Leptocybe invasa
(blue gum chalcid)

Pictures

Picture	Title	Caption	Copyright
Title Female Caption Leptocybe invasa (blue gum chalcid): female. Copyright ©Francesco Nugnes	Female	Leptocybe invasa (blue gum chalcid): female.	©Francesco Nugnes
Title Male Caption Leptocybe invasa (blue gum chalcid): male. Copyright ©Francesco Nugnes	Male	Leptocybe invasa (blue gum chalcid): male.	©Francesco Nugnes
Title Galls Caption Leptocybe invasa (blue gum chalcid); petioles of Eucalyptus sp. with galls. Italy. August 2015. Copyright ©Francesco Nugnes	Galls	Leptocybe invasa (blue gum chalcid); petioles of Eucalyptus sp. with galls. Italy. August 2015.	©Francesco Nugnes
Title Galls Caption Leptocybe 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	Galls	Leptocybe 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
Title Galls Caption Leptocybe invasa (blue gum chalcid); galls on Eucalyptus. Lesbos, Greece. October 2012. Copyright Public Domain - Released Bj.schoenmakers/via wikipedia - CC0 1.0	Galls	Leptocybe invasa (blue gum chalcid); galls on Eucalyptus. Lesbos, Greece. October 2012.	Public Domain - Released Bj.schoenmakers/via wikipedia - CC0 1.0
Title Galls Caption Leptocybe invasa (blue gum chalcid); leaf of Eucalyptus with mature galls along the midrib. Italy. May 2011. Copyright ©Francesco Nugnes	Galls	Leptocybe invasa (blue gum chalcid); leaf of Eucalyptus with mature galls along the midrib. Italy. May 2011.	©Francesco Nugnes
Title Galls Caption Leptocybe invasa (blue gum chalcid); close-up of Eucalyptus leaf with mature galls along the midrib. Italy. May 2011. Copyright ©Francesco Nugnes	Galls	Leptocybe invasa (blue gum chalcid); close-up of Eucalyptus leaf with mature galls along the midrib. Italy. May 2011.	©Francesco Nugnes
Title Leaf-curling Caption Leptocybe invasa (blue gum chalcid); leaf-curling caused by the presence of numerous galls on midribs of Eucalyptus sp. Italy. August 2015. Copyright ©Francesco Nugnes	Leaf-curling	Leptocybe invasa (blue gum chalcid); leaf-curling caused by the presence of numerous galls on midribs of Eucalyptus sp. Italy. August 2015.	©Francesco Nugnes
Title Galls Caption Leptocybe invasa (blue gum chalcid); acute attack on stems of Eucalyptus sp. Italy. March 2014. Copyright ©Francesco Nugnes	Galls	Leptocybe invasa (blue gum chalcid); acute attack on stems of Eucalyptus sp. Italy. March 2014.	©Francesco Nugnes
Title Gall Caption Leptocybe invasa (blue gum chalcid); mature gall with exit hole made by emerging adult. Italy. May 2011. Copyright ©Francesco Nugnes	Gall	Leptocybe invasa (blue gum chalcid); mature gall with exit hole made by emerging adult. Italy. May 2011.	©Francesco Nugnes
Title Natural enemy Caption 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. 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	Natural enemy	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.	©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

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

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

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

Notes on Taxonomy and Nomenclature

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

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

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

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.

History of Introduction and Spread

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

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

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

Hosts/Species Affected

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

Growth Stages

Symptoms

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

Biology and Ecology

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

Latitude/Altitude Ranges

Natural enemies

Notes on Natural Enemies

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, 2010; Zaché 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

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

Pathway Vectors

Economic Impact

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., 2013; IBÁ, 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

• 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

• Damaged ecosystem services
• Ecosystem change/ habitat alteration
• Host damage
• Loss of medicinal resources
• Negatively impacts forestry
• Negatively impacts livelihoods
• Damages animal/plant products

• Competition - monopolizing resources

• Highly likely to be transported internationally accidentally
• Difficult to identify/detect as a commodity contaminant
• Difficult/costly to control

Similarities to Other Species/Conditions

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

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., 2010; Javaregowda et al., 2010; Jhala et al., 2010; Kulkarni, 2010; Nyeko et al., 2010; Vastrad 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

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

Burks, R. A., Mottern, J. L., Waterworth, R., Paine, T. D., 2015. First report of the Eucalyptus gall wasp, Ophelimus maskelli (Hymenoptera: Eulophidae), an invasive pest on Eucalyptus, from the Western Hemisphere. Zootaxa, 3926(3), 448-450. http://www.mapress.com/zootaxa/2015/f/zt03926p450.pdf doi: 10.11646/zootaxa.3926.3.10

CABI/EPPO, 2007. Leptocybe invasa. [Distribution map]. Distribution Maps of Plant Pests, No.December. Wallingford, UK: CABI, Map 698

CABI/EPPO, 2016. Leptocybe invasa. [Distribution map]. Distribution Maps of Plant Pests, No.June. Wallingford, UK: CABI, Map 698 (1st revision)

Cegatta IR, Villegas C, 2013. Efficiency of two systemic insecticides to control blue gum chalcid wasp in seedlings of Eucalyptus camaldulensis. (Eficiência de dois inseticidas sistêmicos no controle de Leptocybe invasa em mudas de Eucalyptus camaldulensis). Revista do Instituto Florestal, 25, 215-221.

Chakrabarti S, 2015. Studies on efficacy of some insecticidal molecules against blue gum chalcid, Leptocybe invasa Fisher & La Salle (Hymenoptera: Eulophidae) in Eucalyptus. Current Biotica, 8(4), 428-431. http://www.currentbiotica.com/CB/Journals8-Issue-IV/CB-8-4-Short-notes-6.pdf

Chen HY, Yao JM, Xu ZF, 2009. First description of the male of Leptocybe invasa Fisher & La Salle (Hymenoptera: Eulophidae). China Journal of Environmental Entomology, 31, 285-287.

Chen YS, Liao ZM, Tu XY, 2015. Study on resistance of different Eucalyptus varieties to Leptocybe invasa in southern Jiangxi. Northern Horticulture, 11, 106-109.

Chirinzane, C. J., Souza, M. D. de, Sousa, N. J., Rezende, E. H., Alves, T., Bandeira, R. R., Fernandes, A. dos M., 2014. First report of Leptocybe invasa Fisher and La'Salle (Hymenoptera: Eulophidae) in Mozambique. African Journal of Agricultural Research, 9(49), 3555-3558. http://www.academicjournals.org/article/article1417524576_Chirinzane%20et%20al.pdf

Costa VA, Berti Filho E, Wilcken CF, Stape JL, 2008. Eucalyptus gall wasp, Leptocybe invasa Fisher & La Salle (Hymenoptera: Eulophidae) in Brazil: new forest pest reaches the New World. Revista de Agricultura (Piracicaba), 83, 136-139.

CPF, 2014. Leptocybe invasa (Hym.: Eulophidae). Sección Vigilancia Fitosanitaria Forestal Subdepartamento Sanidad Vegetal. División Protección Agrícola y Forestal. http://www.cpf.cl/pdf/charla.pdf

De Marzo L, 2014. Larval respiratory system analyzed for three eulophids occurring on eucalypts in Southern Italy (Hymenoptera Chalcidoidea). Entomologica, 45, 3-9.

De Souza AR, 2016. [English title not available]. (Aspectos biológicos de Leptocybe invasa (Hymenoptera:Eulophidae) e de seu parasitoide Selitrichodes neseri (Hymenoptera:Eulophidae) e levantamento de vespas galhadoras em florestas de eucalipto na Austrália. DPhil Thesis). São Paulo, Brazil: São Paulo State University.

Dhahri S, Ben Jamaa ML, Lo Verde G, 2010. First record of Leptocybe invasa and Ophelimus maskelli eucalyptus gall wasps in Tunisia. Tunisian Journal of Plant Protection, 5, 229-234.

Dittrich-Schröder G, Wingfield MJ, Hurley B, Neser S, Mendel Z, Slippers B, 2009. The invasive gall-forming wasp Leptocybe invasa (Hymenoptera: Eulophidae) in South Africa. [Proceedings of the 16th Congress of the Entomological Society of Southern Africa, Stellenbosch], Stellenbosch, South Africa: Entomological Society of South Africa. 27.

Dittrich-Schröder, G., Harney, M., Neser, S., Joffe, T., Bush, S., Hurley, B. P., Wingfield, M. J., Slippers, B., 2014. Biology and host preference of Selitrichodes neseri: a potential biological control agent of the Eucalyptus gall wasp, Leptocybe invasa. Biological Control, 78, 33-41. http://www.sciencedirect.com/science/article/pii/S1049964414001431 doi: 10.1016/j.biocontrol.2014.07.004

Dittrich-Schröder, G., Wingfield, M. J., Hurley, B. P., Slippers, B., 2012. Diversity in Eucalyptus susceptibility to the gall-forming wasp Leptocybe invasa. Agricultural and Forest Entomology, 14(4), 419-427. http://onlinelibrary.wiley.com/journal/10.1111/(ISSN)1461-9563 doi: 10.1111/j.1461-9563.2012.00583.x

Doganlar M, 2015. Diagnosis of Megastigmus spp. (Hymenoptera:Torymidae) reared from galls of Leptocybe invasa Fisher & La Salle, 2004 (Hymenoptera:Eulophidae) on Eucalyptus spp. (Myrtaceae), with description of a new species from South Africa. Entomofauna Zeitschrift für Entomologie, 36, 561-580.

Doganlar, M., Hassan, E., 2010. Review of Australian species of Megastigmus (Hymenoptera: Torymidae) associated with Eucalyptus, with descriptions of new species. Australian Journal of Basic and Applied Sciences, 4(10), 5059-5120. http://www.insipub.com/ajbas/2010/5059-5120.pdf

Doganlar, M., Zaché, B., Wilcken, C. F., 2013. A new species of Megastigmus (Hymenoptera: Torymidae: Megastigminae) from Brazil. Florida Entomologist, 96(1), 196-199. http://www.fcla.edu/FlaEnt/ doi: 10.1653/024.096.0126

Doganlar, O., 2005. Occurrence of Leptocybe invasa Fisher & La Salle, 2004 (Hymenoptera: Chalcidoidea) on Eucalyptus camaldulensis in Turkey, with a description of the male sex. Zoology in the Middle East, 35, 112-114.

Doughty, R. W., 2000. The eucalyptus: a natural and commercial history of the gum tree, [ed. by Doughty, R. W.]. Baltimore, USA: Johns Hopkins University Press.xiv + 228 pp.

Eldridge, K., Davidson, J., Harwood, C., Wyk, G. van, 1994. Eucalypt domestication and breeding, Oxford, UK: Clarendon Press.308 pp.

EPPO, 2006. Addition of Leptocybe invasa to the EPPO Alert List. In: EPPO Reporting Service 2006/190 . Paris, France: European Plant Protection Organization.

EPPO, 2012. EPPO Reporting Service. EPPO Reporting Service. Paris, France: EPPO. http://archives.eppo.org/EPPOReporting/Reporting_Archives.htm

EPPO, 2014. PQR database. Paris, France: European and Mediterranean Plant Protection Organization. http://www.eppo.int/DATABASES/pqr/pqr.htm

Eyidozehi, K., Jahedi, A., Rigi, K., Dehvairi, M. A., 2014. Biology, bioecology and behavior eucalyptus gall wasp, Leptocybe invasa Fisher and La Salle (Hymenoptera: Eulophidae) in Golestan Province. International Journal of Agriculture and Crop Sciences (IJACS), 7(9), 595-600. http://ijagcs.com/wp-content/uploads/2014/06/595-600.pdf

FAO, 2012. Forest pest species profiles - Leptocybe invasa, blue gum chalcid. Rome, Italy: Food and Agriculture Organization. http://www.fao.org/forestry/13569-05912e0e2fe9054c3ed4904ae597e3310.pdf

Franco, J. C., Garcia, A., Branco, M., 2016. First report of Epichrysocharis burwelli in Europe, a new invasive gall wasp atacking eucalypts. Phytoparasitica, 44(4), 443-446. http://rd.springer.com/article/10.1007/s12600-016-0539-9 doi: 10.1007/s12600-016-0539-9

FRIM, 2010. Biodiversity in Malawi. Malawi: Forestry Research Institute of Malawi. http://www.sdnp.org.mw/frim/index.html

Giliomee, J. H., 2011. Recent establishment of many alien insects in South Africa - a cause for concern. African Entomology, 19(1), 151-155. http://journals.sabinet.co.za/essa doi: 10.4001/003.019.0105

Gupta A, Poorani J, 2008. New distribution and host records of Chalcidoidea (Insecta: Hymenoptera) from various parts of India. Check List, 4(4), 410-414.

Gupta A, Poorani J, 2009. Taxonomic studies on a collection of Chalcidoidea (Hymenoptera) from India with new distribution records. Journal of Threatened Taxa, 1(5), 300-304. http://www.threatenedtaxa.org/showAbstract.asp

Han PengFei, Wu JianHui, Qiu BaoLi, Ren ShunXiang, 2012. Extreme low temperature tolerance of Leptocybe invasa. Chinese Journal of Applied Entomology, 49(6), 1553-1558.

Hassan, F. R., 2012. First record of the eucalyptus gall wasp, Leptocybe invasa fisher and la salle (Hymenoptera: Eulophidae), in Iraq. Acta Agrobotanica, 65(3), 93-98. http://www.ib-pan.krakow.pl/ibwyd/obce/ptb-actaagr.html

Hesami, S., Alemansoor, H., Seyedebrahimi, S., 2005. Report of Leptocybe invasa (Hym.: Eulophidae), gall wasp of Eucalyptus camaldulensis with notes on biology in Shiraz vicinity. Journal of Entomological Society of Iran, 24(2), 99-108.

Hill, K. D., Johnson, L. A. S., 2000. Systematic studies in the eucalypts. 10. New tropical and subtropical eucalypts from Australia and New Guinea (Eucalyptus, Myrtaceae). Telopea, 8(4), 503-539.

Hurley B, 2012. First discovery of Selitrichodes neseri in the field. Johannesburg, South Africa: Forestry South Africa. http://www.forestry.co.za/first-discovery-of-selitrichodes-neseri-in-the-field/

IBÁ, 2015. Brazilian Tree Industry. (Indústria Brasileira de Árvores). Report 2015. http://iba.org/images/shared/iba_2015.pdf

ICFR, 2011. Leptocybe invasa, the blue gum chalcid wasp (Information Sheet 01/ 2011). South Africa: Institute for Commercial Forestry Research and Forestry and Agricultural Biotechnology Institute. http://www.forestry.co.za/uploads/File/home/notices/2011/ICFR%20IS01-2011gallwasp.pdf

IPPC, 2012. Occurrence of eucalyptus gall wasp Leptocybe invasa in Mozambique. Rome, Italy: International Plant Protection Convention, Food and Agriculture Organization. https://www.ippc.int/en/countries/mozambique/pestreports/2012/02/occurence-of-eucalyptus-gall-wasp-leptocybe-invasa-in-mozambique/

Jacob JP, Devaraj R, Natarajan R, 2007. Outbreak of the invasive gall inducing wasp Leptocybe invasa on eucalypts in India. Newsletter of the Asia-Pacific Forest Invasive Species Network, 8, 4-5.

Jacob PJ, Ramesh KA, 2009. Incidence of galls induced by Leptocybe invasa (Hymenoptera:Eulophidae) on seedlings of Eucalyptus camaldulensis and E. tereticornis (Myrtaceae) from different seed sources in Southern India. International Journal of Ecology and Environmental Sciences, 35, 187-198.

Jacob, J. P., Senthil, K., Sivakumar, V., Seenivasan, R., Chezhian, P., Kumar, N. K., 2015. Gall wasp Leptocybe invasa (Hymenoptera: Eulophidae) management in Eucalypts. Journal of Biological Control, 29(1), 20-24. http://journalofbiologicalcontrol.com/index.php/jbc/article/view/75789/59037

Javaregowda, J., Prabhu, S. T., Patil, R. S., 2010. Evaluation of botanicals and synthetic insecticides against eucalyptus gall wasp, Leptocybe invasa (Eulophidae: Hymenoptera). Karnataka Journal of Agricultural Sciences, 23(1), 200-202.

Jhala, R. C., Patel, M. G., Vaghela, N. M., 2010. Effectiveness of insecticides against blue gum chalcid, Leptocybe invasa Fisher & La Salle (Hymenoptera: Eulophidae), infesting eucalyptus seedlings in middle Gujarat, India. Karnataka Journal of Agricultural Sciences, 23(1), 84-86.

Jorge C, Martínez G, Gómez D, Bollazzi M, 2016. First record of the eucalypt gall-wasp Leptocybe invasa (Hymenoptera: Eulophidae) from Uruguay. Bosque, 37(3):631-636. http://mingaonline.uach.cl/scielo.php?script=sci_issues&pid=0717-9200&lng=es&nrm=iso

Karunaratne, W. A. I. P., Edirisinghe, J. P., Ranawana, K. B., 2010. Rapid survey of damage due to gall wasp infestation in a coppiced eucalyptus camaldulensis plantation in Maragamuwa, Naula in the Matale district of Sri Lanka. Ceylon Journal of Science, Biological Sciences, 39(2), 157-161. http://www.sljol.info/

Kavitha Kumari N, 2009. Bioecology and management of Eucalyptus gall wasp, Leptocybe invasa Fisher & La Salle (Hymenoptera: Eulophidae). MPhil Thesis. Dharwad, India: University of Agricultural Sciences.

Kavitha Kumari, N., Harish Kulkarni, Vastrad, A. S., Goud, K. B., 2010. Biology of eucalyptus gall wasp, Leptocybe invasa Fisher and La Salle (Hymenoptera: Eulophidae). Karnataka Journal of Agricultural Sciences, 23(1), 211-212.

Kelly J, Salle Jla, Harney M, Dittrich-Schröder G, Hurley B, 2012. Selitrichodes neseri n. sp., a new parasitoid of the eucalyptus gall wasp Leptocybe invasa Fisher & La Salle (Hymenoptera: Eulophidae: Tetrastichinae). Zootaxa, 3333:50. http://www.mapress.com/zootaxa/2012/f/z03333p057f.pdf

Kim IK, Mendel Z, Protasov A, Blumberg D, La Salle J, 2008. Taxonomy, biology, and efficacy of two Australian parasitoids of the Eucalyptus gall wasp, Leptocybe invasa Fisher & La Salle (Hymenoptera: Eulophidae: Tetrastichinae). Zootaxa, 1910, 1-20.

Kulkarni H, 2010. Distribution, seasonal incidence and management of Eucalyptus gall wasp, Leptocybe invasa Fisher & La Salle (Hymenoptera: Eulophidae) with special reference to native parasitoids. MPhil Thesis. Dharwad, India: University of Agricultural Sciences.

Kumar, A., Sangha, K. S., Dhillon, G. P. S., 2015. Screening of 19 genotypes of Eucalyptus spp. against gall wasp (Leptocybe invasa) in North-western India. Journal of Forestry Research, 26(2), 355-359. http://rd.springer.com/journal/11676 doi: 10.1007/s11676-015-0052-x

Kumar, S., Sharma, S. K., Tarun Kant, Emmanuel, C. J. S. K., 2007. Emergence of gall inducing insect Leptocybe invasa (Hymenoptera: Eulophidae) in Eucalyptus plantations in Gujarat, India. Indian Forester, 133(11), 1566-1568. http://www.indianforester.org

La Salle J, Arakelian G, Garrison RW, Gates MW, 2009. A new species of invasive gall wasp (Hymenoptera: Eulophidae: Tetrastichinae) on blue gum (Eucalyptus globulus) in California. Zootaxa, 2121, 35-43.

Lawson S, Griffiths M, Nahrung H, Noack A, Wingfield M, Wilcken C, et al., 2012. Biological control of eucalypt pests overseas and in Australia. Final report for project FST/2011/028. Canberra, Australia: Australian Centre for International Agricultural Research (ACIAR). 40 pp.

Liang Y, Jiyue LI, Xiujun W, Zuozhen LI, 2010. Observation on the male ratio of Leptocybe invasa adult. Forest Pest and Disease, 2010-05, 21-22.

Maged MES, 2016. The interaction between the gall wasp Leptocybe invasa and Eucalyptus camaldulensis leaves: a study of phyto-volatile metabolites. Journal of Pharmacognosy and Phytotherapy, 8(4), 90-98.

Mendel, Z., Protasov, A., Fisher, N., Salle, J. la, 2004. Taxonomy and biology of Leptocybe invasa gen. & sp. n. (Hymenoptera: Eulophidae), an invasive gall inducer on Eucalyptus. Australian Journal of Entomology, 43(2), 101-113. http://blackwell publishing.com/journals/aen doi: 10.1111/j.1440-6055.2003.00393.x

Mifsud D, 2012. Leptocybe invasa Fisher & La Salle, 2004 and Ophelimus maskelli Haliday, 1844 two new records of gall forming Eulophidae from Malta (Hymenoptera, Chalcidoidea). Bulletin of Entomological Society of Malta, 5, 189-193.

Mutitu KE, 2003. A pest threat to Eucalyptus species in Kenya. KEFRI Technical Report. p. 12.

Narendran, T. C., 2007. Indian chalcidoid parasitoids of the Tetrastichinae (Hymenoptera: Eulophidae). Occasional Paper - Records of the Zoological Survey of India, (No.272), 386 pp.

Narendran, T. C., Kumar, P. G., Vastrad, A. S., 2010. Two new species of Megastigmus Dalman (Hymenoptera: Torymidae) from India, with a revised key to Indian species. Records of the Zoological Survey of India, 110(2), 1-6.

Nugnes, F., Gebiola, M., Gualtieri, L., Russo, E., Sasso, R., Bernardo, U., 2016. When exotic biocontrol agents travel without passport: first record of Quadrastichus mendeli, parasitoid of the blue-gum chalcid Leptocybe invasa, in Italy. Bulletin of Insectology, 69(1), 85-91. http://www.bulletinofinsectology.org/

Nugnes, F., Gebiola, M., Monti, M. M., Gualtieri, L., Giorgini, M., Wang JianGuo, Bernardo, U., 2015. Genetic diversity of the invasive gall wasp Leptocybe invasa (Hymenoptera: Eulophidae) and of its Rickettsia endosymbiont, and associated sex-ratio differences. PLoS ONE, 10(5), e0124660. http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0124660 doi: 10.1371/journal.pone.0124660

Nyeko P, 2005. The cause, incidence and severity of a new gall damage on Eucalyptus species at Oruchinga refugee settlement in Mbarara district, Uganda. Uganda Journal of Agricultural Sciences, 11, 47-50.

Nyeko, P., Mutitu, E. K., Day, R. K., 2009. Eucalyptus infestation by Leptocybe invasa in Uganda. African Journal of Ecology, 47(3), 299-307. http://www.blackwell-synergy.com/loi/aje doi: 10.1111/j.1365-2028.2008.01004.x

Nyeko, P., Mutitu, K. E., Otieno, B. O., Ngae, G. N., Day, R. K., 2010. Variations in Leptocybe invasa (Hymenoptera: Eulophidae) population intensity and infestation on eucalyptus germplasms in Uganda and Kenya. International Journal of Pest Management, 56(2), 137-144. http://www.informaworld.com/smpp/775487670-88741131/content˜db=all˜content=a920328188 doi: 10.1080/09670870903248835

Oates, C. N., Külheim, C., Myburg, A. A., Slippers, B., Naidoo, S., 2015. The transcriptome and terpene profile of Eucalyptus grandis reveals mechanisms of defense against the insect pest, Leptocybe invasa. Plant and Cell Physiology, 56(7), 1418-1428. http://pcp.oxfordjournals.org/content/56/7/1418.full doi: 10.1093/pcp/pcv064

Paine, T. D., Steinbauer, M. J., Lawson, S. A., 2011. Native and exotic pests of Eucalyptus: a worldwide perspective. Annual Review of Entomology, 56, 181-201. http://www.annualreviews.org/doi/abs/10.1146/annurev-ento-120709-144817 doi: 10.1146/annurev-ento-120709-144817

Pereira JM, Melo APCde, Rodrigues OD, Dias TKR, Wilcken CF, 2014. Record of the Leptocybe invasa in the state Goiás, Brazil. (Registro de Leptocybe invasa no estado de Goiás.) Ciência Rural, 44(10):1721-1724. http://www.scielo.br/pdf/cr/v44n10/0103-8478-cr-44-10-01721.pdf

Petro, R., Madoffe, S. S., Iddi, S., Mugasha, W. A., 2015. Impact of Eucalyptus gall wasp, Leptocybe invasa infestation on growth and biomass production of Eucalyptus grandis and E. saligna seedlings in Tanzania. International Journal of Pest Management, 61(3), 220-227. http://www.tandfonline.com/loi/ttpm20 doi: 10.1080/09670874.2015.1039096

Protasov, A., Doganlar, M., La Salle, J., Mendel, Z., 2008. Occurrence of two local Megastigmus species parasitic on the eucalyptus gall wasp Leptocybe invasa in Israel and Turkey. Phytoparasitica, 36(5), 449-459. http://www.phytoparasitica.org

Pujade-Villar, J., Riba-Flinch, J. M., 2004. Two Australian eulophids, very harmful to Eucalyptus spp., introduced into the north-east of the Iberian Peninsula (Hymenoptera: Eulophidae). (Dos especies australianas de eulófidos, muy dañinas para Eucalyptus spp., introducidas en el nordeste ibérico (Hymenoptera: Eulophidae)). Boletin de la S.E.A, (No.35), 299-301.

Puretz BO, Potrich M, Miranda FDA, Lozano ER, Freddo Á, 2015. Distribution of eucalyptus gall wasp. (Distribuição da vespa da galha do eucalipto.) Pesquisa Florestal Brasileira, 35(83):329-334. http://pfb.cnpf.embrapa.br/pfb/index.php/pfb/article/view/776/442

Qiu HX, Xu JX, Lin MS, 2011. Study on the biology and effective accumulated temperature by Leptocybe invasa at Eucalyptus. Guangdong Forestry Science and Technology, 27, 1-5.

Ramanagouda, S. H., Vastrad, A. S., Narendran, T. C., Basavanagoud, K., Viraktamath Shashidhar, 2011. Current status of eucalyptus gall wasp and its native parasitoids in Karnataka. Journal of Biological Control, 25(3), 193-197. http://journalofbiologicalcontrol.com/index.php/jbc/article/view/40014/36935

Rolim GS, Almeida TS, Poderoso JCM, Chagas TX, Ribeiro GT, 2014. First record of Leptocybe invasa in Eucalyptus spp. (Myrtaceae) in the state of Sergipe. (Primeiro registro de Leptocybe invasa em Eucalyptus spp. (Myrtaceae) no estado de Sergipe). In: XXV Congresso Brasileiro de Entomologia, Goiânia, Brasil, 14-18 September 2014 . https://issuu.com/ericdamascenokaji/docs/xxv_cbe_miolo_final

Roux J, 2005. Pest alert - Blue gum chalcid. Tree Protection News, 10, 13. https://www.fabinet.up.ac.za/tpcp/newsletters/TPCP_Newsletter_Nov_2005.pdf

Sambaraju K, DesRochers P, Rioux D, Boulanger Y, Kulkarni N, Verma RK, Pautasso M, et al., 2015. Forest ecosystem health and biotic disturbances: perspectives on indicators and management approaches. In: Ecological forest management handbook, [ed. by Larocque GR]. London, UK: CRC Press.

Sánchez I, 2003. Two new eucalypt pests found in Spain. (Descubiertas dos nuevas plagas del eucalipto en España). Quercus, 214, 32-33.

Sangha KS, Dhillon GPS, Kumar V, 2011. Leptocybe invasa (Hymenoptera: Eulophidae), an invasive gall inducer of Eucalyptus in Punjab. In: Extended Abstracts of the 3rd Congress on Insect Science [Pest management for food security and environment health], [ed. by Dhawan, SDR, Kumar R]. Ludhiana, India: Punjab Agricultural University. p. 32.

Sangtongpraow, B., Charernsom, K., 2013. Evaluation of parasitism capacity of Megastigmus thitipornae Doganlar & Hassan (Hymenoptera: Torymidae), the local parasitoid of eucalyptus gall wasp, Leptocybe invasa Fisher & La Salle (Hymenoptera: Eulophidae). Kasetsart Journal, Natural Science , 47(2), 191-204. http://kasetsartjournal.ku.ac.th/

Sangtongpraow, B., Charernsom, K., Siripatanadilok, S., 2011. Longevity, fecundity and development time of eucalyptus gall wasp, Leptocybe invasa Fisher & La Salle (Hymenoptera: Eulophidae) in Kanchanaburi province, Thailand. Thai Journal of Agricultural Science, 44(3), 155-163. http://www.thaiagj.org/images/stories/Journal_online/2011/3/2-155-163-19.pdf

Schauff, M. E., Garrison, R., 2000. An introduced species of Epichrysocharis (Hymenoptera: Eulophidae) producing galls on Eucalyptus in California with notes on the described species and placement of the genus. Journal of Hymenoptera Research, 9(1), 176-181.

Schnell e Schühli, G., Penteado, S. C., Barbosa, L. R., Reis Filho, W., Iede, E. T., 2016. A review of the introduced forest pests in Brazil. Pesquisa Agropecuária Brasileira, 51(5), 397-406. http://seer.sct.embrapa.br/index.php/pab doi: 10.1590/S0100-204X2016000500001

Shylesha AN, 2008. Classical biological control of Eucalyptus gall wasp Leptocybe invasa Fisher & La Salle. Final Project report on the management of emerging pests Eucalyptus. Bangalore, India: National Bureau of Agriculturally Important Insects. http://www.dcpulppaper.org/gifs/report63.pdf

Tang Chao, Wan XiaoJun, Wan FangHao, Ren ShunXiang, Peng ZhengQiang, 2008. The blue gum chalcid, Leptocybe invasa, invaded Hainan province. Chinese Bulletin of Entomology, 45(6), 967-971.

Thu PQ, 2004. The first record of gall forming wasp associated with eucalypt plantations in Vietnam. Science and Technological Journal of Agriculture and Rural Development, 11, 1598-1599.

Thu PQ, Dell B, Burgess TI, 2009. Susceptibility of 18 eucalypt species to the gall wasp Leptocybe invasa in the nursery and young plantations in Vietnam. Science Asia, 35, 113-117.

Triapitsyn SV, Berezovskiy VV, Hoddle MS, Morse JG, 2007. A review of the Nearctic species of Erythmelus (Hymenoptera: Mymaridae), with a key and new additions to the New World fauna. Zootaxa, 1641, 1-64.

Tung GS, La Salle J, 2010. Pest alert - a newly discovered invasion of gall-forming wasps, Leptocybe invasa (Fisher & La Salle), on eucalyptus trees in Taiwan. Formosan Entomologist, 30, 241-244.

Udagedara, U. K. S. K., Karunaratne, W. A. I. P., 2014. Biology, damage and parasitoids of the Eucalyptus gall wasp, Leptocybe invasa (Hymenoptera: Eulophidae), infesting Eucalyptus camaldulensis (Myrtaceae) in Maragamuwa plantation, Sri Lanka. International Journal of Tropical Insect Science, 34(3), 179-189. http://journals.cambridge.org/action/displayJournal?jid=JTI

Vanegas-Rico, J. M., Lomeli-Flores, J. R., Rodríguez-Leyva, E., Jiménez-Quiroz, E., Pujade-Villar, J., 2015. First record of eucalyptus gall wasp Leptocybe invasa (Hymenoptera: Eulophidae) in Mexico. Revista Mexicana de Biodiversidad, 86(4), 1095-1098. http://www.ib.unam.mx/revista/ doi: 10.1016/j.rmb.2015.09.012

Vastrad AS, Kavitha Kumari N, Ramanagouda SH, Basavana Goud K, 2011. Management of eucalyptus gall wasp, Leptocybe invasa Fisher & La Salle in greenhouse. Pestology, 35, 44-53.

Vastrad AS, Ramanagouda SH, 2014. Invasive gall wasp (Leptocybe invasa) in eucalypt and its management. In: Eucalypts in India, Edition I, Dehradun, India: Envis Center on Forestry, Forest Research Institute. 346-380.

Vastrad, A. S., Basavanagoud, K., Kumari, N. K., 2009. Native parasitoids of eucalyptus gall wasp, Leptocybe invasa (Fisher & LaSalle) (Eulophidae: Hymenoptera) and implications on the biological control of the pest. Entomon, 34(3), 197-200.

Viggiani G, 1997. [English title not available]. (Lotta biologica e integrata nella difesa fitosanitaria. Vol. 2: Lotta integrata ai fitofagi), Italy: Liguori Ed.460 pp.

Viggiani G, 2015. Description of the final-instar larvae of the gall inducer wasps Aprostocetus monacoi Viggiani and Leptocybe invasa Fisher et La Salle (Hymenoptera, Chalcidoidea: Eulophidae). Entomological Review, 95(4), 447-449.

Viggiani, G., Laudonia, S., Bernardo, U., 2002. The increase of insect pests in Eucalyptus. (Aumentano gli insetti dannosi agli eucalipti). Informatore Agrario, 58(12), 86-87.

Wiley J, Skelley PA, 2008. A eucalyptus pest, Leptocybe invasa Fisher & La Salle (Hymenoptera: Eulophidae), genus and species new to Florida and North America. Pest Alert. Florida, USA: Florida Department of Agriculture and Consumer Services, Division of Plant Industry.http://www.freshfromflorida.com/content/download/68487/1614796/Pest_Alert_- _Leptocybe_invasa,_Blue_Gum_Chalcid.pdf

Wu YJ, Jiang XJ, Li DW, Luo JT, Zhou GF, Chang MS, Yang ZQ, 2009. Leptocybe invasa, a new invasive forest pest making galls on twigs and leaves of eucalyptus trees in China. Scientia Silvae Sinicae, 45, 161-163.

Wylie, F. R., Speight, M., 2012. Insect pests in tropical forestry, (Ed. 2) [ed. by Wylie, F. R., Speight, M.]. Wallingford, UK: CABI.ix + 365 pp. http://www.cabi.org/cabebooks/ebook/20123223688 doi:10.1079/9781845936365.0000

Yang ManMiao, Lin YuChe, Wu YaoJun, Fisher, N., Saimanee, T., Sangtongpraow, B., Zhu ChaoDong, Chiu, C. H. W., La Salle, J., 2014. Two new Aprostocetus species (Hymenoptera: Eulophidae: Tetrastichinae), fortuitous parasitoids of invasive eulophid gall inducers (Tetrastichinae) on Eucalyptus and Erythrina. Zootaxa, 3846(2), 261-272. http://www.mapress.com/zootaxa/2014/f/zt03846p272.pdf doi: 10.11646/zootaxa.3846.2.6

Zaché B, Zaché RRC, Souza NM, Candelaria MC, Barbosa LR, Moio SG, et al., 2012. [English title not available]. (Ocorrência de Megastigmus sp. (Hymenoptera: Torymidae) parasitoide da vespa da galha Leptocybe invasa (Hymenoptera: Eulophidae) no Brasil). In: XXIV Congresso Brasileiro de Entomologia, Curitiba, Brasil, 16-20 September 2012

Zhang HF, Kang WT, Chen SL, Tang XH, Lin XQ, 2012. Study on the relationship between eucalyptus clones and the damage degrees caused by Leptocybe invasa Fisher & La Salle. Journal of Fujian College of Forestry, 32, 345-349.

Zhao DY, Xu JX, Lin MS, Qiu HX, Zhong TK, Chen MR, Huang MY, Chen RP, 2008. Evaluation for the growth loss of eucalyptus caused by Leptocybe invasa. Guangdong Forestry Science and Technology, 24, 58-60.

Zheng XiaLin, Huang ZongYou, Dong Dan, Guo ChunHui, Li Jun, Yang ZhenDe, Yang XiuHao, Lu Wen, 2016. Parasitoids of the eucalyptus gall wasp Leptocybe invasa (Hymenoptera: Eulophidae) in China. Parasite, 23, 58. http://www.parasite-journal.org/articles/parasite/full_html/2016/01/parasite160063/parasite160063.html

Zheng, X. L., Yang, Z. D., Li, J., Xian, Z. H., Yang, J., Liu, J. Y., Su, S., Wang, X. L., Lu, W., 2014. Rapid identification of both sexes of Leptocybe invasa Fisher & La Salle (Hymenoptera: Eulophidae: Tetrastichinae): a morphological perspective. African Entomology, 22(3), 643-650. http://www.bioone.org/doi/full/10.4001/003.022.0326 doi: 10.4001/003.022.0326

Zhu FangLi, Ren ShunXiang, Qiu BaoLi, Huang Zhen, Peng ZhengQiang, 2012. The abundance and population dynamics of Leptocybe invasa (Hymenoptera: Eulophidae) galls on Eucalyptus spp. in China. Journal of Integrative Agriculture, 11(12), 2116-2123. http://www.sciencedirect.com/science/journal/20953119

Zhu FangLi, Ren ShunXiang, Qiu BaoLi, Wu JianHui, 2015. Effect of temperature on life table parameters of Leptocybe invasa (Hymenoptera: Eulophidae). Austral Entomology, 54(1), 71-78. http://onlinelibrary.wiley.com/journal/10.1111/(ISSN)2052-1758

Links to Websites

Principal Source

Draft datasheet under review

Contributors

18/01/17 Original text by:

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

Distribution Maps