2014
IraqPresentIntroduced2010 Invasive Hassan, 2012
IsraelPresentIntroduced2001 Invasive Mendel et al., 2004; CABI/EPPO, 2007; EPPO, 2014
JordanPresentIntroduced2001 Invasive CABI/EPPO, 2007; Wylie and Speight, 2012; EPPO, 2014
LaosPresentIntroduced2008 Invasive Thu et al., 2009; EPPO, 2014
MalaysiaPresentPresent based on regional distribution
-SabahPresentIntroduced2012 Invasive Lawson et al., 2012
Sri LankaPresentIntroduced2010 Invasive Karunaratne et al., 2010
SyriaPresentIntroduced2001 Invasive CABI/EPPO, 2007; Wylie and Speight, 2012; EPPO, 2014
TaiwanPresentIntroduced2010 Invasive Tung and La Salle, 2010
ThailandPresentIntroduced2004 Invasive CABI/EPPO, 2007; Sangtongpraow et al., 2011; EPPO, 2014
TurkeyPresentIntroduced2000 Invasive Aytar, 2003; CABI/EPPO, 2007; EPPO, 2014
VietnamPresentIntroduced2002 Invasive Thu, 2004; CABI/EPPO, 2007; EPPO, 2014

Africa

AlgeriaPresentIntroduced2002 Invasive Mendel et al., 2004; CABI/EPPO, 2007; EPPO, 2014
EgyptPresentIntroduced2001 Invasive Wylie and Speight, 2012
EthiopiaPresentIntroduced2002 Invasive CABI/EPPO, 2007; Giliomee, 2011; EPPO, 2014
KenyaPresentMutitu, 2003; CABI/EPPO, 2007; EPPO, 2014
MalawiPresentIntroduced2008 Invasive FRIM, 2010
MoroccoPresentIntroduced2001 Invasive Mendel et al., 2004; CABI/EPPO, 2007; EPPO, 2014
MozambiquePresentIntroduced Invasive EPPO, 2012; IPPC, 2012; Chirinzane et al., 2014; EPPO, 2014
South AfricaPresentIntroduced2007 Invasive Dittrich-Schröder et al., 2009; EPPO, 2014
TanzaniaPresentIntroduced2005 Invasive Roux, 2005; CABI/EPPO, 2007; EPPO, 2014
TunisiaPresentIntroduced2004 Invasive Dhahri et al., 2010; EPPO, 2014
UgandaPresentIntroduced2002 Invasive CABI/EPPO, 2007; Nyeko et al., 2009; EPPO, 2014
ZimbabwePresentIntroduced2007 Invasive ICFR, 2011; EPPO, 2014

North America

MexicoPresentIntroduced2014 Invasive Vanegas-Rico et al., 2015
USARestricted distributionEPPO, 2014
-FloridaPresentIntroduced2008 Invasive Wiley and Skelley, 2008; EPPO, 2014

South America

ArgentinaPresentIntroduced2009 Invasive Aquino et al., 2011
BrazilPresentEPPO, 2014
-BahiaPresentIntroduced2007 Invasive Costa et al., 2008; EPPO, 2014
-Espirito SantoPresentIntroduced Invasive Pereira et al., 2014
-GoiasPresentIntroduced2011 Invasive Pereira et al., 2014; Pereira et al., 2014
-MaranhaoPresentIntroduced Invasive EPPO, 2014; Pereira et al., 2014
-Mato Grosso do SulPresentIntroduced Invasive Pereira et al., 2014
-Minas GeraisPresentIntroduced Invasive EPPO, 2014; Pereira et al., 2014
-ParanaPresentIntroduced Invasive Pereira et al., 2014; Puretz et al., 2015
-PernambucoPresentIntroduced Invasive Pereira et al., 2014
-Rio Grande do SulPresentIntroduced Invasive Pereira et al., 2014
-Sao PauloPresentIntroduced2007 Invasive Costa et al., 2008; EPPO, 2014
-SergipePresentIntroduced Invasive Rolim et al., 2014
-TocantinsPresentIntroduced Invasive EPPO, 2014; Pereira et al., 2014
ChilePresentIntroduced2010 Invasive Wylie and Speight, 2012; CPF, 2014
ParaguayPresentIntroduced2012 Invasive Benítez Díaz et al., 2014
UruguayPresentIntroduced2013 Invasive Jorge et al., 2016First galls observed in 2011

Europe

FranceRestricted distributionCABI/EPPO, 2007; EPPO, 2014
-CorsicaPresentIntroduced2004 Invasive CABI/EPPO, 2007; Wylie and Speight, 2012; EPPO, 2014
GreecePresentIntroduced2004 Invasive CABI/EPPO, 2007; Wylie and Speight, 2012; Bella, 2014; EPPO, 2014
ItalyPresentIntroduced2000 Invasive Viggiani et al., 2002; CABI/EPPO, 2007; EPPO, 2014As Aprostocetus sp.
MaltaPresentIntroduced2006 Invasive Mifsud, 2012; EPPO, 2014
PortugalPresentBranco et al., 2006; CABI/EPPO, 2007; EPPO, 2014
SpainPresentIntroduced2003 Invasive Sánchez, 2003; Pujade-Villar and Riba-Flinch, 2004; CABI/EPPO, 2007; EPPO, 2014
-Balearic IslandsPresentIntroduced2003 Invasive Sánchez, 2003; EPPO, 2014
UKPresentIntroduced2006 Invasive Wylie and Speight, 2012

Oceania

AustraliaPresentPresent based on regional distribution
-New South WalesPresentNativeDe Souza, 2016
-QueenslandPresentNativeDe Souza, 2016
New ZealandAbsent, invalid recordBain, 2011

History of Introduction and Spread

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It is impossible to define the first country in which L. invasa was found, as the description of this new genus and species has followed first records in Italy, Turkey and the Middle East. However, after the first records, the blue gum chalcid has been found in all continents suitable for eucalypts. The only probable history of spread has been suggested in the African continent, where L. invasa was first detected in Ethiopia in 2002, moving southwards to Kenya, Tanzania and Zimbabwe, reaching South Africa in 2007 (Dittrich-Schröder et al., 2009). Its South American route of invasion has also been reconstructed to Brazil-Argentina-Chile-Paraguay-Uruguay.

Risk of Introduction

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Globalisation and increasing trade promote the spread of the blue gum chalcid via its main pathways of introduction, including trade of nursery plants with leaves and shoots. Difficult detection of both adults and early stages of the galling process does not facilitate early interception of the pest, which can hence be introduced very easily. Furthermore, the species small dimensions can facilitate its local dispersal both by unintentional carriage and via wind currents. Strict quarantine measures can delay species spread, but almost certainly cannot stop invasion in all countries where eucalypts are grown.

Habitat

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In the invaded range, L. invasa is distributed in agricultural, forest and urban areas, and in rangelands where eucalypts are grown. Hence, it can be found in nurseries and in eucalyptus plantations growing as planted forest stands, as ornamental trees, as windbreaks around orchards or in groves growing under irrigation (Mendel et al., 2004; Nyeko, 2005; Protasov et al., 2008; Thu et al., 2009; Karunaratne et al., 2010; Pereira et al., 2014).

Habitat List

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CategorySub-CategoryHabitatPresenceStatus
Terrestrial-managed/Cultivated / agricultural land Present, no further details Harmful (pest or invasive)
Terrestrial-managed/Protected agriculture (e.g. glasshouse production) Present, no further details Harmful (pest or invasive)
Terrestrial-managed/Managed forests, plantations and orchards Present, no further details Harmful (pest or invasive)
Terrestrial-managed/Managed grasslands (grazing systems) Present, no further details Harmful (pest or invasive)
Terrestrial-managed/Disturbed areas Present, no further details Harmful (pest or invasive)
Terrestrial-managed/Rail / roadsides Present, no further details Harmful (pest or invasive)
Terrestrial-managed/Urban / peri-urban areas Present, no further details Harmful (pest or invasive)
Terrestrial-natural/semi-natural/Natural forests Present, no further details Harmful (pest or invasive)
Terrestrial-natural/semi-natural/Natural grasslands Present, no further details Harmful (pest or invasive)
Terrestrial-natural/semi-natural/Riverbanks Present, no further details Harmful (pest or invasive)
Terrestrial-natural/semi-natural/Wetlands Present, no further details Harmful (pest or invasive)
Terrestrial-natural/semi-natural/Deserts Present, no further details Harmful (pest or invasive)
Terrestrial-natural/semi-natural/Arid regions Present, no further details Harmful (pest or invasive)
Littoral/Coastal areas Present, no further details Harmful (pest or invasive)
Littoral/Coastal dunes Present, no further details Harmful (pest or invasive)

Hosts/Species Affected

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The majority of Eucalyptus species have been confirmed to be susceptible to L. invasa (Jorge et al., 2016). Among these, E. camaldulensis (var. camaldulensis and obtusa), E. grandis, E. robusta and E. tereticornis showed remarkably high susceptibility to the blue gum chalcid (Mendel et al., 2004; Thu et al., 2009; Nyeko et al., 2010). Studies carried out on several clonal hybrids or clones of these species showed that the incidence of L. invasa infestation could affect them differently (Nyeko et al., 2010; ICFR, 2011). E. gomphocephala and E. occidentalis did not show susceptibility to L. invasa, while E. erythrocorys exhibited “cork tissue” symptoms some days after deposition, but no further gall formation was observed (Mendel et al., 2004).

To date, the only susceptible species not belonging to the Eucalyptus genus is Corymbia polycarpa (Thu et al., 2009), with other species of this genus (C. citriodora, C. maculata, C. torelliana) apparently being tolerant (Mendel et al., 2004). 

Host Plants and Other Plants Affected

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Plant nameFamilyContext
Corymbia polycarpaMyrtaceaeOther
EucalyptusMyrtaceaeMain
Eucalyptus alba (white gum)MyrtaceaeMain
Eucalyptus botryoides (southern mahogany)MyrtaceaeMain
Eucalyptus bridgesianaMyrtaceaeMain
Eucalyptus camaldulensis (red gum)MyrtaceaeMain
Eucalyptus cinereaMyrtaceaeMain
Eucalyptus cladocalyx (sugar gum)MyrtaceaeMain
Eucalyptus cloeziana (Gympie messmate)MyrtaceaeMain
Eucalyptus coolabahMyrtaceaeMain
Eucalyptus dunnii (Dunn's white gum)MyrtaceaeMain
Eucalyptus exserta (Queensland peppermint)MyrtaceaeMain
Eucalyptus globulus (Tasmanian blue gum)MyrtaceaeMain
Eucalyptus gomphocephala (tuart)MyrtaceaeMain
Eucalyptus grandis (saligna gum)MyrtaceaeMain
Eucalyptus gunnii (cider gum)MyrtaceaeMain
Eucalyptus leucoxylonMyrtaceaeMain
Eucalyptus maidenii (Maiden's gum)MyrtaceaeMain
Eucalyptus microcorys (Tallowwood)MyrtaceaeMain
Eucalyptus moluccanaMyrtaceaeMain
Eucalyptus nicholii (willow-leaved peppermint)MyrtaceaeMain
Eucalyptus nitens (shining gum)MyrtaceaeMain
Eucalyptus pellita (red mahogany)MyrtaceaeMain
Eucalyptus pilularis (blackbutt)MyrtaceaeMain
Eucalyptus propinqua (grey gum)MyrtaceaeMain
Eucalyptus pulverulentaMyrtaceaeMain
Eucalyptus robusta (swamp mahogany)MyrtaceaeMain
Eucalyptus rudisMyrtaceaeMain
Eucalyptus saligna (Sydney blue gum)MyrtaceaeMain
Eucalyptus sideroxylon (black ironbark)MyrtaceaeMain
Eucalyptus smithiiMyrtaceaeMain
Eucalyptus tereticornis (forest red gum)MyrtaceaeMain
Eucalyptus urophylla (Timor mountain gum)MyrtaceaeMain
Eucalyptus viminalis (ribbon eucalyptus)MyrtaceaeMain

Growth Stages

Top of page Seedling stage, Vegetative growing stage

Symptoms

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L. invasa females usually prefer newly developed leaves, where they lay their eggs in the midribs, petioles and parenchyma tissue of twigs. Usually eggs are laid in a lined group at a distance of 0.3-0.5 mm of each other (Mendel et al., 2004; Shylesha, 2008). After hatching, the larva remains in a tissue cavity and its growth and gall development take place simultaneously. Gall development consists of five stages, described in Mendel et al. (2004):

- First stage: at the deposition site, a little spot of dead cells (epidermic and sub-epidermic), similar to a cork tissue, becomes evident, without any initial gall-shaped formation (Jacob and Ramesh, 2009; Kumar et al., 2015). A change in colour from green to pink or reddish usually occurs to the cells of midribs containing the eggs, and the spherical shape of the gall starts to be visible at the end of the stage, usually 1-2 weeks after deposition (Mendel et al., 2004; Jacob and Ramesh, 2009).
- Second stage: in the following days galls reach their maximum size and attain the typical green bump-shape (Jacob and Ramesh, 2009; Kavitha Kumari et al., 2010; Eyidozehi et al., 2014).
- Third stage: galls start to lose their green colour, turning into a glossy reddish colour (ICFR, 2011).
- Fourth stage: galls lose their glossiness, turning into dull pink/dark red (Kavitha Kumari et al., 2010).
- Fifth stage: corresponds to adult emergence, with exit holes visible on the galls surface. Gall colours turn to light brown on the leaf or red-brown on the stems.

Gall formation on leaf petioles, midribs and young twigs usually results in leaf shape deformation. Heavy infestations can firstly cause leaf deformation, due to curling of the midribs, premature aging and leaf fall (Nugnes et al., 2015), and eventually stunted growth of the tree (Mendel et al., 2004; Eyidozehi et al., 2014). Heavy infestation can seriously damage young plantations and nursery seedlings, although tree mortality has not been observed to date (EPPO, 2006).

List of Symptoms/Signs

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SignLife StagesType
Leaves / abnormal colours
Leaves / abnormal forms
Leaves / abnormal leaf fall
Leaves / leaves rolled or folded
Leaves / wilting
Leaves / yellowed or dead
Stems / distortion
Stems / galls
Stems / stunting or rosetting

Biology and Ecology

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Detailed information on the biology of L. invasa in different environments and hosts is available in many different publications (Mendel et al., 2004; Kavitha Kumari et al., 2010; Sangtongpraow et al., 2011; Eyidozehi et al., 2014; Udagedara and Karunaratne, 2014; Zhu et al., 2015).

Genetics

Few studies have been carried out on the genetic characterisation of L. invasa. Nugnes et al. (2015) found that L. invasa is represented by at least two genetically and biologically distinct lineages: a Chinese lineage present in East Asia and characterized by biparental populations, and a Western lineage (in Italy, Tunisia, Turkey and Argentina) that reproduces by thelytokous parthenogenesis. Each lineage was found to be infested by a respective endosymbiotic Rickettsia which, at least for the Western lineage, is considered responsible for the thelytoky (Nugnes et al., 2015).

Reproductive Biology

Studies on potential fecundity of L. invasa highlight that an increase in size can increase potential fecundity. Indeed, ovaries of small females contained an average of 90 eggs (range of 39-140), in contrast with large females that reached an average of 210 eggs (range of 141-298). As such, potential fecundity of the blue gum chalcid is, in average, 160 eggs/female (Sangtongpraow et al., 2011). Number of eggs is correlated with environmental temperature, with an increase in number of eggs per female being directly proportional to an increase in temperature from 20 to 29°C. Number of eggs/female was the highest at 29°C, with a sharp decrease at 32°C (Zhu et al., 2015).

Generally, realized fecundity is determined taking into account the number of eggs laid on/in a host over the life time of a female. L. invasa females lay eggs in lined groups, at a distance of about 0.3-0.5 mm of each other, in the midribs or petioles of young leaves of eucalyptus (about 0.5-5 cm in length). Due to this oviposition behaviour, it is difficult to detect the real number of eggs laid. Hence, to determine L. invasa’s realized fecundity, the number of emerging progenies over the life time of a female was taken into account (Sangtongpraow et al., 2011).

Dissections of newly emerging females of the blue gum chalcid showed the presence of mature eggs in ovaries, indicating L. invasa to be a pro-ovigenic species (Sangtongpraow et al., 2011; Nugnes et al., 2015). Soon after their emergence females start to lay eggs in host tissues, with a trend for these numbers to decrease with time. Indeed, during the first day, a female could lay about 30 eggs, whereas this number gradually declines, reaching 0.2 eggs/female on the sixth day (Sangtongpraow et al., 2011).

Physiology and Phenology

L. invasa develops two or three overlapping generations per year in most countries where it occurs, depending on the ecological conditions (Mendel et al., 2004), although in Guangxi, China, the species can complete five or six overlapping generations per year (Wu et al., 2009).

Mean development time from eggs to adults has been recorded to last about 138 days in the field (Hesami et al., 2005). In greenhouse, average development time varies greatly according to different studies: 132 days (Mendel et al., 2004), 126 days (Hesami et al., 2005), 60 days (Kavitha Kumari et al., 2010) or 46 days (Sangtongpraow et al., 2011). Duration of each life stage has been estimated as about 11 days for the egg stage, 19 and 30 days for the young and mature larval stages, respectively, and 38 days for the pupal stage. However, temperature affects development time of L. invasa, with development time decreasing linearly as temperature increases (Zhu et al., 2015). The temperature that allowed the shortest development time from egg to adult was 29°C, likely the species optimum developmental temperature. Temperature is also positively correlated to survival rate of the immature stage, with the highest percentage survival at 29°C, and a sudden decrease in survival at 32°C (Zhu et al., 2015). Tests carried out in 2011 in Guangdong, China, reported very low thresholds (0°C) for the development of several stages of the blue gum chalcid (egg, larval, pupal and adult stages). Furthermore, different requirements were estimated for cumulative temperatures (degree-days) of each life stage: 146.6 (eggs), 1228 (larvae), 161.7 (pupae) and 205.2 (adults) (Qiu et al., 2011). The developmental zero temperature (DZT) for the complete life cycle (egg-adult) of L. invasa in Dongfang (Hainan Island, China) was estimated to be about 19°C, while DZTs of egg, larval and pupal stages were 13, 19.7 and 17 °C, respectively. The same study calculated the cumulative temperatures needed for each life stage as 128°C for eggs, 284°C for larvae and 201°C for pupae, totalising a cumulative temperature of 563°C needed for the development period from egg to adult (Zhu et al., 2015).

Longevity

Adult longevity tests have been performed in climatic chamber (at 25°C and 80% relative humidity) under different feed treatments (Mendel et al., 2004; Sangtongpraow et al., 2011). Adult females of L. invasa fed with honey solution (honey:water, 1:1) showed the longest mean life span (6-8 days). Adults lived for 2-5 days if fed with fresh flowers of the host plant (E. camaldulensis), from 1.5 to 3.7 days if fed only with distilled water and 3.5 days if only young fresh foliage of the host plant was available. A diet made up of a combination of fresh foliage and honey solution did not extend life span over the 6 days observed for the “honey solution diet”. Adults with no food and no water lived for about 1.33 days. Male longevity was shorter than for females, with males exposed to the same food sources surviving for 5-6 days (honey solution), 1.22 days (flowers), 1.11 days (water), 1.56 days (water+flowers), 5.22 days (honey solution+flowers) and 1 day (no food and no water) (Sangtongpraow et al., 2011).

Temperature also influences adult longevity, with female longevity being the highest between 23 and 29°C (about 8-9 days), and just 5.8 days at 32°C. Male longevity reached the highest values of 12-13 days at 20 and 23°C and a proportional decline was observed with an increase in temperature, reaching 6 days at 32°C (Zhu et al., 2015).

Activity Patterns

In the field, L. invasa adults are active throughout the day, although their activity increases in sunny hours.

Population Size and Structure

Gall density can vary with tree age: in nursery seedlings and coppice, density was 36.99 galls/10 cm shoot, while on grown-up trees the average number of galls for a shoot of 10 cm only reached about 16 galls (Kavitha Kumari et al., 2010; Kulkarni, 2010). Furthermore, density of galls in different tissues is correlated to the Eucalyptus species host. Studies revealed that E. urophylla x E. camaldulensis hybrids showed a higher density of galls on midribs and twigs, while E. exserta had more galls on petioles (Zhu et al., 2012).

L. invasa populations exhibit different sex ratios in different areas. Males have never been recorded in Europe, Africa, Laos, Malaysia, Sri Lanka, Vietnam, Florida (USA), Argentina, Chile, Mexico, Paraguay and Australia (Nugnes et al., 2015), which might indicate that, in these countries, the species reproduces by thelytoky. The role of symbionts as being responsible for thelytoky has been supported by several facts: complete female-biased sex ratio, high-density localisation within the ovaries, and vertical transmission of a Rickettsia endosymbiont to the offspring (Nugnes et al., 2015). The presence of males has been recorded in India (Karnataka), Turkey, Thailand, Brazil and China (Doganlar, 2005; Chen et al., 2009; Gupta and Poorani, 2009; Kavitha Kumari et al., 2010; Liang et al., 2010; Tung and La Salle, 2010; Zheng et al., 2014; Sangtongpraow et al., 2011; De Souza, 2016). Particularly in China, male proportion ranged from 18 to 48% in some populations (Liang et al., 2010) although, in others, males only occurred occasionally (Zhu et al., 2015). Genetic characterisation of both the insect and the endosymbiotic Rickettsia corresponds to the different geographic sex ratios recorded in populations from China and Mediterranean and South American regions (Nugnes et al., 2015). Furthermore, the presence of males does not always correspond to sexual reproduction, with unmated females from Chinese and Thai populations having offspring of both sexes (Sangtongpraow et al., 2011).

Associations

L. invasa populations have been associated with the endosymbiotic bacteria Rickettsia (Nugnes et al., 2015). In samples from the Mediterranean region and South America, Rickettsia causes parthenogenetic reproduction, resulting in a female biased sex ratio. The association Leptocybe-Rickettsia improves the biotic potential of the infected populations because the whole progeny is feminine, hence potentially doubling the intrinsic rate of population increase.

Environmental Requirements

L. invasa has substantial environmental plasticity, being able to live where the host trees are present, under different climatic conditions. However, some studies have demonstrated a negative correlation between altitude and L. invasa attack to Eucalyptus spp. (Nyeko et al., 2009), with no attack having been observed on trees in plantations at altitudes higher than 1938 m above sea level.

L. invasa shows tolerance to low temperatures, with pupae having higher tolerance than larvae and adults. Indeed, the supercooling points of larvae, pupae and adults were about -25.5, -25 and -21°C respectively, while the freezing points of the same stages were about -24, -23 and -17.5°C, respectively. Male adults showed more resistance than females to lower temperatures (Han et al., 2012).

Climate

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ClimateStatusDescriptionRemark
Af - Tropical rainforest climate Preferred > 60mm precipitation per month
Am - Tropical monsoon climate Preferred Tropical monsoon climate ( < 60mm precipitation driest month but > (100 - [total annual precipitation(mm}/25]))
As - Tropical savanna climate with dry summer Preferred < 60mm precipitation driest month (in summer) and < (100 - [total annual precipitation{mm}/25])
Aw - Tropical wet and dry savanna climate Preferred < 60mm precipitation driest month (in winter) and < (100 - [total annual precipitation{mm}/25])
BS - Steppe climate Preferred > 430mm and < 860mm annual precipitation
BW - Desert climate Preferred < 430mm annual precipitation
Cs - Warm temperate climate with dry summer Preferred Warm average temp. > 10°C, Cold average temp. > 0°C, dry summers
Cw - Warm temperate climate with dry winter Preferred Warm temperate climate with dry winter (Warm average temp. > 10°C, Cold average temp. > 0°C, dry winters)
Cf - Warm temperate climate, wet all year Preferred Warm average temp. > 10°C, Cold average temp. > 0°C, wet all year

Latitude/Altitude Ranges

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Latitude North (°N)Latitude South (°S)Altitude Lower (m)Altitude Upper (m)
63 46

Natural enemies

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Natural enemyTypeLife stagesSpecificityReferencesBiological control inBiological control on
Aprostocetus Parasite not specific
Aprostocetus gala Parasite not specific
Megastigmus Parasite not specific
Megastigmus brasiliensis Parasite not specific
Megastigmus dharwadicus Parasite not specific
Megastigmus leptocybus Parasite not specific
Megastigmus thitipornae Parasite not specific
Megastigmus viggianii Parasite not specific
Megastigmus zebrinus Parasite not specific
Megastigmus zvimendeli Parasite not specific
Quadrastichus mendeli Parasite to species Israel, Kenya, South Africa, India
Selitrichodes krycery Parasite not specific Israel, South Africa, India
Selitrichodes neseri Parasite not specific Kelly et al., 2012 South Africa, Brazil
Telenomus Parasite not specific

Notes on Natural Enemies

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In the native range, natural enemies play a very important role in limiting populations of L. invasa, such that the species does not threaten either wild Eucalyptus or plantations. Surveys carried out in the native area have highlighted the potential of the species Quadrastichus mendeli, Selitrichodes kryceri and S. neseri (Eulophidae, Tetrastichinae) (Kim et al., 2008; Kelly et al., 2012).
In areas invaded by L. invasa, many studies have been carried out looking for natural enemies of the species. Native Megastigmus spp. (Torymidae) have been reared in South America (Argentina and Brazil), the Mediterranean area (Israel, Italy and Turkey), Africa (South Africa) and Asia (India, Sri Lanka and Thailand) (Viggiani et al., 2002; Protasov et al., 2008; Vastrad et al., 2009; Doganlar and Hassan, 2010Zaché et al., 2012; Doganlar et al., 2013; Sangtongpraow and Charernsom, 2013; Udagedara and Karunaratne, 2014; Doganlar, 2015; Nugnes et al., 2016; Zheng et al., 2016). Furthermore, Aprostocetus sp. and Aprostocetus causalis (Eulophidae, Tetrastichinae), Parallelaptera sp. [Erythmelus sp.] (Mymaridae) and Telenomus sp. (Platygasteridae) have also been identified in India (Vastrad et al., 2009).

Means of Movement and Dispersal

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Natural Dispersal

L. invasa can spread by adult flight in small areas, but its movements can be strongly supported by wind currents.

Intentional Introduction

Human influence, via national and international trade and transport, is the most important factor responsible for L. invasa spread all over the world. In particular, spread to new countries occurs by introduction of infested seedlings or plants of Eucalyptus spp., which are widely planted commercially all around the world due to forestry or habitat restoration and improvement (to control soil erosion and as windbreaks). Furthermore, their role as source for fuelwood, pulpwood and medicinal eucalyptus oil is still increasing (Eldridge et al., 1994; Doughty, 2000).

Pathway Causes

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CauseNotesLong DistanceLocalReferences
Acclimatization societies Yes Yes
Botanical gardens and zoos Yes Yes
Breeding and propagation Yes Yes
Cut flower trade Yes Yes
Forestry Yes Yes
Habitat restoration and improvementThrough the use of eucalyptus (especially in coastal dunes) Yes Yes
Hedges and windbreaksThrough the use of eucalyptus as windbreaks Yes Yes
HitchhikerSmall L. invasa adults or movement of leaves with galls (e.g. leaves stuck outside the windscreen of a vehicle) Yes
Landscape improvement Yes Yes
Nursery tradeThe most relevant pathway Yes Yes
Ornamental purposes Yes Yes

Pathway Vectors

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VectorNotesLong DistanceLocalReferences
Bulk freight or cargoPotential transport in refrigerated containers that, due to the low temperature, could extend the life period of blue gum chalcid Yes Yes
Clothing, footwear and possessions Yes
Containers and packaging - non-woodThe small dimension of the pest could help its spread as a hitchhiker, especially in refrigerated containers Yes Yes
Plants or parts of plants Yes Yes
Land vehicles Yes
Wind Yes

Economic Impact

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L. invasa has been considered a pest in eucalypt plantations outside its native range, due to the absence of natural enemies. The impact of L. invasa is exacerbated by both its biological characteristics (overlapping generations, parthenogenetic reproduction) and its wide range of hosts. In the introduced areas, gall formation caused by L. invasa can have a major impact on eucalypt seedlings in nurseries, causing severe injury to young foliage and inducing gall formation mainly on rapid growing shoots (Sambaraju et al., 2015). Severe outbreaks of L. invasa have also occurred on mature plants of eucalypt plantations (Mendel et al., 2004; Jacob et al., 2007; 2009).

Heavy infestations of L. invasa can firstly cause leaf deformation, premature aging and leaf fall, and eventually stunted growth of Eucalyptus trees (Mendel et al., 2004; Eyidozehi et al., 2014; Nugnes et al., 2015). In fact, L. invasa has a highly negative impact on Eucalyptus plant growth, with a marked reduction in height (Petro et al., 2015) or diameter (Zhao et al., 2008). This directly affects the production of biomass, and hence the use of wood, in the construction and industrial sectors. Although damage can vary based on eucalypt species or hybrid (Zhao et al., 2008; Nyeko et al., 2009), the greatest impact occurs when plantations are reliant on a single species or few clones, for which effects could be devastating, causing death of whole nurseries or young plantations (Thu et al., 2009).

L. invasa’s economic impact has not been quantified, but it must take into account the economic value of Eucalyptus plantations, which represent one of the most important economic resources in the world (for pulp and fuelwood) (Paine et al., 2011). Indeed, planted areas of eucalypts outside their native range reach nearly 20 million hectares, with Brazil (almost 5.6 million ha), India (almost 4 million ha) and China (2.5 million ha) being the main growers in the world (Brockerhoff et al., 2013IBÁ, 2015). In addition to biomass loss, a possible economic impact needs to take into account the positive contribution of eucalypts to restoration and habitat improvement (control of soil erosion or as windbreak), its beneficial contribution to human health (reducing malaria incidence by draining soils and via extraction of essential oils) and its contribution to beekeepers production.

Risk and Impact Factors

Top of page Invasiveness
  • Proved invasive outside its native range
  • Highly adaptable to different environments
  • Is a habitat generalist
  • Capable of securing and ingesting a wide range of food
  • Has high reproductive potential
  • Gregarious
  • Has propagules that can remain viable for more than one year
  • Reproduces asexually
Impact outcomes
  • Damaged ecosystem services
  • Ecosystem change/ habitat alteration
  • Host damage
  • Loss of medicinal resources
  • Negatively impacts forestry
  • Negatively impacts livelihoods
  • Damages animal/plant products
Impact mechanisms
  • Competition - monopolizing resources
Likelihood of entry/control
  • Highly likely to be transported internationally accidentally
  • Difficult to identify/detect as a commodity contaminant
  • Difficult/costly to control

Similarities to Other Species/Conditions

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The genus Leptocybe (where L. invasa is the unique species) did not exist until 2004, which caused some authors to misidenty L. invasa as Aprostocetus sp. based on the Tetrastichinae key (Viggiani et al., 2002). L. invasa is distinguished from the other Tetrastichinae by the presence of a weakened area on the vertex behind the ocelli. It can be distinguished from Aprostocetus by several characters that are in common with Baryscapus. Characters useful in distinguishing L. invasa from Baryscapus and Oncastichus (as reported in Mendel et al., 2004) are the following:

- L. invasa vs Baryscapus: propodeum with a raised lobe of the callus that partially overhangs the outer rim of the spiracle; spiracular depression open to anterior margin of propodeum; mesoscutum with a single row of 2-3 adnotaular short, weak setae.

- L. invasa vs Oncastichus: postmarginal vein less than 0.25 the length of the stigmal vein; scape not reaching upper margin of vertex.

First and second stages of L. invasa galls could be confused with early stages of Ophelimus maskelli galls, but while L. invasa makes bump-shaped galls on petioles, leaf midribs and young branches (Zheng et al., 2014), O. maskelli induces blister-like galls on the leaf’s surface (Burks et al., 2015). Similar blister-like galls are also induced by Epichrysocharis burwelli, but this species current distribution range includes the USA, Brazil and Portugal and its main host is Corymbia citriodora (Schauff and Garrison, 2000; Franco et al., 2016; Schnell e Schühli et al., 2016). Selitrichodes globulus also causes multilocular galls that hang from branches and twigs of the host (La Salle et al., 2009).

Prevention and Control

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Prevention

Because the blue gum chalcid has already spread to all continents, it is too late to implement preventive measures that can effectively avoid its introduction to new large areas. Nevertheless, introduction to new countries can perhaps be prevented by using detection protocols that provide accurate examination of leaves, petioles and twigs when searching for galls and by adopting quarantine measures that allow development of visible stages of symptoms and consequent detection of the pest. In addition, avoiding movement of infested plants or seedlings could prevent further spread from a plantation to another, especially in areas where L. invasa is not totally widespread.

Control

Physical/mechanical control

Physical control has been suggested during the early stage attack of the blue gum chalcid only. Indeed, removing and destroying infested material could decrease L. invasa populations. However, this method is not efficient for late and/or high infestations, because it is arduous, or even impossible, to remove all infested material. Furthermore, due to the overlapping generations of L. invasa in the field, removal of the attached material would be practically incessant (ICFR, 2011).

Biological control

Biological control seems to be the most promising solution for L. invasa’s control. Different species of parasitoids have been found and studied since the first finding of the blue gum chalcid.

Quadrastichus mendeli - The best performing parasitoid against L. invasa which, from 2007, has been released in Israel, Kenya and India as part of classical biological control programs (Kim et al., 2008; Shylesha, 2008; K.E. Mutitu, pers. comm.). In Israel, percentage of parasitism of L. invasa by Q. mendeli reached 73%, and its spread and establishment were confirmed by its retrieval in all sampled sites (Kim et al., 2008). In contrast, Q. mendeli did not express any control action against L. invasa in Kenya (Dittrich-Schröder et al., 2012) while, from preliminary studies, a reduction in gall infestation in nurseries has recently emerged in India (Jacob et al., 2015). In Italy, Q. mendeli was never officially released but, from 2013, specimens were collected from galls of L. invasa on Eucalyptus camaldulensis and subsequent surveys showed its spread in Central and Southern Italy (including in Sicily). In Italy, the highest mean percentage of parasitisation reached 50.5 ± 6.16%, while the lowest percentage was 30.2 ± 8.10%. However, its effective control action against the blue gum chalcid was shown both by the 100% parasitisation percentage reached in the Southeast coast and the complete disappearance of L. invasa galls from Portici (Southwest Italy) soon after the first record of the parasitoid (Nugnes et al., 2016).

Selitrichodes neseri - This eulophid wasp was originally collected in Queensland (Australia) in 2010 (Kelly et al., 2012). It has been reared in quarantine in South Africa, where its nominal parasitism rate ranged from 9.7 to 71.8% and where it was shown to be specific for L. invasa, when tested on 17 possible non-target hosts from South Africa (Dittrich-Schröder et al., 2014). In 2012, it was released in fields in South Africa and some adults emerged in subsequent sampling sessions (Hurley, 2012). Preliminary laboratory and field studies about the efficiency of S. neseri were carried out in Brazil, showing a higher index of population growth in the fields than in laboratory (De Souza, 2016).

Selitrichodes kryceri - This biparental parasitoid was introduced to Israel as part of a biological control program and its percentage of parasitism of L. invasa reached 52% (Kim et al., 2008). It has been released in India (Shylesha, 2008) and South Africa too (ICFR, 2011). Detailed descriptive and biological features of the species are available in Kim et al. (2008).

Aprostocetus causalis - Firstly identified as A. gala in India (Kavitha Kumari, 2009; Vastrad et al., 2009), but a subsequent identification clarified its species status (Yang et al., 2014). Its control activity was tested in 2010 in greenhouses, confirming its effectiveness (Vastrad and Ramanagouda, 2014).

Megastigmus dharwadicus - Although it was found in a survey in India in 2008 as the most dominant parasitoid on L. invasa galls (90.7%) (Vastrad et al., 2009), it was described for the first time in 2010 (Narendran et al., 2010).

Megastigmus thitipornae - Although its life cycle is shorter than that of the blue gum chalcid, a preliminary study carried out in Thailand demonstrated its scarce parasitism capacity due to its low potential and realized fecundities, and its male-biased sex ratio (Sangtongpraow and Charernsom, 2013).

Megastigmus leptocybus - Reared from galls of L. invasa on E. camaldulensis from Israel, Turkey and Italy (Doganlar and Hassan, 2010; Doganlar, 2015).

Megastigmus zebrinus - Reared from 2010 from galls of L. invasa in South Africa (Kelly et al., 2012).

Megastigmus zvimendeli - Found in 2010 in Queensland (Australia) and then introduced to Israel and Turkey (Doganlar, 2015).

Megastigmus viggianii - Reported for the first time in India on leaf galls of the blue gum chalcid (Gupta and Poorani, 2008), with a percentage of parasitisation almost reaching 25% in China (Zheng et al., 2016).

Megastigmus brasiliensis - Its behaviour is considered parasitic against the blue gum chalcid because of the findings of adults in stems and leaves of eucalypts infested by L. invasa (Doganlar et al., 2013).

Parallelaptera sp. [Erythmelus sp.] (Mymaridae) and Telenomus sp. (Platygastridae) - Found once in India, but their role in the control of the blue gum chalcid is not clarified yet (Vastrad et al., 2009). Based on species from the same families, these two parasitoids should be oophagous, and gall wasps are usually not included among the hosts of Telenomus spp. (Viggiani, 1997), while Erythmelus spp. are usually parasitoids of Hemiptera eggs (Triapitsyn et al., 2007).

Chemical control

Chemical control is probably not feasible both in large plantations and natural environments, but may be possible in nurseries and seedlings (EPPO, 2006). However, because L. invasa completes its life cycle inside a gall, chemical control could be ineffective (Maged, 2016) or effective only with systemic insecticides. The use of systemic insecticides has been tested in different studies and results are very variable depending on eucalypt species and environments (Basavana Goud et al., 2010Javaregowda et al., 2010; Jhala et al., 2010; Kulkarni, 2010; Nyeko et al., 2010Vastrad et al., 2011; Cegatta and Villegas, 2013; Chakrabarti, 2015). Furthermore, their use would be too expensive and dangerous towards its natural enemies (both of the blue gum chalcid and of other eucalypt pests), so it is not considered a practicable option for large plantations of Eucalyptus spp.

Host resistance

There seem to be differences in the efficiency of insecticides and of natural enemies, probably associated to environmental factors or to the existence of two L. invasa lineages. Numerous studies have highlighted the susceptibility, resistance or tolerance of eucalypt species (including hybrids and clones) to L. invasa attack (Nyeko, 2005; Thu et al., 2009; Basavana Goud et al., 2010; Javaregowda et al., 2010; Dittrich-Schröder et al., 2012; Zhang et al., 2012; Chen et al., 2015; Jacob et al., 2015). Differences in chemical, structural and nutritional characteristics could clarify the mechanisms ruling the resistance or susceptibility of the hosts (Nyeko et al., 2010; Oates et al., 2015).

References

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Aquino DA, Botto E, Loiacono MS, Pathauer P, 2011. [English title not available]. ("Avispa de la agalla del eucalipto", Leptocybe invasa Fischer & La Salle (Hymenoptera: Eulophidae: Tetrastichinae), en Argentina). Revista de Investigaciones Agropecuarias, 37(2), 159-164.

Aytar F, 2003. Natural biology, distribution and control method of Leptocybe invasa Fisher & La Salle (Hym., Eulophidae), Eucalyptus gall wasp in Turkey. Journal of DOA, 9, 47-66.

Bain J, 2011. Leptocybe invasa, a gall forming wasp on eucalyptus, not in New Zealand. In: Forest Health News 217 . https://www.scionresearch.com/__data/assets/pdf_file/0008/35396/FHNews-217_July2011.pdf

Basavana Goud, K., Kumari, N. K., Vastrad, A. S., Maheshwari Bhadragoudar, Harish Kulkarni, 2010. Screening of eucalyptus genotypes against gall wasp, Leptocybe invasa Fisher and La Salle (Hymenoptera: Eulophidae). Karnataka Journal of Agricultural Sciences, 23(1), 213-214.

Bella S, 2014. Invasive insect pests and their associated parasitoids on ornamental urban plants on Corfu island - Phytoliriomyza jacarandae Steyskal and Spencer 1978 (Diptera, Agromyzidae) a new record in Greece. Hellenic Plant Protection Journal, 7(2):53-59. http://en.bpi.gr/files/journal/2014/July/VOLUME%207%20-%20ISSUE%202%20(July%202014).pdf

Benítez Díaz EA, Costa VA, de Moraes GJ, Godziewsky D, 2014. First record of Leptocybe invasa Fisher & La Salle (Hymenoptera: Eulophidae) and Rhombacus eucalypti Ghosh & Chakrabarti (Acari: Eriophyidae) from Paraguay. Boletín del Museo Nacional de Historia Natural de Paraguay, 18, 129-132.

Branco, M., Franco, J. C., Valente, C., Mendel, Z., 2006. Survey of Eucalyptus gall wasps (Hymenoptera: Eulophidae) in Portugal. Boletín de Sanidad Vegetal, Plagas, 32(2), 199-202.

Brockerhoff, E. G., Jactel, H., Parrotta, J. A., Ferraz, S. F. B., 2013. Role of eucalypt and other planted forests in biodiversity conservation and the provision of biodiversity-related ecosystem services. Forest Ecology and Management, 301, 43-50. http://www.sciencedirect.com/science/article/pii/S037811271200552X doi: 10.1016/j.foreco.2012.09.018

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Links to Websites

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WebsiteURLComment
Consorcio Protecciòn Fitosanitaria Forestalhttp://www.cpf.cl/
Forestry Research Institute of Malawihttp://www.sdnp.org.mw/frim/
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.
Indústria Brasileira de Árvoreshttp//iba.org/pt/

Principal Source

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Draft datasheet under review

Contributors

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18/01/17 Original text by:

Francesco Nugnes, Consiglio Nazionale delle Ricerche, Istituto per la Protezione Sostenibile delle Piante, Italy

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